Cell Polarization and Cytokinesis in Budding Yeast

Erfei Bi; Hay-Oak Park

doi:10.1534/genetics.111.132886

. 2012 Jun;191(2):347–387. doi: 10.1534/genetics.111.132886

Cell Polarization and Cytokinesis in Budding Yeast

Erfei Bi ^*,¹, Hay-Oak Park ^†

PMCID: PMC3374305 PMID: 22701052

Abstract

Asymmetric cell division, which includes cell polarization and cytokinesis, is essential for generating cell diversity during development. The budding yeast Saccharomyces cerevisiae reproduces by asymmetric cell division, and has thus served as an attractive model for unraveling the general principles of eukaryotic cell polarization and cytokinesis. Polarity development requires G-protein signaling, cytoskeletal polarization, and exocytosis, whereas cytokinesis requires concerted actions of a contractile actomyosin ring and targeted membrane deposition. In this chapter, we discuss the mechanics and spatial control of polarity development and cytokinesis, emphasizing the key concepts, mechanisms, and emerging questions in the field.

Keywords: actomyosin ring; bud-site selection; Cdc42, cytoskeleton; exocytosis

ASYMMETRIC cell division, which is composed of cell polarization and cytokinesis, plays important roles in generating cell diversity during development in plants and animals, as well as in the decision of stem cells to undergo self-renewal vs. differentiation (Knoblich 2010; Paciorek and Bergmann 2010; De Smet and Beeckman 2011). The budding yeast Saccharomyces cerevisiae reproduces by asymmetric cell division and has thus served as an excellent model for studying this fundamental process (Pruyne and Bretscher 2000b; Park and Bi 2007).

Cell polarization, or the formation of distinct cellular domains, is crucial for performing specific functions such as neuronal transmission (Witte and Bradke 2008), ion transport across epithelia (Drubin and Nelson 1996), and pollen tube growth in plants (Kost 2008). Budding yeast undergo pronounced polarized cell growth during three distinct phases: budding, mating, and filamentous growth (Pruyne and Bretscher 2000b; Park and Bi 2007). These polarization events all involve the conserved small GTPase Cdc42, cytoskeletal polarization, and exocytosis. They differ in the instructive cues and spatiotemporal controls. During budding, polarization is induced by the cell-cycle clock and oriented by the bud-site selection program (Pruyne and Bretscher 2000b; Park and Bi 2007). During mating, polarization is induced and oriented by an external gradient of pheromone (Arkowitz 2009; Saito 2010; Waltermann and Klipp 2010). During starvation, polarization is induced by specific nutrient environments (Dickinson 2008; Saito 2010; Waltermann and Klipp 2010) and oriented by a modified version of the bud-site selection program.

Cytokinesis is essential for increasing cell numbers and cell diversity during development (Balasubramanian et al. 2004; Barr and Gruneberg 2007; Pollard 2010). Cytokinesis can be viewed as a specialized form of polarized growth. Both budding and division require polarized actin and exocytosis, but they differ in the temporal controls and the acquisition of an additional actomyosin system for the division process. During budding, the growth machine is directed toward the bud cortex to promote bud growth. Later in the cell cycle, the same growth machine is redirected to the mother-bud neck to promote cytokinesis. Cytokinesis in animal and fungal cells involves spatiotemporally coordinated functions of a contractile actomyosin ring (AMR) and targeted membrane deposition (Balasubramanian et al. 2004; Barr and Gruneberg 2007; Pollard 2010). The AMR is thought to generate a contractile force that powers the ingression of the plasma membrane (PM) and also guides membrane deposition. Targeted vesicle fusion at the division site increases surface area and also delivers enzymes for localized extracellular matrix (ECM) remodeling. Although the core principles and components of cytokinesis are largely conserved from yeast to human, different organisms use different means to specify the division site. In wild-type S. cerevisiae, bud-site selection specifies the site of budding and division. In this chapter, we will discuss the mechanisms of cell polarization during budding and cytokinesis, as well as their spatial control; the temporal control of these morphogenetic events is discussed in the chapter by Howell and Lew (2012) and the polarization mechanisms during mating and starvation are discussed elsewhere (Dickinson 2008; Arkowitz 2009; Saito 2010; Waltermann and Klipp 2010).

Establishment and maintenance of polarized cell growth

Polarization of growth and the cytoskeleton during the cell cycle

S. cerevisiae cells undergo cell-cycle–regulated polarized growth toward a single cortical site, leading to bud emergence and enlargement until telophase when the growth machinery is redirected to the bud neck to promote cytokinesis and cell separation (Figure 1A) (Hartwell 1971b; Pringle and Hartwell 1981). During this process, the mother cell displays little or no change in size. Pulse-chase labeling experiments using fluorophore-conjugated concanavalin A, which binds to cell surface glycoproteins, indicate that new growth is first targeted to the bud tip from late G1 to G2 phases of the cell cycle, an “apical growth” mode that drives cell lengthening, and then targeted to the entire bud upon the entry into mitosis, an “isotropic growth” mode that drives uniform bud expansion (Farkas et al. 1974; Lew and Reed 1993). The relative duration of the two growth modes determines the bud shape, which is normally ovoid. The apical-to-isotropic switch is controlled by Cdk1 (Cdc28)/cyclin complexes.

Cdc42, cell growth, and cytoskeletal polarizations during the cell cycle. (A) Cdc42 (green) localization and the direction of cell growth (arrows) are indicated. (B) Actin organization during the cell cycle. Branched actin filaments in actin patches, nucleated by the Arp2/3 complex, regulate endocytosis. Linear actin cables, nucleated by the formins Bni1 and Bnr1, guide polarized exocytosis. The actin ring, nucleated by the formins (mainly Bni1), is involved in cytokinesis. (C) Septin organization during the cell cycle. Polarized Cdc42 directs septin recruitment to the incipient bud site to form a cortical ring. Upon bud emergence, the septin ring is expanded into an hourglass spanning the entire mother-bud neck. At the onset of cytokinesis, the MEN triggers the splitting of the hourglass into two cortical rings. Modified from (Park and Bi 2007) with permission.

Three cytoskeletal systems are polarized during the yeast cell cycle: actin, septins, and cytoplasmic microtubules (Kaksonen et al. 2006; Moseley and Goode 2006; Moore et al. 2009; Oh and Bi 2011). Filamentous (F) actin structures in yeast include distinct actin cables, actin patches, and the cytokinetic actin ring (Figure 1B) (Pruyne and Bretscher 2000a; Park and Bi 2007). Polarized actin cables act as “tracks” to guide the delivery of secretory vesicles toward the site of growth (Adams and Pringle 1984; Pruyne et al. 1998). Actin patches regulate endocytosis (Kaksonen et al. 2003). The actin ring is involved in cytokinesis (Epp and Chant 1997; Bi et al. 1998; Lippincott and Li 1998a). Septins are assembled into a cortical ring at the incipient bud site, which is expanded into an hourglass structure upon bud emergence (Figure 1C). At the onset of cytokinesis, the septin hourglass is split into two cortical rings that sandwich the cytokinesis machine. The septin rings/hourglass function as a scaffold and/or diffusion barrier to effect bud morphogenesis, cytokinesis, and many other processes (Longtine et al. 1996; Gladfelter et al. 2001; Weirich et al. 2008; McMurray and Thorner 2009; Oh and Bi 2011). Cytoplasmic microtubules, which emanate from the spindle pole body (the yeast counterpart of the animal centrosome), are also polarized during bud emergence and bud growth (Moore et al. 2009). However, disruption of microtubules does not affect polarized growth (Adams and Pringle 1984; Palmer et al. 1992; Sullivan and Huffaker 1992), suggesting that microtubules do not play a major role in this process. Thus, the actin cytoskeleton (especially cables) and the septins are the major determinants of cellular morphogenesis in budding yeast. Here, we discuss the key regulatory molecules and pathways that control the polarized assembly of actin cables and the septin ring.

Cdc42: the center of cell polarization

The small GTPase Cdc42 plays a central role in cell polarity from yeast to humans (Etienne-Manneville 2004; Park and Bi 2007). CDC42 was initially identified as a temperature-sensitive mutant defective in polarized actin organization and cell growth in S. cerevisiae (Adams et al. 1990; Johnson and Pringle 1990). Homologs from other species, including humans, share 80–85% identity in amino acid sequence and functionally complement yeast cdc42 mutants (Johnson and Pringle 1990; Munemitsu et al. 1990; Shinjo et al. 1990; Chen et al. 1993; Luo et al. 1994; Miller and Johnson 1994; Eaton et al. 1995). Thus, Cdc42 is a master regulator of cell polarity.

In response to temporal and spatial signals, Cdc42 in S. cerevisiae becomes polarized at a predetermined cortical site to drive bud growth (Park and Bi 2007). Remarkably, in the absence of any spatial cues, such as in rsr1Δ cells (Bender and Pringle 1989), Cdc42 can still polarize at a random site in the cell cortex and fulfill its essential role in polarized cell growth without evident defects (Irazoqui et al. 2003; Wedlich-Soldner et al. 2003). Thus, yeast cells possess intrinsic mechanisms for “symmetry breaking.” Below, we will first describe the Cdc42 GTPase module and then discuss its functions and mechanisms. All polarity proteins relevant to our discussions are described in Table 1.

Table 1. Proteins involved in polarized cell growth.

Name of protein or protein complex^a	Protein activity	Function^b (mutant phenotypes and/or key protein interactions)	Key references
Cdc42 and its regulators and effectors

Cdc42	Rho-like GTPase	Essential for polarity establishment and maintenance (“Master regulator” of eukaryotic cell polarity)	Adams et al. 1990; Johnson and Pringle 1990; Iwase et al. 2006
		Mutants are defective in polarized actin organization, septin ring assembly, and bud emergence
Cdc24	GEF for Cdc42	Essential for polarity establishment and maintenance Mutants are defective in polarized actin organization, septin ring assembly, bud emergence, and shmoo formation	Sloat and Pringle 1978; Chenevert et al. 1994; Zheng et al. 1994; Shimada et al. 2004; Wiget et al. 2004
Bem2	GAP for Cdc42 and Rho1	Important for polarity establishment and maintenance	Bender and Pringle 1991; Kim et al. 1994; Peterson et al. 1994; Marquitz et al. 2002; Knaus et al. 2007
Bem3	GAP for Cdc42	Important for polarity regulation and septin ring assembly	Bender and Pringle 1991; Zheng et al. 1993; Zheng et al. 1994; Gladfelter et al. 2002; Smith et al. 2002; Caviston et al. 2003; Knaus et al. 2007
Rga1	GAP for Cdc42	Essential for preventing budding or cell polarization within old division sitesImportant for suppressing basal signaling during mating, and septin ring assembly	Stevenson et al. 1995; Chen et al. 1996; Gladfelter et al. 2002; Smith et al. 2002; Caviston et al. 2003; Tong et al. 2007
Rga2	GAP for Cdc42	Important for polarity regulation and septin ring assembly	Gladfelter et al. 2002; Smith et al. 2002; Caviston et al. 2003; Sopko et al. 2007
Rdi1	GDI for Cdc42, Rho1, and Rho4	Important for cycling of Rho GTPases between the cytosol and the PM during cell polarization	Masuda et al. 1994; Koch et al. 1997; Richman et al. 2004; Tcheperegine et al. 2005; Tiedje et al. 2008; Slaughter et al. 2009; Logan et al. 2011
Bem1	Scaffold for GEF-based amplification of Cdc42 activation	Important for polarity establishment during budding and matingForms complex with Cdc24, Cla4, Rsr1 during budding	Bender and Pringle 1989; Bender and Pringle 1991; Chenevert et al. 1992; Leeuw et al. 1995; Park et al. 1997; Gulli et al. 2000; Bose et al. 2001; Irazoqui et al. 2003; Shimada et al. 2004
Cla4	PAK (p21-activated kinase) Effector of Cdc42	Important for septin ring assembly, phosphorylates septins Cdc3 and Cdc10 Important for polarity regulation Down-regulation of sterol uptake	Cvrckova et al. 1995; Benton et al. 1997; Weiss et al. 2000; Caviston et al. 2003; Versele and Thorner 2004; Wild et al. 2004; Kozubowski et al. 2008; Lin et al. 2009
Ste20	PAK Effector of Cdc42	Important for MAPK signaling during pheromone response, pseudohyphal growth, and invasive growth Down-regulation of sterol uptake	Leberer et al. 1992; Ramer and Davis 1993; Peter et al. 1996; Leeuw et al. 1998; Kozubowski et al. 2008; Lin et al. 2009
Skm1	PAK Effector of Cdc42	Down-regulation of sterol uptake Regulate morphogenesis	Martin et al. 1997; Lin et al. 2009

Bni1	Formin, nucleates the assembly of linear actin filaments Effector of Cdc42 and Rho1 Polarisome component	Plays important roles in exocytosis, cytokinesis, spindle orientation, and mating by promoting the assembly of actin cables and actin rings	Kohno et al. 1996; Evangelista et al. 1997; Lee et al. 1999; Miller et al. 1999; Pruyne et al. 2002; Sagot et al. 2002b; Moseley et al. 2004; Moseley and Goode 2005; Moseley and Goode 2006
Gic1	Effector of Cdc42	Shares a role with Gic2 in cytoskeletal polarization and polarized cell growth	Brown et al. 1997; Chen et al. 1997; Iwase et al. 2006
		gic1Δ gic2Δ cells are temperature sensitive for growth
		Interacts with septins
Gic2	Effector of Cdc42	Shares a role with Gic1 in cytoskeletal polarization and polarized cell growth gic1Δ gic2Δ cells are temperature sensitive for growth Interacts with septins Undergoes ubiquitin-mediated degradation by SCF^GRR1	Brown et al. 1997; Chen et al. 1997; Iwase et al. 2006; Jaquenoud et al. 1998

Actin cables, exocytosis, and key regulators

Act1	Actin	Involved in exocytosis, endocytosis, cytokinesis, and many other functions	Engqvist-Goldstein and Drubin 2003; Moseley and Goode 2006; Park and Bi 2007
Bni1	Formin (See above)
Bnr1	Formin, nucleates the assembly of linear actin filaments	Plays an important role in exocytosis by promoting actin cable assembly	Imamura et al. 1997; Pruyne et al. 2002; Sagot et al. 2002b; Moseley et al. 2004; Moseley and Goode 2005; Moseley and Goode 2006
Pfy1	Profilin	Plays a role in actin organization, endocytosis, and exocytosis Binds to monomeric actin, phosphatidylinositol 4,5-bisphosphate, and polyproline regions Catalyzes ADP/ATP exchange on actin monomers	Haarer et al. 1990; Haarer et al. 1996; Moseley and Goode 2006; Sagot et al. 2002b
Bud6	Actin-binding protein Formin-binding protein Polarisome component	Involved in bipolar bud-site selection, actin cable assembly, and polarized cell growth Binds to monomeric actin and Bni1	Amberg et al. 1997; Evangelista et al. 1997; Moseley et al. 2004; Moseley and Goode 2005
Tpm1	Major isoform of tropomyosin	Stabilizes actin filaments in actin cables and actin rings Involved in polarized cell growth and organelle inheritance Binds actin more efficiently upon Tpm1 acetylation by the NatB complex	Liu and Bretscher 1989a; Pruyne et al. 1998; Bretscher 2003; Singer and Shaw 2003
Tpm2	Minor isoform of tropomyosin	Stabilizes actin filaments in actin cables and actin rings Shares an essential role with Tpm1 in polarized cell growth and organelle inheritance Plays a role in morphogenesis that is distinct from Tpm1	Liu and Bretscher 1989a; Drees et al. 1995; Pruyne et al. 1998; Bretscher 2003; Singer and Shaw 2003; Yoshida et al. 2006
Sac6	Fimbrin, an actin-bundling protein	Acts in concert with Scp1 (transgelin-like protein) for the organization and maintenance of the actin cytoskeleton	Adams et al. 1989; Goodman et al. 2003; Winder et al. 2003
Abp140	AdoMet-dependent tRNA methyltransferase and actin-binding protein	Binds actin filaments in actin patches and cables Modifies the anti-codon loop of tRNA-Thr and tRNA-Ser	Asakura et al. 1998; D’Silva et al. 2011; Noma et al. 2011
Ypt31, Ypt32	Rab GTPases	Play important roles in intra-Golgi traffic or vesicle budding from the trans-Golgi	Benli et al. 1996; Jedd et al. 1997;Grosshans et al. 2006
		Share an essential role in the processes mentioned above
Sec4	Rab GTPase	Essential for post-Golgi vesicle transport and tethering Interacts with the exocyst subunit Sec15 to promote exocyst assembly at the PM	Salminen and Novick 1987; Goud et al. 1988; Guo et al. 1999b
Sec2	Rab GEF	Essential for post-Golgi vesicle transport and tethering	Walch-Solimena et al. 1997
		GEF for Sec4
Msb3, Msb4	Rab GAPs Polarisome components	Regulate post-Golgi exocytosis by acting as a GAP for Sec4 Localize to the sites of polarized growth and share a role in exocytosis Multi-copy suppressor of cdc42 and cdc24 mutants Interact with Spa2	Albert and Gallwitz 1999; Bi et al. 2000; Gao et al. 2003; Tcheperegine et al. 2005
Myo2	Myosin-V	Essential for actin-based transport of cargoes (secretory vesicles, vacuoles, late Golgi elements, peroxisomes, and the mitotic spindle)	Johnston et al. 1991; Lillie and Brown 1994; Govindan et al. 1995; Bretscher 2003
Myo4	Myosin-V	Involved in actin-based transport of cargoes (Ash1 mRNA)	Bobola et al. 1996; Estrada et al. 2003
		Cortical ER inheritance
Spa2	Scaffold protein Polarisome component	Interacts with Bud6, Bni1, Pea2, Msb3, and Msb4 Scaffold for the MAPK cell wall integrity pathway Mutants are defective in polarized growth and bipolar budding	Snyder 1989; Sheu et al. 1998; Sheu et al. 2000; van Drogen and Peter 2002; Tcheperegine et al. 2005
Pea2	Polarisome component	Required for efficient mating and bipolar budding Interacts with Spa2, and regulates polarized growth	Chenevert et al. 1994; Valtz and Herskowitz 1996; Sheu et al. 1998
Sec3	Exocyst subunit	Required for the tethering of post-Golgi vesicles to the PM Localizes to the sites of polarized growth and acts a spatial landmark for exocytosis Binds to PIP2 Interacts with Rho1 and Cdc42	TerBush et al. 1996; Finger et al. 1998; Guo et al. 1999a; Guo et al. 2000; Guo et al. 2001; Boyd et al. 2004; Zhang et al. 2001; Zhang et al. 2008; Yamashita et al. 2010
Sec5, Sec6, Sec8, Sec10, Exo84	Exocyst subunits	Required for the tethering of post-Golgi vesicles to the PM	Guo et al. 1999a; TerBush et al. 1996; Guo et al. 2000; Boyd et al. 2004
Sec15	Exocyst subunit	Required for the tethering of post-Golgi vesicles to the PM Interacts with Sec4-GTP and Bem1	Boyd et al. 2004; France et al. 2006; Guo et al. 1999a; Guo et al. 1999b; Guo et al. 2000; TerBush et al. 1996
Exo70	Exocyst subunit	Required for the tethering of post-Golgi vesicles to the PM Binds to PIP2 Interacts with Cdc42, and Rho3	TerBush et al. 1996; Guo et al. 1999a; Robinson et al. 1999; Guo et al. 2000; Boyd et al. 2004; He et al. 2007; Wu et al. 2010
Sec1	Fusion factor	Involved in docking and fusion of post-Golgi vesicles with the PM Interacts with the exocyst and binds to assembled SNARE complexes Localizes to the sites of polarized growth	Novick and Schekman 1979; Carr et al. 1999; Scott et al. 2004; Wiederkehr et al. 2004

Actin patches, endocytosis, and key regulators

Act1	Actin (see above)
“Arp2/3 complex”	Nucleates the assembly of branched actin filaments	Plays an essential role in endocytosis	Winter et al. 1999b; Moseley and Goode 2006
Ent1, Ent2	Epsin-like protein	Involved in endocytosis and actin patch assembly Contain a clathrin-binding motif at the C terminus Functionally redundant Interacts with Cdc42-GAPs	Wendland et al. 1999; Aguilar et al. 2006; Mukherjee et al. 2009
Las17	Activator of the Arp2/3 complex (WASP homolog)	Promotes Arp2/3-mediated actin assembly	Li 1997; Madania et al. 1999; Winter et al. 1999a; Lechler et al. 2001
Vrp1	WIP (WASP-interacting protein)-like protein	Proline-rich protein involved in actin-patch organization, endocytosis, and cytokiensis	Donnelly et al. 1993; Munn et al. 1995; Thanabalu and Munn 2001
Myo3, Myo5	Myosin-Is	Localize to actin patches and share important roles in endocytosis and polarized actin organization	Geli and Riezman 1996; Goodson et al. 1996; Anderson et al. 1998; Geli et al. 2000
Sac6	Fimbrin (see above)

Septins and key regulators

Cdc3, Cdc10, Cdc11, Cdc12, Shs1	Septins	Components of the septin ring/hourglass that acts as scaffold and/or diffusion barrier to effect cytokinesis, bud morphogenesis, etc. Vegetatively expressed, form heterooligomeric complex	Hartwell 1971b; Byers and Goetsch 1976b; Haarer and Pringle 1987; Sanders and Field 1994; Longtine et al. 1996; Frazier et al. 1998; Gladfelter et al. 2001; Mortensen et al. 2002; Vrabioiu et al. 2004; Bertin et al. 2008; McMurray and Thorner 2009; Oh and Bi 2011;
Bni5	Septin-associated protein	Required for Myo1 targeting to the bud neck before cytokinesis	Lee et al. 2002; Fang et al. 2010
		Regulates septin organization
Elm1	Septin-associated kinase	Regulates septin organization, bud morphogenesis, cytokinesis, and mitotic exit Regulates other septin-associated kinases	Blacketer et al. 1993; Bouquin et al. 2000; Mortensen et al. 2002; Woods et al. 2003; Asano et al. 2006; Szkotnicki et al. 2008; Caydasi et al. 2010; Moore et al. 2010
Gin4	Septin-associated kinase	Regulates septin organization and bud growth	Altman and Kellogg 1997; Okuzaki et al. 1997; Longtine et al. 1998; Mortensen et al. 2002
Nap1	Nucleosome assembly protein	Regulates septin organization and bud growth Interacts with mitotic cyclin Clb2 Involved in the transport of H2A and H2B histones to the nucleus	Ishimi and Kikuchi 1991; Kellogg et al. 1995; Iwase and Toh-E 2001; Longtine et al. 2000; Mosammaparast et al. 2002

Other Rho GTPases

Rho2	Rho GTPase	May have overlapping role with Rho1 in polarized cell growth May regulate microtubule assembly Nonessential for viability No specific GEFs, GAPs, and GDI have been identified	Madaule et al. 1987; Kim et al. 1994; Ozaki et al. 1996; Manning et al. 1997; Perez and Rincon 2010
Rho3	Rho GTPase	Regulates exocytosis and interacts with Myo2 and Exo70 Involved in formin activation Nonessential for viability Shares a role with Rho4 in regulating polarized cell growth Rgd1 is a GAP for Rho3	Matsui and Toh-e 1992; Adamo et al. 1999; Doignon et al. 1999; Robinson et al. 1999; Dong et al. 2003; Wu and Brennwald 2010; Wu et al. 2010
Rho4	Rho GTPase	Involved in formin activation Nonessential for viability Shares a role with Rho3 in regulating polarized cell growth Regulates interaction between Bnr1 and Hof1 Is regulated by the GAP (Rgd1) and the GDI (Rdi1)	Matsui and Toh-e 1992; Kamei et al. 1998; Doignon et al. 1999; Dong et al. 2003; Tiedje et al. 2008
Rho5	Rho GTPase	Null mutation confers resistance to various stresses (cell wall stress, osmotic stress, and oxidative stress) Nonessential for viability Rgd2 acts as a GAP for Rho5	Roumanie et al. 2001; Schmitz et al. 2002; Annan et al. 2008; Singh et al. 2008

Rho1 and its regulators and effectors

Rho1	Rho GTPase	Essential GTPase that is required for cell wall remodeling and resistance to oxidative stress Functions as a regulatory subunit for the glucan synthases Fks1 and Fks2 and also regulates Pkc1 and Mpk1-mediated cell wall integrity pathway Regulates formin activation and exocytosis Regulates actin ring assembly and cytokinesis	Yamochi et al. 1994; Drgonova et al. 1996; Kohno et al. 1996; Qadota et al. 1996; Drgonova et al. 1999; Guo et al. 2001; Tolliday et al. 2002; Dong et al. 2003; Yoshida et al. 2006; Yoshida et al. 2009; Lee et al. 2011
Rom1	GEF for Rho1	Nonessential for cell viability rom1Δ and rom2Δ are synthetically lethal	Ozaki et al. 1996; Manning et al. 1997; Schmidt et al. 1997
Rom2	GEF for Rho1	rom2Δ cells are temperature-sensitive for growth rom1Δ and rom2Δ are synthetically lethal	Ozaki et al. 1996; Manning et al. 1997; Schmidt et al. 1997
Tus1	GEF for Rho1	Nonessential for cell viability Multicopy suppressor of tor2 mutation Regulates cytokinesis	Schmelzle et al. 2002; Yoshida et al. 2006; Yoshida et al. 2009
Lrg1	GAP for Rho1	Involved in Pkc1 and Mpk1-mediated cell wall integrity pathway Regulates glucan synthesis specifically lrg1Δ and sac7Δ are synthetically lethal	Muller et al. 1994; Lorberg et al. 2001; Watanabe et al. 2001
Bem2	GAP for Rho1 and Cdc42 (see above)
Sac7	GAP for Rho1	Involved in actin organization Mutations in SAC7 suppresses mutations in TOR2 and ACT1	Dunn and Shortle 1990; Schmidt et al. 1997; Schmidt et al. 2002
Bag7	GAP for Rho1	Nonessential for cell viability Structurally and functionally related to Sac7	Roumanie et al. 2001; Schmidt et al. 2002
Rdi1	GDI for Rho1, Rho4, and Cdc42 (see above)
Fks1	Catalytic subunit of 1,3-β-D-glucan synthase Effector of Rho1	Cell wall synthesis Binds to regulatory subunit Rho1 Localizes to sites of polarized growth fks1Δ and fks2Δ are synthetically lethal	Parent et al. 1993; Douglas et al. 1994; Inoue et al. 1995; Mazur et al. 1995; Drgonova et al. 1996; Qadota et al. 1996
Fks2	Catalytic subunit of 1,3-β-D-glucan synthase Effector of Rho1	Cell wall synthesis Binds to regulatory subunit Rho1 fks1Δ and fks2Δ are synthetically lethal Involved in spore wall formation	Douglas et al. 1994; Mazur et al. 1995; Drgonova et al. 1996; Qadota et al. 1996; Ishihara et al. 2007
Pkc1	Protein kinase C	Regulates cell wall remodeling through the cell-wall–integrity pathway Localizes to sites of polarized growth Involved in formin activation	Levin et al. 1990; Levin and Bartlett-Heubusch 1992; Levin et al. 1994; Andrews and Stark 2000; Dong et al. 2003; Denis and Cyert 2005
Bni1	Formin and effector of Rho1 and Cdc42 (see above)
Sec3	Exocyst subunit and effector of Rho1 and Cdc42 (see above)

Proteins involved in cell wall remodeling and CWI signaling

Fks1	Glucan synthase and effector of Rho1 (see above)
Fks2	Glucan synthase and effector of Rho1 (see above)
Chs2	Chitin synthase II	Required for primary septum formation during cytokinesis Activity is stimulated by trypsin treatment in vitro Localization regulated by exocytosis and Cdk1	Sburlati and Cabib 1986; Shaw et al. 1991; Bi 2001; Schmidt et al. 2002; VerPlank and Li 2005; Zhang et al. 2006; Teh et al. 2009
Chs3	Catalytic subunit of chitin synthase III	Required for synthesis of majority of cellular chitin Required for synthesis of the chitin ring (“bud-scar” chitin) during bud emergence Activated by Chs4 Trafficking between chitosomes and the PM is subjected to cell-cycle–dependent complex regulation	Shaw et al. 1991; Bulawa 1992; Bulawa 1993; Chuang and Schekman 1996; Ziman et al. 1996; DeMarini et al. 1997; Ziman et al. 1998
Pkc1	Protein kinase C (see above)
Bck1 (Slk1)	Mitogen-activated protein kinase kinase kinase (MAPKKK)	Involved in Pkc1-activated cell wall integrity pathway Activates downstream Mkk1 and Mkk2	Lee and Levin 1992; Levin 2005; Park and Bi 2007
			Lee and Levin 1992; Levin 2005; Park and Bi 2007
Mkk1	MAPKK	Involved in Pkc1-activated cell wall integrity pathway	Irie et al. 1993; Levin 2005; Park and Bi 2007
		Activates downstream Mpk1
		Functionally redundant with Mkk2
Mkk2	MAPKK	Involved in Pkc1-activated cell wall integrity pathway	Irie et al. 1993; Levin 2005; Park and Bi 2007
		Activates downstream Mpk1
		Functionally redundant with Mkk1
Mpk1 (Slt2)	MAPK	Involved in Pkc1-activated cell wall integrity pathway Regulates cell-cycle progression	Torres et al. 1991; Lee et al. 1993; Levin 2005; Park and Bi 2007
Swi4-Swi6	Transcriptional activator	Regulates G1/S-specific transcription (G1 cyclins, etc.)	Andrews and Herskowitz 1989; Nasmyth and Dirick 1991; Andrews and Moore 1992; Sidorova and Breeden 1993; Dodou and Treisman 1997; Watanabe et al. 1997; Levin 2005; Levin 2005; Park and Bi 2007;
Rlm1	MADS-box transcription factor	Involved in Pkc1-activated cell wall integrity pathway Activated by Mpk1	Dodou and Treisman 1997; Watanabe et al. 1997; Levin 2005; Park and Bi 2007
Mss4	Phosphatidylinositol-4-phosphate 5-kinase (PI4P-5K)	Regulates actin and septin organizations, polarity establishment, exocytosis, cell wall remodeling and many other processes	Audhya and Emr 2002; Wild et al. 2004; He et al. 2007; Takahashi and Pryciak 2007; Orlando et al. 2008; Zhang et al. 2008; Bertin et al. 2010; Garrenton et al. 2010

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Information on individual proteins is partly based on Saccharomyces Genome Database (SGD: http://www.yeastgenome.org/).

Only functions related to polarized cell growth and cytokinesis are indicated here.

Cdc42 GTPase module:

Like all members of the Ras superfamily, Cdc42 cycles between its inactive guanosine diphosphate (GDP)-bound and active guanosine triphosphate (GTP)-bound states (Figure 2). Cdc42 activation is catalyzed by the guanine nucleotide-exchange factor (GEF), Cdc24 (Zheng et al. 1994; Tcheperegine et al. 2005). Inactivation by GTP hydrolysis is stimulated by the GTPase-activating proteins (GAPs), Bem2, Bem3, Rga1, and Rga2 (Zheng et al. 1993, 1994; Marquitz et al. 2002; Tong et al. 2007). Bem2 is a GAP for both Cdc42 and Rho1 (Zheng et al. 1993; Marquitz et al. 2002), whereas the others are thought to be Cdc42 specific. Cdc42 is also regulated by the Rho GDP-dissociation inhibitor (GDI), Rdi1 (Masuda et al. 1994; Eitzen et al. 2001; Richman et al. 2004; Tcheperegine et al. 2005).

Regulation of Cdc42 and a model for Cdc42-controlled actin cable and septin ring assembly. Internal or external cues activate the GEF Cdc24, which converts Cdc42 to its active GTP-bound state. Activated Cdc42 binds to its effectors to promote actin cable and septin ring assembly (see text for details). Cdc42-GAPs (Rga1, Rga2, Bem2, and Bem3), which are also regulated by internal and external cues, inactivate Cdc42 by stimulating its intrinsic GTPase activity. Rdi1 (Rho GDI) cycles Cdc42-GDP between the PM and the cytosol. Modified from (Park and Bi 2007) with permission.

Cdc24, the only known GEF for Cdc42 in budding yeast (Zheng et al. 1994), localizes to the sites of polarized growth (Nern and Arkowitz 1999; Toenjes et al. 1999; Shimada et al. 2000) and plays an essential role in the establishment and maintenance of polarized cell growth (Hartwell 1971b; Sloat and Pringle 1978; Sloat et al. 1981; Adams et al. 1990; Gladfelter et al. 2002).

The GAPs for Cdc42 regulate different aspects of cell polarization. In contrast to the essential GEF, none of the individual GAPs are essential for cell viability. However, rga1Δ and bem2Δ are synthetically lethal (Chen et al. 1996), suggesting that GAPs are collectively required for cell viability. At the beginning of the cell cycle, three GAPs (Rga1, Rga2, and Bem3) regulate septin ring assembly at the incipient bud site, presumably facilitating the cycling of Cdc42 between its two states (Gladfelter et al. 2002; Smith et al. 2002; Caviston et al. 2003). In addition, three GAPs (Rga2, Bem2, and Bem3) are phosphorylated by Cdk1/G1 cyclins, which is thought to inhibit their GAP activity and thus contribute to the timely activation of Cdc42 during bud emergence (Knaus et al. 2007; Sopko et al. 2007). Rga1 is uniquely required to prevent Cdc42 activation (and hence budding) at the cytokinesis site (Tong et al. 2007). All GAPs localize to the sites of polarized growth at one point of the cell cycle (Caviston et al. 2003; Knaus et al. 2007; Sopko et al. 2007), with Bem2 and Rga1 showing additional localization at the mother-bud neck before cytokinesis (Caviston et al. 2003; Huh et al. 2003; Knaus et al. 2007). It remains unclear how the localization and/or activity of the GAPs are regulated during the cell cycle and how this regulation contributes to polarity establishment and maintenance.

Rho GDI proteins display three biochemical activities on their target GTPases: they inhibit dissociation of GDP (Fukumoto et al. 1990; Leonard et al. 1992; Chuang et al. 1993), inhibit both intrinsic and GAP-stimulated GTPase activity (Hart et al. 1992; Chuang et al. 1993; Hancock and Hall 1993), and extract the GTPase from membranes into the cytosol (Hori et al. 1991; Nomanbhoy and Cerione 1996; Johnson et al. 2009). The major function of the GDI appears to cycle GDP-bound Rho GTPases between the cytosol and the PM, but the underlying mechanism remains unclear. Rdi1, the only known and nonessential Rho GDI in S. cerevisiae (Masuda et al. 1994), extracts Cdc42, Rho1, and Rho4 from membranes effectively (Eitzen et al. 2001; Richman et al. 2004; Tcheperegine et al. 2005; Tiedje et al. 2008). Overexpression of Rdi1 in a cdc24-Ts mutant causes cell lethality and loss of cell polarity, indicating a negative role of Rdi1 in cell polarization (Tcheperegine et al. 2005). On the other hand, Rdi1 is thought to promote polarization by facilitating the cycling of Cdc42 between the PM and the cytosol (Slaughter et al. 2009). Indeed, deletion of RDI1 reduces polarized growth in Candida albicans (Court and Sudbery 2007) and causes decreased pseudohyphal growth in S. cerevisiae (Tiedje et al. 2008).

Singularity in budding and Cdc42 polarization

S. cerevisiae cells bud once and only once per cell cycle (Hartwell 1971b). This singularity in budding appears to be controlled by Cdc42, as the hyperactive cdc42^G60D mutant can drive polarization at multiple random sites in the complete absence of the GEF (Figure 3A) (Caviston et al. 2002). This G60D mutation falls in the GTP hydrolysis domain and presumably slows, but does not block, GTP hydrolysis, as Cdc42 variants locked in the GTP-bound state (e.g., cdc42^G12V and cdc42^Q61L) cannot support cell growth (Ziman et al. 1991; Irazoqui et al. 2003). Interestingly, a single copy of wild-type CDC42 completely suppresses the multi-budded phenotype of cdc42^G60D, suggesting that efficient cycling of Cdc42 between GDP- and GTP-bound states enforces singularity in polarization (Caviston et al. 2002). Rewiring the Cdc42-GTP amplification loop by fusing the scaffold Bem1 to a transmembrane protein (Snc2) also leads to cell polarization at multiple sites with low frequency (Howell et al. 2009). Intriguingly, both experiments and mathematical modeling suggest that during cell polarization, multiple Cdc42-GTP clusters form transiently and compete with each other until one “wins” (Goryachev and Pokhilko 2008; Howell et al. 2009).

Singularity of polarization. (A) During each cell cycle, wild-type (WT) cells undergo a single round of budding. (Blue, DNA; red, actin.) In contrast, cells with the hyperactive *cdc42^G60D* allele can bud more than once per cell cycle. (B) Models for Cdc42 polarization. (Top) The scaffold protein Bem1 binds Cdc24 and Cla4 through distinct domains. Cdc24 increases Cdc42-GTP concentration at the polarization site. Increased Cdc42-GTP binds Cla4, which phosphorylates and may activate Cdc24, creating a positive feedback loop. (Bottom) Cdc42-GTP binds the formin Bni1, causing polarization of actin cables toward the growth site. The cables mediate myosin-V (Myo2)-dependent transport of vesicles (V) carrying Cdc42 as a “cargo.” The released Cdc42 will be converted to its active form, which binds to Bni1, leading to more actin cables and more Cdc42 transport, generating a positive feedback loop.

Two distinct mechanisms, both involving positive feedback loops, have been hypothesized to account for Cdc42 polarization at a single cortical site in the absence of any spatial cue such as in rsr1Δ cells (Figure 3B). The first is actin independent and involves the scaffold protein Bem1, which binds Cdc42-GTP, Cdc24, and Cla4 (Figure 3B, top) (Bose et al. 2001; Butty et al. 2002; Irazoqui et al. 2003; Goryachev and Pokhilko 2008; Kozubowski et al. 2008). The importance of Bem1 in this mechanism is highlighted by the synthetic lethality between bem1Δ and rsr1Δ (Irazoqui et al. 2003). Cla4, a p21-activated kinase (Pak), is an effector of Cdc42 (Cvrckova et al. 1995) and is chiefly responsible for phosphorylation of Cdc24, along with Cdk1 (Gulli et al. 2000; Bose et al. 2001; Wai et al. 2009). Yet the role of Cla4 in polarized growth remains controversial (Gulli et al. 2000; Bose et al. 2001; Hofken and Schiebel 2002; Irazoqui et al. 2003; Wild et al. 2004; Kozubowski et al. 2008; Wai et al. 2009). The consensus is that some Cdc42-GTP molecules are spontaneously clustered at a cortical site, which bind to the Cdc24-Bem1-Cla4 complex, leading to further activation of Cdc42 by Cdc24 in the initial cluster. Increased Cdc42-GTP at the cortical site, in turn, recruits more Cdc24-Bem1-Cla4 complexes and the positive cycle continues.

The second positive feedback loop for Cdc42 polarization involves an actomyosin-based transport system (Figure 3B, bottom) (Wedlich-Soldner et al. 2003). Here, a spontaneously formed cluster of Cdc42-GTP orients actin cables toward the cluster. The cables guide Myo2 (myosin-V)-powered delivery of more Cdc42 on secretory vesicles to the cluster, leading to an increased local concentration of Cdc42. The increased Cdc42, in turn, directs more actin cables toward the cluster and the positive cycle continues. The major finding supporting this hypothesis is that wild-type or GTP-locked Cdc42^Q61L, and other polarity factors such as Bem1, fail to establish a polarization state in several mutants defective in actin cable-mediated transport (Wedlich-Soldner et al. 2003; Zajac et al. 2005). In addition, Cdc42 is associated with two different populations of secretory vesicles (Orlando et al. 2011). In contrast, other studies found that Cdc42 and Bem1 could polarize successfully in several mutants with defects in the same actin transport pathway (Yamamoto et al. 2010). More importantly, endogenous Cdc42 polarizes at a single cortical site with nearly normal kinetics in cells treated with latrunculin A (LatA), which disrupts all F-actin structures (Ayscough et al. 1997; Moseley and Goode 2006). Furthermore, recent modeling work suggests that actomyosin-based transport would perturb, rather than enforce, Cdc42 polarization (Layton et al. 2011). Thus, it remains unclear to what degree the actomyosin-based feedback system contributes to Cdc42 polarization.

The actomyosin-based transport system and the Bem1-based amplification loop may act in concert to ensure robust cell polarization, as treatment of bem1Δ cells with LatA prevents Cdc42 polarization completely (Wedlich-Soldner et al. 2004). A caveat with this view is that LatA treatment may prevent Rsr1 localization to the sites of polarized growth, thereby mimicking rsr1Δ bem1Δ cells (Kozubowski et al. 2008). On the other hand, endogenous Cdc42 is indeed associated with secretory vesicles (Orlando et al. 2011). In addition, rewired cells with only the actin-dependent positive feedback mechanism are capable of Cdc42 polarization and bud growth (Howell et al. 2009). Thus, the directed transport system may play a fine-tuning role. Fluorescence recovery after photobleaching (FRAP) analysis indicates that Cdc42 at the polarization site undergoes rapid cycling between the PM and the cytosol, suggesting that its polarization is dynamically maintained (Wedlich-Soldner et al. 2004). Indeed, actin cable-mediated delivery (exocytosis) and actin patch-mediated dispersal (endocytosis) of Cdc42 are proposed to counteract lateral diffusion of Cdc42 on the PM, resulting in dynamic maintenance of Cdc42 at the polarization site (Irazoqui et al. 2005). Further studies suggest that internalization of Cdc42 occurs by two recycling pathways, the fast-acting Rdi1 pathway and the slow-acting endocytic pathway (Slaughter et al. 2009).

Key questions in Cdc42 polarization:

Despite recent progress, there are many outstanding questions regarding the mechanism of Cdc42 polarization. For example, what is the relative contribution of the GEF-Bem1-Pak amplification loop vs. the actomyosin-based transport system to the initial polarization of Cdc42 at a single cortical site? Is Bem1 a special Cdc42 effector dedicated to the amplification loop? What is the role of the Pak Cla4 in the initial Cdc42 polarization? What fraction of Cdc42 is delivered to the site of polarization via vesicle transport? What is the nucleotide-bound state of Cdc42 on the vesicles?

Cdc42-controlled actin and septin organization

Actin organization, dynamics, and functions:

In both budding and fission yeasts, three F-actin structures—cables, patches, and ring—play critical roles in polarized exocytosis, endocytosis, and cytokinesis, respectively (Figures 1B) (Moseley and Goode 2006; Kovar et al. 2011). Here, we briefly discuss the structures and functions of actin cables and patches, with a focus on how they are polarized in response to Cdc42.

Actin cables and exocytosis:

Actin cables consist of staggered linear actin filaments that are bundled together (Karpova et al. 1998). They are dynamic structures, as they disappear within ∼15 sec of treatment with LatA (Ayscough et al. 1997; Karpova et al. 1998; Yang and Pon 2002). Actin cables are polarized toward the sites of cell growth (Figure 1, A and B) (Adams and Pringle 1984; Novick and Botstein 1985; Karpova et al. 1998). The immediate depolarization of vesicle markers upon cable disassembly in formin (bni1-Ts bnr1Δ) and tropomyosin (tpm1-2 tpm2Δ) mutants indicates that actin cables are chiefly responsible for polarized exocytosis (Pruyne et al. 1998; Evangelista et al. 2002; Sagot et al. 2002a).

Actin cable assembly involves nucleation by formins, stabilization by tropomyosins, and cross-linking or bundling by actin-binding proteins (ABPs) (Moseley and Goode 2006). There are two arrays of actin cables in budding yeast, one polarized toward the bud cortex and the other toward the mother-bud neck; these are nucleated by two formins, Bni1 and Bnr1, respectively (Kohno et al. 1996; Zahner et al. 1996; Evangelista et al. 1997, 2002; Imamura et al. 1997; Pruyne et al. 2002; Sagot et al. 2002a,b; Moseley et al. 2004; Pruyne et al. 2004). Bni1 localizes to the sites of polarized cell growth during the cell cycle (Evangelista et al. 1997; Ozaki-Kuroda et al. 2001; Pruyne et al. 2004; Buttery et al. 2007) and is dynamic at all locations (Buttery et al. 2007). Bni1-nucleated actin filaments form either linear cables to mediate bud growth or a ring to drive cytokinesis. In contrast, Bnr1 is stably localized to the mother side of the bud neck from bud emergence to the onset of cytokinesis (Pruyne et al. 2004; Buttery et al. 2007). Even though Bni1 and Bnr1 nucleate actin cables at distinct locations, bni1Δ and bnr1Δ are synthetically lethal (Kamei et al. 1998; Vallen et al. 2000) and redundantly required for polarized growth (Evangelista et al. 2002; Sagot et al. 2002a). bni1Δ cells show stronger defects in polarity and cytokinesis than do bnr1Δ cells (Imamura et al. 1997; Kamei et al. 1998; Vallen et al. 2000), suggesting that Bni1 is the major formin involved in these processes.

Formin-nucleated actin filaments are stabilized by tropomyosins, Tpm1 and Tpm2, which are the only proteins known to exclusively decorate actin cables (Liu and Bretscher 1989a,b; Drees et al. 1995; Pruyne et al. 1998). The major isoform Tpm1 and the minor isoform Tpm2 share an essential role in maintaining actin-cable structures (Drees et al. 1995; Pruyne et al. 1998). The tropomyosin-decorated actin filaments are presumably cross-linked into cables by ABPs such as Sac6 (yeast fimbrin) (Adams et al. 1991) and ABP140 (Asakura et al. 1998; Yang and Pon 2002; Riedl et al. 2008), but the precise architecture remains unknown.

Polarized actin cables guide exocytic vesicles from the Golgi to the incipient bud site to drive bud emergence and enlargement (Figure 4A) (Pruyne et al. 1998). Distinct steps of exocytosis, including vesicle budding, delivery, tethering, and fusion at specific membrane compartments, are regulated by distinct Rab GTPases (Guo et al. 2000; Hutagalung and Novick 2011). To enhance specificity and order of action, the Rab GTPases are organized into activation and inactivation cascades (Hutagalung and Novick 2011). Ypt32 promotes vesicle budding from the Golgi and interacts with both a GAP (Gyp1) for the earlier Rab Ypt1 and the GEF (Sec2) for the subsequent Rab Sec4 (Ortiz et al. 2002; Rivera-Molina and Novick 2009). The vesicles are transported by Myo2 (a myosin-V) along actin cables from the mother compartment to the bud (Johnston et al. 1991; Schott et al. 2002) in a manner dependent on Sec4 and Sec2 (Goud et al. 1988; Walch-Solimena et al. 1997). The vesicles are then tethered to the PM by an evolutionarily conserved eight-protein complex called the exocyst (Sec3, Sec5, Sec6, Sec8, Sec10, Sec15, Exo70, and Exo84) (TerBush et al. 1996), which is an effector of Sec4 (Guo et al. 1999b) thought to form dynamically during each round of exocytosis (Boyd et al. 2004). Sec4 and all exocyst subunits except Sec3 can associate with vesicles (Figure 4A, right, Exocyst B′), but Sec3 and a fraction of Exo70 can also associate with the PM at the sites of polarized growth (Figure 4A, right, Exocyst A′) (Boyd et al. 2004). When a vesicle arrives, a functional exocyst is assembled, which brings the vesicle membrane and the PM into proximity for the fusion event that is mediated by the SNARE [soluble NSF (N-ethylmaleimide-sensitive factor) attachment protein receptor] proteins (Rothman 1996; Boyd et al. 2004).

Roles of Cdc42 in polarized exocytosis and septin ring assembly. (A) Roles of Cdc42 and polarisome in polarized exocytosis. (Left) Spatial relationship between Cdc42-GTP and exocytosis. Gic2-PBD (p21-binding domain) fused to tdTomato is a reporter for Cdc42-GTP (PBD) and Exo84-GFP is a marker for polarized exocytosis. Localizations from a time-lapse series are shown. (Right) Spa2, the scaffold protein of the polarisome, binds Bni1 and the Rab GAPs Msb3/Msb4 through distinct domains. Cdc42 and Rho1 control the localization of the exocyst by interacting with the exocyst components Sec3 and Exo70 (Exocyst A′). Cdc42 and Rho1 also control the localization and activation of Bni1, which promotes actin cable assembly toward the site of cell growth. Vesicles (V) carrying the Rab Sec4, Sec2 (the GEF for Sec4), and part of the exocyst (Exocyst B′, which consists of Sec5, Sec6, Sec8, Sec10, Sec15, and Exo70 and Exo84) are transported by myosin-V (Myo2) along the actin cables. Upon vesicle arrival, intact exocyst is assembled by the interaction of exocyst A′ with exocyst B′, which then promotes vesicle tethering to the PM and subsequent membrane fusion. GTP hydrolysis of Sec4 is stimulated by Msb3 and Msb4. (Bottom) Domains of Bni1 (Mosley and Goode 2005, 2006; Ozaki-Kuroda *et al.* 2001). GBD/DID, GTPase-binding domain/diaphanous inhibitory domain; FH 1-3, formin homology 1-3; SBD, Spa2-binding domain; DAD, diaphanous auto-regulatory domain; BBS, Bud6-binding site. (B) Roles of Cdc42 in septin ring assembly. (Left) Spatial relationship between Cdc42-GTP (PBD) and the septins at the incipient bud site (0 min) and after bud emergence (30 min). (Bottom) Stages of septin ring assembly. (Right) Comparison of yeast and mammalian pathways.

Role of Cdc42 in actin cable-mediated exocytosis: the “polarisome” platform:

Cdc42 is thought to control actin cable-mediated exocytosis by regulating the localization and/or activity of the formins. Bni1 localizes to the sites of polarized growth throughout the cell cycle (Evangelista et al. 1997; Ozaki-Kuroda et al. 2001; Pruyne et al. 2004) and its localization depends on Cdc42 (Ozaki-Kuroda et al. 2001). Bni1 binds directly to Cdc42 and Rho1 through its N-terminal GTPase-binding domain (GBD) (Figure 4A) (Kohno et al. 1996; Evangelista et al. 1997). However, Bni1 lacking this domain appeared to localize normally (Ozaki-Kuroda et al. 2001). Thus, how Cdc42 controls Bni1 localization remains unknown.

The FH2 domain of Bni1 forms a dimer that nucleates nonbranched actin filaments (Pruyne et al. 2002; Sagot et al. 2002b) (Figure 4A). This dimer also functions as a “leaky capper” for the barbed end of an actin filament, which allows processive elongation and prevents capping by a “tight capper” (Pring et al. 2003; Zigmond et al. 2003). The nucleation activity of Bni1 is thought to be autoinhibited by the binding of its N-terminal diaphanous inhibitory domain (DID) to its C-terminal diaphanous autoregulatory domain (DAD), and activated by the binding of a small GTPase to its GBD, which presumably opens the autoinhibitory loop (Figure 4A) (Dong et al. 2003; Moseley and Goode 2006). Whether Cdc42, Rho1, or any other small GTPases activate Bni1 in such a manner remains to be tested.

Bni1 displays rapid dynamics at the sites of polarized growth. It localizes to the PM transiently and then undergoes retrograde movements along actin cables (Buttery et al. 2007). Bni1 is thought to be activated only at the PM where its potential activators (Cdc42, Rho1, Rho3, and Bud6) are localized (Dong et al. 2003; Moseley and Goode 2005; Buttery et al. 2007). How Cdc42 controls the localization-coupled activation of Bni1 and whether Cdc42 also controls the dissociation of Bni1 from the PM requires further investigation.

The polarisome (Figures 2 and 4A, right) consists of the scaffold protein Spa2 (Sheu et al. 1998, 2000; van Drogen and Peter 2002), Pea2, which interacts with Spa2 and regulates its localization (Valtz and Herskowitz 1996), Bni1 (Evangelista et al. 1997), Bud6, an actin monomer-binding protein and an activator of Bni1 nucleation activity (Amberg et al. 1997; Moseley et al. 2004; Moseley and Goode 2005), and Msb3 and Msb4, a pair of GAPs for the Rab GTPase Sec4 (Bi et al. 2000; Gao et al. 2003; Tcheperegine et al. 2005). Sec4-GTP is associated with secretory vesicles and promotes vesicle tethering through the exocyst (Guo et al. 2000). Msb3 and Msb4 located at the sites of polarized growth stimulate GTP hydrolysis by Sec4, facilitating the cycling of Sec4 between its nucleotide-bound states (Walworth et al. 1989; Bi et al. 2000; Gao et al. 2003). Spa2 interacts with Bni1 and Msb3/Msb4 via distinct domains (Fujiwara et al. 1998; Sheu et al. 1998; Tcheperegine et al. 2005). Thus, by physically linking Bni1 regulation to Sec4 regulation, the polarisome helps to coordinate actin cable formation and vesicle fusion (Tcheperegine et al. 2005).

Bnr1 contains all the domains present in Bni1 except the Spa2\x{2011}binding domain (SBD) and Bud6\x{2011}binding site (BBS) (Moseley and Goode 2005). Bnr1 activation is also thought to involve opening of an autoinhibitory loop by small GTPases (Moseley and Goode 2006). Rho4 is the only GTPase that binds to the GBD of Bnr1 (Imamura et al. 1997), but this binding is not required for Bnr1 activation in vivo (Dong et al. 2003). In addition, Bnr1 localizes to the mother-bud neck in a septin-dependent manner from bud emergence to the onset of cytokinesis (Pruyne et al. 2004); whereas Rho4 localizes to the sites of polarized growth (Tiedje et al. 2008). Thus, Rho4 is unlikely to activate Bnr1 directly. The Rho4-binding site overlaps with the putative septin-binding site in Bnr1 (Kikyo et al. 1999; Gao et al. 2010). This raises the possibility that Rho4 and septin binding to Bnr1 may be competitive, and that binding of Bnr1 to the septin ring may activate Bnr1, whereas Rho4 binding is somehow involved in the “priming” of Bnr1 for septin binding (or simply keeping a reservoir of Bnr1 at the PM). In these scenarios, Cdc42 would control Bnr1 activation indirectly via septin ring assembly.

Role of Cdc42 in actin cable-independent exocytosis:

Cdc42 may have a direct role in exocytosis. A specific cdc42 mutant displays exocytosis defects despite seemingly well-polarized actin cables (Adamo et al. 2001). In addition, formin and tropomyosin mutants deficient in actin cable assembly still form small buds (Yamamoto et al. 2010). Bud emergence and limited bud growth can even occur in the complete absence of F-actin when cells exit from quiescence (Sahin et al. 2008). These results suggest that Cdc42 can control polarized exocytosis independently of F-actin. Cdc42 interacts directly with Sec3 and Exo70 (Zhang et al. 2001; Wu and Brennwald 2010; Wu et al. 2010), two of the exocyst subunits that can localize to the sites of polarized growth even in the absence of F-actin (Finger et al. 1998; Boyd et al. 2004). In addition, Bem1, which interacts with Cdc42 and Cdc24, binds to the exocyst subunit Sec15 (Zajac et al. 2005; France et al. 2006). Hence, Cdc42 may regulate exocytosis directly by controlling exocyst localization and/or activation.

Actin patches and endocytosis:

Actin patches are motile, short-lived, cortical foci with a diameter of ∼200 nm (Rodal et al. 2005) and a lifespan of <20 sec (Doyle and Botstein 1996; Waddle et al. 1996; Karpova et al. 1998; Smith et al. 2001; Carlsson et al. 2002). The patches consist of short, branched actin filaments (Young et al. 2004; Rodal et al. 2005) nucleated by the evolutionarily conserved Arp2/3 complex (Winter et al. 1997, 1999b; Pollard and Borisy 2003; Moseley and Goode 2006). Actin patches play a critical role in endocytosis (Engqvist-Goldstein and Drubin 2003), which regulate the levels of membrane lipids and proteins including cell wall synthetic enzymes (Ziman et al. 1996; Valdivia et al. 2002). Both receptor-mediated and fluid-phase endocytosis occur in S. cerevisiae (Engqvist-Goldstein and Drubin 2003). The receptor-mediated endocytosis is carried out by the sequential actions of distinct protein modules that regulate distinct processes such as coat formation, membrane invagination, and vesicle scission (Kaksonen et al. 2005).

Role of Cdc42 in actin patch polarization:

In wild-type cells, actin patches are concentrated at the sites of polarized growth (Adams and Pringle 1984). In cdc42 and cdc24 mutants, actin patches are assembled but distributed randomly at the cell cortex (Adams and Pringle 1984; Adams et al. 1990; Johnson and Pringle 1990), suggesting that Cdc42 is required for actin patch polarization, not assembly.

How does Cdc42 control actin patch polarization? One possibility is that Cdc42 may subtly enhance patch assembly at sites of polarized growth by stimulating p21-activated kinases (PAKs, which are Cdc42 effectors) to phosphorylate and activate myosin-I (Lechler et al. 2001). Another possible contributor is that Cdc42 interacts directly with some early-acting components of the endocytic machinery. Indeed, Cdc42-GAPs (Rga1, Rga2, and Bem3) interact with Ent1 and Ent2, a functionally redundant pair of epsin-like proteins with essential roles in endocytosis (Aguilar et al. 2006; Mukherjee et al. 2009). These interactions are independent of the endocytic function of Ent1 and Ent2 and are believed to couple polarity to endocytosis. In addition, Cdc42 appears to control polarized localization of Vrp1 [verprolin, yeast equivalent of Wiskott-Aldrich syndrome protein (WASP)-interacting protein (WIP)] and Las17 via the formins independently of F-actin (Lechler et al. 2001). Furthermore, Ent2 exhibits a two-hybrid interaction with Cdc24 and affects its localization (Drees et al. 2001; Cole et al. 2009). Thus, Cdc42 interactions may influence the sites of endocytic internalization, and endocytic proteins may modulate Cdc42 activity. Cdc42 may also influence actin patch location by controlling polarized delivery of endocytosis-promoting factors on vesicles (Gao et al. 2003). This hypothesis explains why a defect in secretion or actin cable assembly can cause defects in actin patch polarization (Pruyne et al. 1998; Gao et al. 2003) and why endocytosis is always spatially coupled to exocytosis.

Septin organization and dynamics:

Septins, a conserved family of GTP-binding proteins, assemble into heterooligomeric complexes and higher-order structures such as filaments, rings, and gauzes (Byers and Goetsch 1976a; Gladfelter et al. 2001; Longtine and Bi 2003; Hall et al. 2008; Weirich et al. 2008; McMurray and Thorner 2009; Oh and Bi 2011). Here, we briefly discuss septin organization and dynamics in the cell, with a focus on the role of Cdc42 in septin ring assembly.

Plasticity in septin complex and filament assembly:

In S. cerevisiae, five of the seven septins (Cdc3, Cdc10, Cdc11, Cdc12, and Shs1/Sep7) are expressed vegetatively and the other two (Spr3 and Spr28) are expressed exclusively during sporulation (Longtine et al. 1996). CDC3 and CDC12 are essential under all tested conditions (Frazier et al. 1998; McMurray et al. 2011). cdc10Δ and cdc11Δ cells are temperature sensitive for growth and display severe defects in septin organization, morphogenesis, and cytokinesis (Frazier et al. 1998; McMurray et al. 2011). Deletion of SHS1 has the least effect in most genetic backgrounds (Mino et al. 1998; Lee et al. 2002; Dobbelaere et al. 2003; Bertin et al. 2008), but it enhances cdc10Δ mutants and suppresses cdc11Δ mutants (Iwase et al. 2007; McMurray et al. 2011). In the W303 genetic background, shs1Δ causes cold sensitivity that is suppressed by increased dosage of Cdc11 but not of other septins (Iwase et al. 2007). In vitro reconstitution experiments indicate that four septins, Cdc3, Cdc10, Cdc11, and Cdc12, form rod-shaped, nonpolar octameric septin complexes (Cdc11-Cdc12-Cdc3-Cdc10-Cdc10-Cdc3-Cdc12-Cdc11). It is not clear how Shs1 fits, but there might be two types of septin complexes, with Shs1 replacing Cdc11 in the second type (Bertin et al. 2008), consistent with the genetic interactions observed between SHS1 and CDC11 (Iwase et al. 2007; McMurray et al. 2011).

Septin localization and filament assembly appear to be essential for cell survival. All vegetatively expressed septins display an identical pattern of localization at the mother-bud neck during the cell cycle (Longtine et al. 1996). Their localizations are interdependent, at least at high temperatures (Longtine et al. 1996; Iwase et al. 2007). The only exception is Shs1, as shs1Δ cells fail to form colonies at low temperatures but the other septins are still localized (Iwase et al. 2007). This lethality may be related to a specific role of Shs1 in cytokinesis. A recent study indicates that the survival of cells deleted for individual septin genes such as cdc10Δ and cdc11Δ is due to plasticity in septin complex and filament assembly; i.e., the remaining septin subunits are still capable of forming rod-shaped complexes that can assemble into filaments and rings, but they do so with reduced efficiency (Frazier et al. 1998; McMurray et al. 2011). Structure-based mutations that have little or no effect on septin complex formation but disrupt filament assembly invariably cause cell death, suggesting that filament assembly is essential (McMurray et al. 2011).

Septin dynamics and regulation during the cell cycle:

In budding yeast, septins undergo cell-cycle–regulated organizational changes (Figure 1C) (Weirich et al. 2008; McMurray and Thorner 2009; Oh and Bi 2011). After the launch of a new cell cycle, a nascent septin ring is assembled at the incipient bud site. This ring is dynamic as indicated by FRAP analysis (Caviston et al. 2003; Dobbelaere et al. 2003). Upon bud emergence, the septin ring is converted into a stable hourglass that covers a wider region of the mother-bud neck. Around the onset of cytokinesis, the septin hourglass is split into two dynamic rings that sandwich the cytokinesis machinery. The transition from the dynamic ring to the stable hourglass is likely caused by the arrangement or cross-linking of septin filaments into ordered arrays; whereas the hourglass splitting is triggered by the mitotic exit network (MEN) (Cid et al. 2001; Lippincott et al. 2001). Septins also undergo cell-cycle–dependent modifications including phosphorylation (Longtine et al. 1998; Mortensen et al. 2002; Egelhofer et al. 2008) and SUMOylation (Johnson and Blobel 1999; Johnson and Gupta 2001). How these modifications affect septin organization and/or dynamics requires further investigation.

Role of Cdc42 in polarized septin ring assembly:

In S. cerevisiae, Cdc42 controls polarized septin ring assembly at the incipient bud site (Figure 4B) (Pringle et al. 1995; Cid et al. 2001; Iwase et al. 2006). In the first step, septin complexes are recruited to the incipient bud site to increase local concentration for filament and ring assembly. Newly recruited septins are usually present in disorganized “clouds” or “patches” (Iwase et al. 2006). Septin recruitment completely depends on Cdc42 (Cid et al. 2001; Iwase et al. 2006) and partly on Gic1 and Gic2, a pair of Cdc42 effectors (Iwase et al. 2006). Both Gic1 and Gic2 contain a Cdc42/Rac interactive binding (CRIB) motif, which interacts specifically with Cdc42-GTP (Burbelo et al. 1995; Brown et al. 1997; Chen et al. 1997), and both proteins interact with septins (Iwase et al. 2006). Besides a few highly related yeast species, Gic1 and Gic2 do not have apparent homologs in other organisms, although Borg3 (also called CDC42EP5), a CRIB motif-containing effector of Cdc42 in mammalian cells, also interacts with septins (Figure 4B) (Joberty et al. 2001). As gic1Δ gic2Δ cells are able to assemble septin rings at low but not high temperatures (Brown et al. 1997; Chen et al. 1997; Iwase et al. 2006), Cdc42 must also control septin recruitment through other pathways.

Once recruited to the incipient bud site, septin complexes associate with the PM via interactions between septin polybasic motifs and plasma-membrane phospholipids (Zhang et al. 1999; Casamayor and Snyder 2003; Rodriguez-Escudero et al. 2005; Tanaka-Takiguchi et al. 2009; Bertin et al. 2010). These septins then undergo an organizational change from clouds to a smooth ring of ∼1.0 μm in diameter within minutes (Figure 4B) (Iwase et al. 2006). This step requires Cdc42 to cycle between GTP- and GDP-bounds states (Gladfelter et al. 2002), plus the GAPs for Cdc42 (Gladfelter et al. 2002; Smith et al. 2002; Caviston et al. 2003; Kadota et al. 2004). The GAPs may facilitate the “unloading” of septin complexes from the recruitment pathways (Gladfelter et al. 2002; Smith et al. 2002; Caviston et al. 2003; Kadota et al. 2004). The PAK Cla4 also regulates septin ring assembly by directly phosphorylating a subset of septins (Versele and Thorner 2004).

Following bud emergence, the dynamic septin ring at the incipient bud site is converted into a stable septin hourglass at the mother-bud neck. The mechanism underlying this transformation remains unknown, but it involves the Lkb1-related kinase Elm1 (Bouquin et al. 2000), the Gin4 kinase (also a substrate of Elm1) (Asano et al. 2006), and the septin-associated proteins Bni5 and Nap1 (Altman and Kellogg 1997; Lee et al. 2002), as cells lacking any of these proteins can assemble a seemingly normal septin ring but not the hourglass (Gladfelter et al. 2004).

An integrated model for Cdc42-controlled actin cable and septin ring assembly:

We hypothesize that in S. cerevisiae, Cdc42 controls actin cable and septin ring assembly at the incipient bud site through two genetically separable, biochemically cross-talking pathways, the polarisome and the Gic1/Gic2 pathways (Figure 2). In this model, the polarisome assists Cdc42 in polarized actin cable assembly and cable-dependent exocytosis. This pathway also contributes to septin ring assembly by an unknown mechanism (Goehring et al. 2003; Kadota et al. 2004). The actin cytoskeleton is involved in fine tuning septin ring assembly (Kadota et al. 2004; Kozubowski et al. 2005; Iwase et al. 2006). Thus, the polarisome could regulate septin ring assembly through Bni1-nucleated actin filaments and/or through actin cable-mediated delivery of transmembrane cargoes such as Axl2, which is known to play a role in septin organization (Gao et al. 2007). In contrast, the Gic1/Gic2 pathway mainly regulates septin ring assembly through direct interactions with septin complexes. This pathway also regulates actin cable organization by affecting septin-dependent Bnr1 localization (Pruyne et al. 2004). The polarisome and the Gic1/Gic2 pathways act in parallel, as inactivation of both pathways results in synthetic lethality (Bi et al. 2000; Jaquenoud and Peter 2000). The two pathways also cross-talk, as Bud6 and Pea2 interact with the Gic proteins by two-hybrid analysis (Jaquenoud and Peter 2000). In this view, Cdc42 controls polarized assembly of actin cables and the septin ring at the same time and same location through molecular pathways that are integrated in a way that permits independent but also cooperative assembly of the two cytoskeletal structures.

Key questions in Cdc42-controlled actin and septin organization:

A number of basic questions regarding the roles of Cdc42 in actin and septin organization remain unanswered. For example, does Cdc42 control Bni1 localization directly or indirectly through other polarity proteins? How is Bni1 activated? How does Cdc42 control exocytosis? How does Cdc42 control polarized actin patch organization or endocytosis? How does Cdc42 control septin recruitment to the incipient bud site in addition to the Gic1/Gic2 pathway? How do Cdc42 effectors interact with septin complexes and/or filaments at the molecular level? Answers to these questions will clarify the roles of Cdc42 in cytoskeletal polarization and exocytosis.

Rho1 in polarized growth

RHO1 is essential and its role in polarized growth has been analyzed extensively, whereas the functions of the other four Rhos (Rho2–Rho5) remain poorly understood. Here, we briefly review the Rho1 GTPase module and its roles in cell wall remodeling, actin organization, and exocytosis during polarized bud growth.

Rho1 GTPase module:

Rho1 is regulated by its GEFs (Rom1, Rom2, and Tus1) (Ozaki et al. 1996; Manning et al. 1997; Schmelzle et al. 2002), GAPs (Bem2, Lrg1, Sac7, and Bag7) (Dunn and Shortle 1990; Bender and Pringle 1991; Zheng et al. 1993; Kim et al. 1994; Peterson et al. 1994; Schmidt et al. 1997, 2002; Martin et al. 2000; Roumanie et al. 2001; Watanabe et al. 2001; Fitch et al. 2004), and GDI (Rdi1) (Masuda et al. 1994; Tiedje et al. 2008) (Figure 5). Inactive Rho1 is associated with post-Golgi vesicles and is activated by its GEFs at the PM upon vesicle arrival (McCaffrey et al. 1991; Abe et al. 2003).

Rho1 in cell wall remodeling:

Rho1 plays a major role in localized cell wall remodeling (Levin 2005; Park and Bi 2007). Cell walls provide the rigidity to withstand turgor, protect against sudden changes in osmolarity and other environmental stresses, and also function in cell–cell communication during mating (Klis et al. 2006; Lesage and Bussey 2006). Cell walls consist of an electron-transparent inner layer, which contains glucan (D-glucose polymers) and chitin (N-acetylglucosamine polymers), and an electron-dense outer layer, which contains heavily glycosylated mannoproteins. The inner layer is responsible for mechanical protection, whereas the outer layer is responsible for cell–cell or cell–environment communication.

Glucan and chitin, the two major cell wall polymers, are synthesized by glucan synthases and chitin synthases, respectively. Fks1 and Fks2 are the catalytic subunits of β-1,3-glucan synthases, which function during normal and stressed growth conditions, respectively (Douglas et al. 1994; Inoue et al. 1995; Mazur et al. 1995). There are three chitin synthases, CS I–III, in S. cerevisiae with Chs1, Chs2, and Chs3 as their catalytic subunits, respectively (Cabib et al. 2001; Klis et al. 2006; Lesage and Bussey 2006). The expression, localization, activity, and function of all three chitin synthases are subjected to complex and distinct regulations during the cell cycle.

Rho1 regulates cell wall synthesis by two different mechanisms (Figure 5). Under normal growth conditions, Rho1 promotes cell wall synthesis by functioning as the regulatory subunit of the glucan synthases (Drgonova et al. 1996; Mazur and Baginsky 1996; Qadota et al. 1996). Under stressed conditions, Rho1 also regulates the expression of cell wall-synthetic genes through the cell wall integrity (CWI) pathway (Heinisch et al. 1999; Cabib et al. 2001; Levin 2005; Park and Bi 2007). The CWI pathway is a mitogen-activated protein kinase (MAPK) pathway, which is activated by Rho1 and its effector Pkc1, the sole protein kinase C in S. cerevisiae (Figure 5) (Kamada et al. 1996). Cell wall stresses are sensed by transmembrane “receptors” (Wsc1, Mid2, etc.), which activate the Rho1 GEFs (Philip and Levin 2001; Audhya and Emr 2002). The MAPK cascade activates the transcriptional factors Swi4–Swi6 (SBF complex) and Rlm1, which induce the expression of genes required for G1–S transition and cell wall synthesis, respectively (Levin 2005; Park and Bi 2007).

Rho1 in actin organization:

Depletion of Rho1 at 30° does not cause clear defects in polarized actin organization (Yamochi et al. 1994), but specific temperature-sensitive mutations in RHO1 disrupt actin organization at 37° (Helliwell et al. 1998; Guo et al. 2001). Rho1 regulates actin organization through Pkc1-mediated activation of the formin Bni1 (Dong et al. 2003), and also through the CWI pathway at 37° (Mazzoni et al. 1993) (Figure 5). Upon shift to 37°, wild-type cells depolarize actin patches and cables transiently, reaching the peak of depolarization within ∼30–45 min, and then repolarize at 60–120 min (Lillie and Brown 1994; Desrivieres et al. 1998). The heat stress is thought to weaken the cell wall, which activates the CWI pathway to repair damage (Kamada et al. 1995). CWI pathway activation first depolarizes actin through Pkc1 and then repolarizes actin through MAPK activation (Delley and Hall 1999).

Rho1 in exocytosis:

Rho1 regulates polarized exocytosis by regulating actin cable assembly through the formin Bni1 (see above) and also by controlling the localization of the exocyst through an interaction with Sec3 (Guo et al. 2001). Rho1 also regulates the trafficking of Chs3 from the “chitosomes” to the PM (Valdivia and Schekman 2003).

Key questions on the roles of Rho1 in cell polarization:

The function of Rho1 in cell wall remodeling is well understood. In contrast, it remains unclear how Rho1 regulates actin organization. For example, how Rho1 regulates Bni1 localization and/or activation has not been clearly established. It is also unclear how Rho1 regulates actin depolarization or repolarization through the CWI pathway. Another outstanding question is how Rho1 is spatiotemporally coordinated with Cdc42 and other small GTPases during polarized growth. For example, does Cdc42 simply specify the location for Rho1-mediated glucan synthesis or also regulate Rho1 activation and/or its effector pathways?

Mechanism of Cytokinesis

Cytokinesis in S. cerevisiae is carried out by the concerted actions of the contractile actomyosin ring (AMR), targeted membrane deposition, and primary septum (PS) formation (Figure 6, A and B) (Bi 2001). AMR contraction is followed closely by the centripetal growth of the PS, a specialized chitinous cell wall (Lesage and Bussey 2006). At the end of PS formation, two secondary septa (SS) are synthesized at either side of the PS (Lesage and Bussey 2006). The SS, which are structurally similar to the lateral cell wall (Lesage and Bussey 2006), likely involve Rho1-controlled glucan synthesis as in the budding process (Yoshida et al. 2009). The PS and a portion of the SS are then degraded by an endochitinase and glucanases from the daughter side, resulting in cell separation (Lesage and Bussey 2006). The expression of these hydrolytic enzymes is controlled, in part, by the conserved nuclear-Dbf2-related (NDR)/large tumor suppressor (LATS) signaling network (Hergovich and Hemmings 2009) or the (regulation of Ace2 activity and cellular morphogenesis (RAM) (Nelson et al. 2003) pathway that is normally activated only in the daughter cells of S. cerevisiae (to be discussed in the planned YeastBook chapter by Eric L. Weiss).

Events of cytokinesis. (A) Coupling of AMR contraction to membrane trafficking and primary septum (PS) formation during cytokinesis. Myo1, myosin-II; Myo2, myosin-V; Chs2, a transmembrane chitin synthase responsible for PS formation. Black circles, post-Golgi vesicles; red lines, actin cables. (B) EM visualization of the primary and secondary septa. SS, secondary septa; CW, cell wall. An AMR is drawn to illustrate its spatial relationship with the PS during cytokinesis. (C) Cytokinesis defects of *myo1Δ* cells. Unlike wild-type (WT) cells, which are either unbudded or single-budded, *myo1Δ* cells form extensive chains or clusters, indicative of cytokinesis and cell-separation defects. Micrographs in B and for WT cells in C were published previously (Fang *et al.* 2010).

The AMR generates a contractile force that powers the ingression of the PM and is also thought to guide membrane deposition and the formation of the PS (Vallen et al. 2000; Fang et al. 2010). The functions of the AMR and the PS appear to be interdependent (Bi 2001; Schmidt et al. 2002; VerPlank and Li 2005), as disruption of the AMR causes severely misoriented PS formation (Fang et al. 2010), whereas disruption of PS formation results in abnormal AMR contraction (Bi 2001; Schmidt et al. 2002; VerPlank and Li 2005; Nishihama et al. 2009). It is noteworthy that S. cerevisiae cells lacking the AMR are viable and able to divide in most genetic backgrounds, though less efficiently than wild-type cells (Figure 6C) (Watts et al. 1987; Rodriguez and Paterson 1990; Bi et al. 1998; Lippincott and Li 1998a). Thus, in S. cerevisiae, the AMR-dependent and -independent mechanisms act together to ensure that cytokinesis occurs with optimum efficiency and fidelity, but the AMR-independent route can suffice. Here, we discuss the mechanisms underlying the structures and functions of the AMR and the PS and their spatiotemporal relationship. All cytokinesis proteins relevant to our discussions are described in Table 2.

Table 2. Proteins involved in cytokinesis.

Name of protein or protein complex^a	Protein activity	Function^b (mutant phenotypes and/or key protein interactions)	Key references
Proteins involved in actomyosin ring (AMR) assembly

Rho1	Rho GTPase, required for actin ring assembly
Act1	Actin, required for actin ring assembly
Pfy1	Profilin, required for actin assembly
Bni1	Formin, plays a major in actin ring assembly
Bnr1	Formin, may contribute to actin ring assembly
Myo1	Myosin-II	Required for AMR assembly and constriction Null cells are viable in most genetic backgrounds (except W303) but display severe defects in cytokinesis (Figure 6C) Guides membrane deposition and primary septum formation	Watts et al. 1987; Bi Rodriguez and Paterson 1990; et al. 1998; Lippincott and Li 1998a
Mlc1	Essential light chain (ELC) for Myo1	Serves as a light chain for Iqg1 and Myo2 Essential for cell viability and actin ring assembly Required for Iqg1 localization at the bud neck throughout the cell cycle Required for Myo1 localization at the division site during cytokinesis	Stevens and Davis 1998; Boyne et al. 2000; Shannon and Li 2000; Luo et al. 2004; Fang et al. 2010
Mlc2	Regulatory light chain (RLC) for Myo1	Bud-neck localization depends on Myo1	Luo et al. 2004; Tully et al. 2009
		May regulate Myo1 disassembly during cytokinesis
		Null cells are viable
Septins	Act as a scaffold for AMR assembly before the onset of cytokinesis and may act as a diffusion barrier and/or scaffold during cytokinesis		Bi et al. 1998; Lippincott and Li 1998a; Dobbelaere and Barral 2004; Wloka et al. 2011
Bni5	Required for Myo1 targeting to the division site from bud emergence to the onset of cytokinesis		Fang et al. 2010
Iqg1	IQGAP	Essential for cell viability and actin ring assembly Required for Myo1 localization at the division site during cytokinesis Involved in septum formation	Epp and Chant 1997; Lippincott and Li 1998a; Shannon and Li 1999; Boyne et al. 2000; Korinek et al. 2000; Shannon and Li 2000; Luo et al. 2004; Corbett et al. 2006; Fang et al. 2010

Proteins involved in targeted membrane deposition and primary septum (PS) formation

Bni1	Formin, required for actin cable assembly during cytokinesis
Myo2	Myosin-V, required for vesicle transport during cytokinesis
Exocyst	Required for tethering post-Golgi vesicles to the PM during cytokinesis
Chs2	Chitin synthase II, required for PS formation during cytokinesis
Chs3	Catalytic subunit of chitin synthase III, required for “remedial-septum” formation during cytokinesis

Proteins involved in the coordination between the AMR and PS formation

Septins	See above
Iqg1	See above
Inn1		Required for PS formation and cleavage-furrow ingression May interact with Iqg1 Binds to the SH3 domains of Hof1 and Cyk3 via distinct PXXP motifs	Sanchez-Diaz et al. 2008; Jendretzki et al. 2009; Nishihama et al. 2009; Meitinger et al. 2010;
Hof1	F-BAR protein	Involved in PS formation Binds to Inn1 via its SH3 domain May regulate AMR contraction Undergoes cell-cycle–dependent phosphorylation and degradation	Lippincott and Li 1998b; Kamei et al. 1998; Vallen et al. 2000; Blondel et al. 2005; Sanchez-Diaz et al. 2008; Nishihama et al. 2009; Meitinger et al. 2010; Meitinger et al. 2011
Cyk3		Involved in PS formation Binds to Inn1 via its SH3 domain	Korinek et al. 2000; Jendretzki et al. 2009; Nishihama et al. 2009; Meitinger et al. 2010

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Information on individual proteins is partly based on Saccharomyces Genome Database (SGD: http://www.yeastgenome.org/).

Only functions related to polarized cell growth and cytokinesis are indicated here.

Actomyosin ring assembly and disassembly

The AMR is thought to generate a contractile force through the sliding of myosin-II motors on actin filaments, as with sarcomere behavior during muscle contraction (Schroeder 1968; Schroeder 1972; Balasubramanian et al. 2004; Eggert et al. 2006; Pollard 2008). Yet despite its prevalence, this model has not been demonstrated in any experimental system. Specifically, it is not clear whether myosin-II forms bipolar filaments at the cleavage furrow and how myosin-II filaments are arranged with respect to actin filaments in the AMR. It is also unclear how other cytokinesis proteins such as IQGAP facilitate AMR assembly. During AMR contraction, the volume of the ring decreases, suggesting that contraction is coupled with disassembly (Schroeder 1972), which contrasts with Huxley’s “sliding-filament model” for muscle in which the number of contractile units remains unchanged during contraction (Huxley and Hanson 1954; Huxley 1969). How the AMR is disassembled during and at the end of cytokinesis remains poorly understood in any system.

AMR assembly:

In S. cerevisiae, six families of proteins (septins, Myo1, Mlc1, Iqg1, Bni1, and actin) are required for the AMR assembly. Septins are the first family of proteins to arrive at the division site and they are required for the localization of all other known cytokinesis proteins at the division site. Consequently, septins are required for both the AMR-dependent and -independent cytokinesis pathways, and cytokinesis is not even attempted in their absence (Hartwell 1971a). The septin hourglass structure (described earlier) is maintained at the bud neck until telophase when it splits into two cortical rings sandwiching the AMR (Cid et al. 2001; Lippincott et al. 2001; Dobbelaere and Barral 2004). Septins are thought to play two distinct roles in cytokinesis. Prior to cytokinesis, the septin hourglass functions as a scaffold required for the localization of AMR components to the division site and thus for AMR assembly (Bi et al. 1998; Lippincott and Li 1998a). During cytokinesis, the split septin rings may provide a diffusion barrier to retain diffusible cytokinesis factors at the division site (Dobbelaere and Barral 2004), although this diffusion barrier is dispensable for cytokinesis (Wloka et al. 2011).

Myo1 is the heavy chain of the sole myosin-II in S. cerevisiae. Like all conventional myosin-IIs, Myo1 forms a dimer with two globular heads each harboring an ATPase and an actin-binding site(s), and a long coiled-coil tail (Fang et al. 2010). Each Myo1 binds to one essential light chain (ELC), Mlc1, and one regulatory light chain (RLC), Mlc2, via distinct IQ motifs (Luo et al. 2004). Deletion of MYO1 is not lethal but abolishes actin ring assembly and causes defects in cytokinesis and cell separation, including misoriented PS formation (Bi et al. 1998; Lippincott and Li 1998a; Fang et al. 2010). Strikingly, Myo1 lacking the entire head domain, including the light chain-binding sites, is able to assemble an actin ring (Fang et al. 2010). This “headless” AMR constricts with a rate of only 20–30% less than the wild-type AMR does and is largely sufficient for directing PS formation and cytokinesis (Lord et al. 2005; Fang et al. 2010), implying that AMR assembly is driven by the Myo1 tail.

Myo1 localizes to the incipient bud site and the bud neck in a septin-dependent manner prior to the splitting of the septin hourglass (Bi et al. 1998; Lippincott and Li 1998a), then remains at the division site between the split septin rings during cytokinesis (Dobbelaere and Barral 2004). In contrast, actin ring assembly is initiated around the onset of anaphase and is progressively matured thereafter (Epp and Chant 1997; Bi et al. 1998; Lippincott and Li 1998a). Thus, a functional AMR is assembled in late anaphase or telophase in budding yeast, similar to animal cells. Myo1 localizes to the division site via two distinct targeting signals in its tail that act sequentially during the cell cycle and via two molecular pathways (Fang et al. 2010). From late G1 to telophase, Myo1 localization depends on the septins and Bni5 (septins → Bni5 → Myo1) (Fang et al. 2010). Deletion of BNI5 causes only mild defects in cytokinesis (Lee et al. 2002; Fang et al. 2010). From anaphase to the end of cytokinesis, Myo1 localization depends on Mlc1 and Iqg1 (Mlc1 → Iqg1→ Myo1), although a direct interaction between Iqg1 and Myo1 has not been established (Fang et al. 2010). Besides being the ELC for Myo1 (Boyne et al. 2000; Luo et al. 2004), Mlc1 is also a light chain for the myosin-V, Myo2, and Iqg1 (Stevens and Davis 1998; Boyne et al. 2000; Shannon and Li 2000) and is required for the localization of Iqg1 to the bud neck (Boyne et al. 2000; Shannon and Li 2000). Both Mlc1 and Iqg1 are essential for actin ring assembly, cytokinesis, and cell survival (Epp and Chant 1997; Stevens and Davis 1998; Boyne et al. 2000; Shannon and Li 2000). The Bni5- and Iqg1-mediated Myo1-targeting pathways functionally overlap from the onset of anaphase to the onset of telophase (Fang et al. 2010). The Bni5 pathway might be more species-specific and involved in Myo1-mediated retrograde flow of actin cables before cytokinesis (Huckaba et al. 2006; Fang et al. 2010). In contrast, the Iqg1 pathway is conserved in fission yeast (Almonacid et al. 2011; Laporte et al. 2011; Padmanabhan et al. 2011). This pathway is responsible for AMR assembly and largely accounts for the role of Myo1 in cytokinesis (Fang et al. 2010).

The formins are collectively required for actin ring assembly (Kamei et al. 1998; Vallen et al. 2000; Tolliday et al. 2002). Bni1 is the only formin present at the division site during cytokinesis (Buttery et al. 2007), consistent with its more prominent role in this process (Vallen et al. 2000). Rho1 is required for actin ring assembly, which is thought to occur, at least in part, by activating Bni1 (Tolliday et al. 2002; Yoshida et al. 2006, 2009).

A model and key questions on AMR assembly:

The core components that directly participate in the AMR assembly are Myo1, Iqg1, and Bni1. Thus, it is paramount to determine whether and how these proteins interact with each other to promote AMR assembly. One possibility is that formin (mainly Bni1 with some contribution from Bnr1)-nucleated actin filaments are captured by the actin-binding calponin homology (CH) domain of Iqg1 (Epp and Chant 1997; Shannon and Li 1999) and then organized into a ring structure using Myo1 bipolar filaments as a “template.” It is currently unknown whether Myo1 forms bipolar filaments and whether such a higher-order structure is important for cytokinesis.

AMR disassembly:

AMR contraction must be coupled with disassembly (Schroeder 1972), yet the underlying mechanism remains obscure. Current evidence suggests that the RLC, the motor activity of myosin-II, and the IQGAP are involved. In S. cerevisiae, Mlc2 (RLC) is localized to the division site by binding to Myo1 and is thought to play a role in Myo1 disassembly, as deletion of MLC2 causes Myo1 to linger at the division site at the end of cytokinesis (Luo et al. 2004). Deletion of the head domain of Myo1, including the Mlc2-binding site, causes a more severe defect in AMR disassembly than does the deletion of MLC2 (Fang et al. 2010), suggesting that the motor activity of myosin-II regulates AMR disassembly. Finally, Iqg1 is a target of anaphase promoting complex or cyclosome (APC/C), an E3 ligase that targets substrates for ubiquitin-mediated degradation by the 26S proteasome (Ko et al. 2007; Tully et al. 2009). Increased levels of Iqg1 in APC/C mutants cause prolonged duration of Iqg1 at the division site and at ectopic sites (Ko et al. 2007; Tully et al. 2009). At each site, Iqg1 colocalizes with Myo1, Mlc1, and Mlc2, suggesting that the AMR components are disassembled together. Thus, APC/C-mediated degradation of Iqg1 appears to define a major mechanism for AMR disassembly (Tully et al. 2009). Importantly, the Mlc2- and Iqg1-mediated disassembly mechanisms act synergistically, as mlc2Δ enhances the disassembly defect of the APC/C mutants (Tully et al. 2009).

Targeted membrane deposition and primary septum formation

Polarized exocytosis and membrane addition at the division site:

During cytokinesis, the “growth machine” used for budding, including Cdc42, actin cables, and post-Golgi vesicles, is redirected from the bud cortex to the bud neck (Figure 7A). The underlying mechanism for this spatiotemporal switch is unknown, but it presumably involves cell-cycle–regulated disassembly and reassembly. Both cytokinesis and budding require Myo2 (myosin-V)–powered delivery of post-Golgi vesicles along polarized actin cables (Pruyne et al. 1998; VerPlank and Li 2005), but notable differences exist. First, Cdc42 is essential for polarized organization of actin cables during budding (Adams et al. 1990; Johnson and Pringle 1990). In contrast, a clear and specific role of Cdc42 in cytokinesis has yet to be established, even though Cdc42 and its regulators are localized at the bud neck during cytokinesis (Ziman et al. 1993; Toenjes et al. 1999; Nern and Arkowitz 2000; Richman et al. 2002; Caviston et al. 2003). Conditional lethal mutations in CDC42 arrest cells at bud emergence but not cytokinesis (Adams et al. 1990; Johnson and Pringle 1990; Iwase et al. 2006), suggesting that Cdc42 may play a fine-tuning or redundant role in cytokinesis. Alternatively, the Cdc42 activity threshold required for cytokinesis may be lower than that for budding. Second, during budding, vesicles fuse with the PM upon arrival at the bud cortex. In contrast, during cytokinesis, the Myo2-loaded vesicles likely switch tracks from polarized actin cables to the actin filaments in the AMR, leading to a more uniform distribution of vesicles along the division site (Fang et al. 2010). In the absence of the AMR (e.g., myo1Δ cells), secretory vesicles are delivered to the bud neck and directly fuse with the PM between the split septin rings, by a process similar to that during budding. As the bud neck is ∼1.0 μm in diameter (Bi et al. 1998; Lippincott and Li 1998a), a mere ∼50 post-Golgi vesicles would suffice to fill both sides of the neck, and perhaps this small requirement explains why force production by the AMR, required in systems with a larger diameter furrow, is not required in yeast (Fang et al. 2010).

Spatiotemporal coupling of actomyosin ring contraction with membrane trafficking and septum formation during cytokinesis. (A) Spatiotemporal relationship between Myo1 (magenta) and Myo2 (green) before, during, and after cytokinesis. (B) Spatiotemporal relationship between Myo1 (magenta) and Chs2 (green) before, during, and after cytokinesis.

Regulation of Chs2 and primary septum formation:

Chs2 expression peaks near the end of mitosis (Chuang and Schekman 1996) and is held at the endoplasmic reticulum (ER) by Cdk1 phosphorylation (Figure 7B) (Teh et al. 2009). Upon mitotic exit, Chs2 is induced by the MEN to exit the ER and delivered to the bud neck through the secretory pathway (Chuang and Schekman 1996; VerPlank and Li 2005; Zhang et al. 2006). Chs2 may require further activation at the bud neck to catalyze PS formation, as, in mutants such as inn1Δ cells, Chs2 is localized to the bud neck with correct timing but fails to form any PS (Nishihama et al. 2009). Proteolysis of Chs2 by trypsin stimulates its activity in vitro, suggesting a possible zymogen-like behavior in vivo (Sburlati and Cabib 1986; Uchida et al. 1996; Martinez-Rucobo et al. 2009). Indeed, a soluble protease was found to stimulate Chs2 activity but its identity remains undetermined (Martinez-Rucobo et al. 2009). Together, these observations indicate that Chs2 activity is spatiotemporally controlled at multiple levels to ensure its optimal function during cytokinesis.

Although Chs2 is essential for PS formation during cytokinesis (Sburlati and Cabib 1986; Shaw et al. 1991), deletion of CHS2 is not lethal in most genetic backgrounds but causes severe defects in cytokinesis. However, deletion of CHS2 and CHS3 together causes cell lethality with cytokinesis arrest. It is thought that in the absence of Chs2, Chs3 contributes to cell survival by promoting the assembly of a frequently misshaped “remedial” septum (Cabib and Schmidt 2003). Importantly, Chs3 localization at the bud neck during cytokinesis depends on Rho1 (Yoshida et al. 2009). Thus, Rho1 plays critical roles in both AMR-dependent and -independent cytokinesis pathways (Yoshida et al. 2009). In chs2Δ cells, the AMR is assembled but often undergoes asymmetric contraction, leading to the idea of mutual dependency between the PS and the AMR (Bi 2001; Schmidt et al. 2002; VerPlank and Li 2005).

Coordination of the actomyosin ring and primary septum formation

AMR contraction and PS formation must be coordinated in time and space to ensure robust cytokinesis. Cells lacking the formin Bni1 are defective in actin ring assembly and often display asymmetric, little, or no AMR contraction (Vallen et al. 2000). In these mutant cells, septum formation is usually asymmetric or misaligned, suggesting that AMR contraction may guide PS formation. This hypothesis has been corroborated by a number of studies (Bi 2001; Schmidt et al. 2002; VerPlank and Li 2005; Fang et al. 2010). Here, we discuss the potential role of four proteins (Iqg1, Inn1, Cyk3, and Hof1) in the coupling of AMR contraction and PS formation during cytokinesis (Figure 8).

A molecular model for cytokinesis in budding yeast. At the onset of cytokinesis, the septin hourglass is split into two cortical rings (light brown), Mlc1 and Iqg1 maintain Myo1 at the division site, and all three proteins are required for AMR assembly and constriction. Iqg1 is also involved in septum formation, possibly by interacting with Inn1. Inn1 interacts with Hof1 and Cyk3 to somehow “activate” Chs2 for PS formation. AMR “guides” membrane deposition and septum formation whereas the latter “stabilizes” the AMR and its constriction. Efficient cytokinesis requires spatiotemporal coordination of the AMR and septum formation.

Iqg1 must play a role in AMR-independent cytokinesis, presumably promoting septum formation (Epp and Chant 1997; Lippincott and Li 1998a; Korinek et al. 2000; Ko et al. 2007), as deletion of IQG1, but not MYO1, is lethal in all genetic backgrounds. Deletion of INN1 prevents PS formation but permits AMR assembly (Sanchez-Diaz et al. 2008; Jendretzki et al. 2009; Nishihama et al. 2009; Meitinger et al. 2010). Inn1 interacts with and localizes to the bud neck after Iqg1 (Epp and Chant 1997; Lippincott and Li 1998a; Sanchez-Diaz et al. 2008). Thus, Inn1 likely acts downstream of Iqg1 in PS formation (Figure 8) (Nishihama et al. 2009; Meitinger et al. 2010). Cyk3 localizes to the bud neck shortly after Inn1, constricts with the AMR, and lingers at the division site for a few minutes before it disappears (Korinek et al. 2000; Jendretzki et al. 2009). Deletion of CYK3 does not cause any obvious defects in AMR assembly but causes a partial defect in PS formation, and overexpression of Cyk3 leads to ectopic PS formation (Korinek et al. 2000; Meitinger et al. 2010), suggesting a stimulatory role for Cyk3. Multicopy CYK3 suppresses the growth and cytokinesis defects of iqg1Δ and inn1Δ cells by promoting PS formation and without restoring actin ring assembly in iqg1Δ cells (Korinek et al. 2000; Jendretzki et al. 2009; Nishihama et al. 2009). Thus, Cyk3 likely acts downstream of Iqg1 and Inn1 in PS formation (Figure 8) (Nishihama et al. 2009). Inn1 also binds to the F-BAR protein Hof1 (Nishihama et al. 2009). Hof1 colocalizes with the septins from S/G2 to the onset of cytokinesis, when it is phosphorylated first by the Polo kinase Cdc5 and then by the MEN kinase Dbf2 (Lippincott and Li 1998b; Vallen et al. 2000; Blondel et al. 2005; Meitinger et al. 2011). Phosphorylated Hof1 dissociates from the septins to bind and contract with the AMR (Meitinger et al. 2011). After cytokinesis, Hof1 lingers at the division site for a few minutes before being degraded (Blondel et al. 2005). Deletion of HOF1 causes no obvious defects in AMR assembly but is synthetically lethal with myo1Δ, suggesting that Hof1 plays a role in the AMR-independent cytokinesis pathway (Figure 8) (Vallen et al. 2000). Indeed, PS formation is abnormal in hof1Δ cells (Meitinger et al. 2011).

Key questions on cytokinesis

The core components and events of cytokinesis are conserved from yeast to humans, with inevitable differences in regulation. However, key questions remain: how are the myosin-II and actin filaments organized into “contractile units?” How do other ring components such as IQGAP and the formins facilitate AMR assembly? How is the AMR coupled with membrane trafficking and localized ECM remodeling or PS formation during cytokinesis? How does abscission occur after AMR contraction? What are the functions of the septin double rings during cytokinesis and cell separation? How are the various cellular events in cytokinesis regulated by the cell-cycle machinery? Answers to these questions in multiple model systems will reveal the common and unique mechanisms underlying cytokinesis in different organisms.

Spatial Control of Polarized Cell Growth and Division

Patterns of bud-site selection

S. cerevisiae cells choose a cortical site for polarized growth in a nonrandom pattern depending on their cell type. Haploid a and α cells (as well as a/a and α/α diploids) bud in an axial pattern in which both mother and daughter cells select a bud site immediately adjacent to their previous division site. In contrast, diploid a/α cells bud in a bipolar pattern: mother cells select a bud site adjacent to their daughter or on the opposite end of the cell, whereas daughter cells almost exclusively choose a bud site directed away from their mother (Freifelder 1960; Hicks et al. 1977; Chant and Pringle 1995) (Figure 9). The choice of a bud site determines the axis of cell polarization during budding and ultimately the cell division plane, which is perpendicular to the axis of cell polarization. Successive divisions produce distinct patterns of bud scars that mark the sites of cell division on the mother cell surface (Figure 9). In cells undergoing axial budding, the division site is marked by a transient spatial signal, whereas in cells undergoing bipolar budding, both poles of the cell are marked by persistent signals that direct future budding events (Chant and Pringle 1995).

Three groups of genes, collectively called “BUD genes,” are involved in producing these patterns. The first group includes BUD3, BUD4, AXL1, and AXL2/BUD10, which are specifically required for the axial pattern (Chant and Herskowitz 1991; Chant et al. 1995; Halme et al. 1996; Roemer et al. 1996; Sanders and Herskowitz 1996). The second group includes BUD7–BUD9, RAX1, and RAX2, which are specifically required for bipolar budding (Zahner et al. 1996; Chen et al. 2000; Fujita et al. 2004; Kang et al. 2004a). The third group, which includes RSR1 (also known as BUD1), BUD2, and BUD5 (Bender and Pringle 1989; Chant et al. 1991; Chant and Herskowitz 1991; Bender 1993; Park et al. 1993), is required for both budding patterns and is thus thought to encode the “general site-selection machinery” (Chant and Pringle 1995). These gene products convey cell-type–specific information to the downstream polarity establishment machinery (Figure 10) (Chant and Pringle 1995; Pringle et al. 1995; Park and Bi 2007). All bud-site selection proteins relevant to our discussion are listed in Table 3.

Pathways governing axial and bipolar budding in haploid (a or α) and diploid (a/α) cells. Although physical interaction has been demonstrated in some cases, many interactions are postulated on the basis of genetic and localization data. All proteins do not necessarily interact at the same time. See text for further details. Modified from (Park and Bi 2007) with permission.

Table 3. Proteins involved in bud-site selection.

Name of protein or protein complex^a	Protein activity (or domain/motif)	Function^b (mutant phenotypes and/or key protein interactions)	Key references
Rsr1/Bud1	Ras-like GTPase	Required for axial and bipolar budding Interacts with Cdc24 and Cdc42	Bender and Pringle 1989; Chant et al. 1991; Park et al. 1997; Kozminski et al. 2003; Kang et al. 2010
Bud2	GAP for Rsr1	Required for axial and bipolar budding	Park et al. 1993; Bender 1993; Park et al. 1999
Bud5	GEF for Rsr1	Required for axial and bipolar budding Interacts with Axl2, Bud8, and Bud9	Chant et al. 1991; Powers et al. 1991; Kang et al. 2001; Kang et al. 2004b; Kang et al. 2012
Bud3	Axial landmark	Required for axial budding	Chant et al. 1995; Lord et al. 2000; Kang et al. 2012
Bud4	Axial landmark	Required for axial budding	Sanders and Herskowitz 1996; Kang et al. 2012
Axl1	Axial landmark (Metalloendopeptidase activity)	Required for axial budding and a-factor processing	Fujita et al. 1994; Adames et al. 1995; Lord et al. 2002; Kang et al. 2012
Axl2	Axial landmark	Required for axial budding	Roemer et al. 1996; Halme et al. 1996; Sanders et al. 1999; Lord et al. 2000; Gao et al. 2007; Kang et al. 2012
Bud8, Bud9	Bipolar landmarks	Required for bipolar budding Interact with Bud5	Zahner et al. 1996; Harkins et al. 2001; Schenkman et al. 2002; Krappmann et al. 2007
Rax1	Bipolar landmark	Required for bipolar budding	Kang et al. 2004a; Fujita et al. 2004
		Required for localization of Bud8, Bud9, and Rax2
Rax2	Bipolar landmark	Required for bipolar budding	Chen et al. 2000; Kang et al. 2004a
Bud7	Member of the ChAPs (Chs5p-Arf1p-binding proteins) family of proteins	Required for bipolar budding	Zahner et al. 1996

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Information on individual proteins is partly based on Saccharomyces Genome Database (SGD: http://www.yeastgenome.org/).

Only functions related to polarized cell growth and cytokinesis are indicated here.

The Rsr1 GTPase module: the center of spatial regulation

The Rsr1 GTPase module:

A visual screen for mutants with altered budding patterns led to the identification of BUD genes including BUD1, BUD2, and BUD5 (Chant et al. 1991; Chant and Herskowitz 1991). BUD1 is identical to RSR1, which was originally identified as a multicopy suppressor of a cdc24 mutation (Bender and Pringle 1989). BUD2 and BUD5 were also identified from independent genetic screens (Powers et al. 1991; Benton et al. 1993; Cvrckova and Nasmyth 1993). RSR1 encodes a Ras-like GTPase (Bender and Pringle 1989). BUD2 and BUD5 encode the GAP and GEF for Rsr1, respectively (Chant et al. 1991; Powers et al. 1991; Bender 1993; Park et al. 1993; Zheng et al. 1995; Park and Chant 1996). Rsr1, Bud2, and Bud5 thus constitute a functional GTPase module involved in proper bud-site selection (Figure 10). Expression of RSR1^G12V or RSR1^K16N, which encodes Rsr1 constitutively in the GTP- or in the GDP-bound (or nucleotide-empty) state, respectively, results in selection of a random bud site as does deletion of RSR1 (Ruggieri et al. 1992). Consistent with this observation, deletion of BUD2 or BUD5 also randomizes the budding pattern (Chant et al. 1991; Bender 1993; Park et al. 1993). Thus, cycling of Rsr1 between the GTP- and GDP-bound states is critical for its function in bud-site selection. Indeed, Rsr1 interacts with specific binding partners depending on its GTP- or GDP-bound state (see below).

Localization of Rsr1, Bud2, and Bud5:

Rsr1 localizes to the sites of polarized growth as well as internal membranes, particularly the vacuolar membrane. After cell division, Rsr1 remains enriched at the division site (Park et al. 2002; Kang et al. 2010). The C-terminal CAAX (A is aliphatic; X is any amino acid) box and the polybasic region (PBR) of Rsr1 are important for its efficient localization to the PM (Park et al. 2002; Kang et al. 2010).

Bud5 also localizes to the sites of polarized growth in a or α cells and to the mother-bud neck during G2/M. In late M, Bud5 appears as a double ring encircling the mother-bud neck, which then splits into two single rings at cytokinesis. Newly born G1 cells thus have the Bud5 ring at the division site (Kang et al. 2001; Marston et al. 2001). Bud5 localizes in distinct patterns in a/α cells, particularly during M and G1. Before bud emergence, Bud5 is often present at both poles of a/α cells: as a ring at one pole, which is the previous division site, and in a patch at the opposite pole, which becomes a new bud site. At a later stage of the cell cycle, Bud5 localizes to the neck and one pole of the mother cell (and/or bud tip) and occasionally only at the neck as in a or α cells (Kang et al. 2001; Marston et al. 2001). Overexpression of Bud5 results in mislocalization and random budding, suggesting that its localization is critical for proper bud-site selection (Kang et al. 2001).

Unlike Rsr1 and Bud5, Bud2 is not enriched at the division site during M and early G1. Bud2 concentrates at the incipient bud site in late G1 and at the mother-bud neck after bud emergence and then delocalizes during G2/M (Park et al. 1999; Marston et al. 2001). These localization patterns of Rsr1, Bud2, and Bud5 imply that localized action of the Rsr1 GTPase module promotes proper bud-site selection (Park et al. 1993; Michelitch and Chant 1996). Bud5 may be the key player that interacts with a spatial landmark and recruits Rsr1, while Bud2 is likely to be important for targeted release of the bud-site assembly proteins (e.g., Cdc42 and Cdc24) at the chosen site (see below).

Polarization of the Rsr1 GTPase module:

Rsr1 associates with itself and with Cdc42 (see below). The homotypic interaction of Rsr1 depends on its GEF Bud5 (Kang et al. 2010), suggesting that Rsr1 needs to maintain its ability to pass through the GDP-bound state to function, consistent with previous findings (Ruggieri et al. 1992; Park et al. 1993, 1997). In fact, Rsr1^G12V fails to form a dimer and concentrate at the division site, whereas Rsr1^K16N forms persistent homodimers (Park et al. 2002; Kang et al. 2010). The transient homotypic interaction of Rsr1, unlike that of Rsr1^K16N, suggests that Rsr1 dimerization occurs in a spatially and temporally controlled manner. Mutations in RSR1 that cause defects in its homotypic interaction and heterotypic interaction with Cdc42 result in random budding and poor membrane association (Park et al. 2002; Kang et al. 2010). Thus it remains uncertain whether the GTPase interactions and/or membrane association of Rsr1 is critical for its polarization.

Selection of a bud site in the axial pattern

Mutations in BUD3, BUD4, AXL1, or AXL2/BUD10 (AXL2 hereafter) disrupt axial budding of a or α cells, resulting in bipolar budding, while these mutations do not affect normal bipolar budding of a/α cells (Chant and Herskowitz 1991; Fujita et al. 1994; Adames et al. 1995; Chant et al. 1995; Halme et al. 1996; Roemer et al. 1996; Sanders and Herskowitz 1996). Septins also play an important role in axial budding, as some septin mutants are defective in axial budding (Flescher et al. 1993; Chant et al. 1995). Proteins encoded by these genes are thus thought to function as (or regulate) a transient cortical marker for the axial budding pattern. Genetic and localization data support the view that the cycle of assembly and disassembly of a protein complex at the mother-bud neck (and the division site) provides a spatial memory from one cell cycle to the next.

Molecular nature of the axial-budding–specific proteins:

AXL1 is the only known BUD gene that is expressed in a and α cells but not in a/α cells, and ectopic expression of AXL1 in a/α cells increases axial budding (Fujita et al. 1994). Axl1 shares homology with the insulin-degrading enzyme family of endoproteases and is also required for processing of the mating pheromone a-factor precursor (Adames et al. 1995). However, mutations in the presumptive active site of Axl1 do not perturb bud-site selection despite disrupting a-factor precursor processing, suggesting that its protease activity is not necessary for bud-site selection (Adames et al. 1995). Bud4 and Bud3 contain a putative GTP-binding motif (Sanders and Herskowitz 1996) and a Rho GEF homology domain (also called DH domain), respectively. Bud4 is indeed a GTP-binding protein and plays a critical role in the assembly of the axial landmark (Kang et al. 2012). Axl2 is a type-I transmembrane glycoprotein (Roemer et al. 1996) but has no similarity to ligand-binding or catalytic domains of known transmembrane receptors. It is possible that Axl2 functions like noncatalytic receptors such as the integrins, for which clustering drives downstream signaling (Halme et al. 1996), but it is not known whether Axl2 undergoes clustering or oligomerization. Although Axl2 contains four cadherin-like motifs in its extracellular domain (Dickens et al. 2002), the role of these motifs is obscure.

Localization of Bud3, Bud4, Axl1, and Axl2:

Bud3 and Bud4 localize as a double ring encircling the mother-bud neck during and after the G2 phase and as a single ring at the division site after cytokinesis (Chant et al. 1995; Sanders and Herskowitz 1996). Localization of Bud3 and Bud4 depends on septin integrity (Chant et al. 1995; Sanders and Herskowitz 1996). Bud4 is inefficiently localized in cdc12 mutants, and extra copies of BUD4 suppress the temperature-sensitive growth of a cdc12 mutant (Sanders and Herskowitz 1996). Thus, Bud4 may assemble at the mother-bud neck through direct interaction with septins and recruit Bud3 (Kang et al. 2012), although molecular details are not known.

Axl1 and Axl2 also localize as a double ring encircling the mother-bud neck prior to cytokinesis, and this double ring splits into two single rings after cytokinesis (Halme et al. 1996; Roemer et al. 1996). While the localized Axl1 signal is absent in late G1 and weak in S phase (Lord et al. 2000), the Axl2 signal is most intense in cells with emerging buds and appears at the periphery of small buds (Halme et al. 1996; Roemer et al. 1996). Axl1 and Bud4 localize normally in the absence of a component of the Rsr1 GTPase module, consistent with the idea that the axial landmark functions upstream of the Rsr1 GTPase module. Localization of Axl1 and Axl2 to the mother-bud neck depends on Bud3 and Bud4 to different extents (Halme et al. 1996; Lord et al. 2002; Gao et al. 2007; Kang et al. 2012). In contrast, both Bud3 and Bud4 seem to localize to the mother-bud neck normally in the absence of Axl2 (Halme et al. 1996; Roemer et al. 1996). These observations support the view that Bud3 and Bud4 recruit Axl1 and Axl2 to the division site (Gao et al. 2007; Kang et al. 2012).

AXL2 is expressed in a cell-cycle–dependent manner, peaking in late G1, and is delivered to the cell surface via the secretory pathway (Halme et al. 1996; Roemer et al. 1996; Sanders et al. 1999; Powers and Barlowe 2002). Axl2 fails to localize specifically to the bud side of the mother-bud neck in pmt4 mutants, which are defective in O-linked glycosylation of some secretory and cell surface proteins, and daughter cells of the pmt4 mutants exhibit a specific defect in the axial pattern (Sanders et al. 1999). These findings support the idea that localization of Axl2 to the mother-bud neck is important for proper bud-site selection in the subsequent cell division cycle while its localization in late G1 is likely to be important for organization of the septin filaments (Gao et al. 2007).

Choosing a nonoverlapping bud site:

Despite enrichment of the landmark proteins at the division site, a new bud appears next to, but not overlapping with, the previous division site in axially budding cells (Chant and Pringle 1995). This phenomenon depends on the activity of the Cdc42 GAP Rga1. Rga1 establishes an exclusion zone at the division site that blocks subsequent polarization within that site (Tong et al. 2007). Strikingly, in the absence of localized Rga1, a new bud forms within the old division site. The level of Cdc42-GTP is also elevated at the division site in rga1Δ cells, unlike in wild-type cells in which Cdc42-GTP localized adjacent to but outside the old division site. Deletion of RGA1 also causes a similar phenotype in diploid cells, although to a lesser extent.

Selection of a bud site in the bipolar pattern

A genetic screen for mutants with specific defects in bipolar budding identified BUD8 and BUD9 (Zahner et al. 1996). RAX1 and RAX2, which were identified as extragenic suppressors of an axl1 mutant, are also involved in bipolar budding (Chen et al. 2000; Fujita et al. 2004; Kang et al. 2004a). Null mutations in any of these genes disrupt bipolar budding but not axial budding. Strikingly, bud8 mutants bud almost exclusively at the proximal pole (the birth pole), whereas bud9 mutants predominantly bud at the distal pole (the pole opposite the birth end) (Zahner et al. 1996). These unipolar patterns differ from the axial pattern, since bud sites do not appear in a sequential chain but cluster in the vicinity of either pole in no particular order. These findings suggest that BUD8 and BUD9 encode key components that mark the poles distal and proximal to the birth pole of a daughter cell, respectively (Zahner et al. 1996).

Molecular nature of the bipolar-budding–specific proteins:

Both Bud8 and Bud9 are transmembrane proteins with a similar cytoplasmic domain and a predicted N-terminal extracellular domain, which appears to be heavily glycosylated. It has been postulated that the cytoplasmic domains of Bud8 and Bud9 may provide a signal that is recognized by a common downstream target such as a component of the Rsr1 GTPase module (Harkins et al. 2001). However, a Bud5-responsive region has been mapped within the extracellular domains of Bud8 and Bud9 (Krappmann et al. 2007). It is thus not clear whether Bud5 interacts directly with Bud8 or Bud9, or with a transmembrane protein, which indirectly bridges the interaction (see below).

Unlike Axl2, which undergoes a rapid turnover, Rax1 and Rax2 are very stable (Chen et al. 2000; Kang et al. 2004a), which fits the persistent nature of the bipolar landmark (Chant and Pringle 1995). Rax1 and Rax2 also appear to be integral membrane proteins. Rax2 has a type-I orientation, with a long extracellular N terminus (Kang et al. 2004a). Current evidence suggests that Rax1 and Rax2 interact closely with each other and with Bud8 and Bud9 in helping to mark both poles for bipolar budding.

Rax1 is necessary for efficient delivery of Bud8 and Bud9 to the proper sites for bipolar budding (Fujita et al. 2004; Kang et al. 2004a). While Rax1 and Rax2 are almost totally unable to localize to the bud tip or distal pole in the absence of Bud8, they localize normally to the proximal poles of daughter cells in the absence of Bud9 (Kang et al. 2004a). Nonetheless, Rax1 and Rax2 do not suffice to provide a spatial signal, as a bud9 null mutant almost never buds at the proximal pole (Zahner et al. 1996; Harkins et al. 2001). Thus, all of these proteins are likely to function together to provide spatial signals at both poles of a/α cells.

Localization of Bud8, Bud9, Rax1, and Rax2:

Consistent with their predicted roles, Bud8 localizes to the distal pole of a newly born cell and Bud9 localizes to the bud side of the mother-bud neck (which becomes the proximal pole of the daughter cell) just before cytokinesis (Harkins et al. 2001). In some strain backgrounds, Bud9 is observed more frequently at the distal pole of daughter cells (Taheri et al. 2000; Krappmann et al. 2007). Interestingly, the levels of BUD8 mRNA and BUD9 mRNA peak in late G2/M and G1, respectively, and this timing appears to dictate the localization of these proteins (Schenkman et al. 2002). Thus, translation and/or delivery of the proteins to the cell surface might be regulated in a cell-cycle–dependent manner, although the underlying mechanism remains unknown. Bud9 localization depends on actin and septins (Harkins et al. 2001; Schenkman et al. 2002), and Bud8 localization requires the formin Bni1, indicating a dependence on bud tip-directed actin cables (Harkins et al. 2001; Ni and Snyder 2001; Tcheperegine et al. 2005).

Rax1 and Rax2 localize to the bud tips of cells with small- or medium-sized buds and to the mother-bud necks of cells with fully formed septa, and thus these proteins remain at distal pole and the division site in both mother and daughter cells. Their presence at the division site is persistent such that multiple Rax1 and Rax2 rings are found in cells that have budded multiple times (Chen et al. 2000; Fujita et al. 2004; Kang et al. 2004a). Although this property fits expectations for a persistent bipolar landmark, several questions remain. What provides the spatial signal for bipolar budding at the previous division sites on mother cells? Since Rax1 and Rax2 localize persistently to these sites unlike Bud8 or Bud9, which is rarely present at the division sites on mother cells, Rax1 and Rax2 could provide the spatial signal. But then, why are Rax1 and Rax2 unable to do so at the proximal pole of daughter cells without Bud9? Discovering the precise functions of each protein will help clarify how mother and daughter cells respond to bipolar spatial cues (see below).

Other players in bipolar budding:

Some mild actin mutations such as act1-116 and act1-117 minimally affect cell growth but perturb the bipolar budding pattern (Yang et al. 1997). Interestingly, in a/α cells carrying specific act1 mutations, daughter cells correctly position their first bud at the distal pole of the cell, whereas the mother cells bud randomly, indicating that different rules govern bud-site selection of mother and daughter cells in a/α diploids (Yang et al. 1997). A similar phenomenon is also observed in other bipolar mutants including spa2 and bud6/aip3 (Zahner et al. 1996). Bipolar budding is also disrupted by mutations in many other genes, which may affect bipolar budding indirectly (Snyder 1989; Sivadon et al. 1995; Valtz and Herskowitz 1996; Zahner et al. 1996; Finger and Novick 1997; Vaduva et al. 1997; Yang et al. 1997; Sheu et al. 1998; Tennyson et al. 1998; Bi et al. 2000; Ni and Snyder 2001; Tcheperegine et al. 2005).

Mechanisms of the cell-type–specific budding patterns

Coupling of spatial landmarks to the Rsr1 GTPase module:

How is the spatial signal transmitted to the Rsr1 GTPase module? Recruitment of Bud5 to the landmarks appears to be critical for the establishment of the correct budding pattern (Kang et al. 2001; Marston et al. 2001). This idea is further supported by isolation of bud5 alleles that specifically disrupt bipolar budding and mislocalize only in a/α cells (Zahner et al. 1996; Kang et al. 2001, 2004b). Bud5 associates with Axl2, Bud8, and Bud9 (Kang et al. 2001, 2004b; Krappmann et al. 2007), potentially linking the landmark to the Rsr1 GTPase module (Figure 10). Bud5 indeed associates with the axial landmark only in a and α cells but not in a/α cells (Kang et al. 2012). However, it is not known whether these interactions are direct and whether distinct domains of Bud5 recognize each landmark, as no axial-specific alleles of BUD5 have yet been identified.

Bud2 localizes to the presumptive bud site initially even in the absence of Rsr1 or Bud5 (although it is not stably maintained) (Park et al. 1999; Marston et al. 2001). Bud5 localizes to the division site in the absence of Bud2. Thus, both Bud2 and Bud5 are likely to interact with spatial landmarks independently. Isolation of bud2 alleles with a specific defect in bipolar budding also supports this idea (Zahner et al. 1996). However, as with BUD5, no axial-specific alleles of BUD2 are currently known. It is also unknown which landmark protein(s) interacts with Bud2.

An important issue is whether and how Bud2 and Bud5 are regulated. It is not known whether spatial landmarks (e.g., Axl2 or Bud8) only recruit Bud5 to the presumptive bud site or also activate its GEF activity. A number of localization studies (see above) suggest that interaction of a spatial landmark with Bud5 should occur during the late M or early G1 phases, potentially activating the Rsr1 GTPase cycle, coincident with Rsr1 dimerization. Genetic and high throughput data suggest a possible regulation of Bud2 by a G1 CDK (Benton et al. 1993; Cvrckova and Nasmyth 1993; Drees et al. 2001; Holt et al. 2009), but this remains to be tested.

Regulation by cell type:

Budding patterns depend on cell types (Hicks et al. 1977; Chant and Pringle 1995), which are controlled by transcriptional regulators encoded by the mating loci MATa and MATα (Herskowitz 1988). It was thus initially proposed that the cell-type–specific budding pattern is produced by transcriptional repression of genes critical to axial budding by the corepressor a1-α2 present in diploid a/α (MATa/MATα) cells (Chant and Herskowitz 1991). This idea was supported by the isolation of AXL1, which is expressed only in a or α cells and is necessary for axial budding (Fujita et al. 1994). However, determination of cell-type–specific budding pattern is likely to be more complex than initially thought. In the absence of both Bud8 and Bud9, a/α cells exhibit a partially randomized budding pattern with an increased tendency to bud at the proximal pole, rather than at random sites. When a potential axial landmark is also absent in a/α bud8 bud9 mutant, a more fully randomized budding pattern is observed (Harkins et al. 2001). Thus, a/α cells have some ability to use axial cues in the absence of both putative bipolar landmarks. Despite our current knowledge of several proteins that control or constitute spatial landmarks, the mechanism by which the cell-type–specific budding pattern is determined remains largely unknown. One feasible model is that Axl1 may play a key role in assembly of an active axial landmark, and it may block the function of Rax1 and/or Rax2, thus inhibiting bipolar budding in haploid a or α cells. In diploid a/α cells where AXL1 is not expressed, Rax1 and Rax2 may be active for establishment of the bipolar landmark.

Directing polarity establishment by coupling of the Rsr1 and Cdc42 GTPase modules

Numerous studies suggest the coupling of bud-site selection with bud-site assembly. Overexpression of RSR1 suppresses the temperature-sensitive growth of a cdc24 (cdc24-4) mutant (Bender and Pringle 1989), and certain alleles of CDC24 including cdc24-4 show a bud-site selection defect (Sloat and Pringle 1978; Sloat et al. 1981). Rsr1-GTP binds Cdc24 (Zheng et al. 1995; Park et al. 1997) but not Cdc24-4 (Shimada et al. 2004), and Rsr1-GDP preferentially binds Bem1 (Park et al. 1997). RSR1 is necessary for localization of Cdc24 to a correct bud site in late G1 (Park et al. 2002; Shimada et al. 2004). It has been suggested that Rsr1 also activates Cdc24 by triggering its conformational change (Shimada et al. 2004). However, the underlying mechanism is less certain as there are some discrepancies among studies regarding a domain of Cdc24, which is necessary for its cortical localization or interaction with Rsr1 (Park et al. 1997; Toenjes et al. 1999; Shimada et al. 2004; Toenjes et al. 2004).

RSR1 also exhibits genetic interactions with CDC42. RSR1 was identified as an allele-specific dosage suppressor of a temperature-sensitive cdc42 allele (cdc42-118) that is defective in polarity establishment (Kozminski et al. 2003). Unlike suppression of cdc24-Ts, overexpression of GTP-locked Rsr1 (RSR1^G12V) cannot suppress cdc42-118, suggesting that cycling of Rsr1 between GDP- and GTP-bound states is required (Kozminski et al. 2003). Rsr1 also binds Cdc42 in vitro and this association is enhanced by Cdc24 (Kozminski et al. 2003). Interestingly, a mutation of RSR1 (rsr1-7), which maintains its ability to suppress cdc24-4, is no longer able to suppress cdc42-118, suggesting that this mutation disrupts the Rsr1–Cdc42 interaction without affecting the Rsr1–Cdc24 interaction (Kozminski et al. 2003; Kang et al. 2010). The Rsr1–Cdc42 interaction is thus likely to be direct rather than bridged by Cdc24. Similar GTPase heterodimerization has been reported in various organisms (Sekiguchi et al. 2001; Weibel et al. 2003; Shan et al. 2004). Interestingly, rsr1Δ exhibits synthetic lethality with cdc42-118 at 30° (Kozminski et al. 2003), and cells lacking RSR1, GIC1, and GIC2 also fail to form a bud (Kawasaki et al. 2003). These genetic interactions suggest that Rsr1 functions not only in selection of a growth site but also in polarity establishment. This notion is reinforced by high-resolution microscopy of live cells, which indicates that Rsr1 is required for both selecting and stabilizing the polarity axis in G1 (Ozbudak et al. 2005).

How does the Rsr1 GTPase module function in linking the spatial landmark to bud site assembly? A scheme in which the Rsr1 GTPase cycle orchestrates bud-site assembly at a proper bud site has been proposed (Park et al. 1997; Kozminski et al. 2003) (Figure 11). Recruitment of Bud5 and Bud2 to the presumptive bud site by the spatial landmark may lead to rapid cycling of Rsr1 between GTP- and GDP-bound states at an adjacent site. This Rsr1 cycling coupled with differential affinities of each of these species for binding partners such as Cdc24 and Bem1 may trigger the ordered assembly of a complex at the proper bud site. Several rounds of this cycle may be necessary to assemble critical levels of Cdc42-GTP and its associated proteins at the proper bud site. In the absence of the Rsr1 GTPase module, localization of Cdc24 and Cdc42 to a random bud site may occur through a distinct default pathway yet to be identified or by a “symmetry breaking” mechanism (Figure 3B, and the YeastBook chapter by Howell and Lew, 2012).

A model for how the Rsr1 GTPase cycle directs polarity establishment to a specific site. (Step 1) Bud5, which is recruited to a specific site by a spatial landmark, catalyzes GDP/GTP exchange on Rsr1. (Step 2) Rsr1-GTP associates with Cdc24 and Cdc42 and guides them to the presumptive bud site. (Step 3) Bud2 stimulates Rsr1 to hydrolyze its bound GTP. (Step 4) Cdc24 no longer interacts with Rsr1 and catalyzes the exchange of GDP for GTP on Cdc42, leading to local Cdc42 activation. Cdc42-GTP then triggers actin assembly and exocyst localization to establish an axis of cell polarization. Bud5 at the presumptive bud site may convert Rsr1 to a GTP-bound state (dashed line), allowing for another GTPase cycle. Homotypic Rsr1–Rsr1 interaction and heterotypic Rsr1–Cdc42 interaction may stabilize these GTPases at a single site, contributing to proper bud-site selection and polarity establishment. Modified from (Park and Bi 2007) with permission.

While the Rsr1 GTPase module is at the center of spatial regulation of budding by virtue of its role in linking the spatial landmark to the polarity machinery, the current model is mostly based on binary interactions of the proteins involved in bud-site selection and bud-site assembly. A future challenge is to integrate information on individual players into a comprehensive model for the spatial and temporal regulation of bud-site selection and polarity establishment.

Acknowledgments

We thank Danny Lew and Peter Pryciak for their insightful comments, Carsten Wloka and Satoshi Okada for their help in making figures, and the members of Bi and Park laboratories for discussions. We apologize to colleagues for not citing all relevant articles due to the broad scope and space limitation of this review article. Research in the Bi laboratory is supported by the National Institutes of Health grants GM59216 and GM87365 and in the Park laboratory by GM76375.

Footnotes

Communicating editor: P. Pryciak

Literature Cited

Abe M., Qadota H., Hirata A., Ohya Y., 2003. Lack of GTP-bound Rho1p in secretory vesicles of Saccharomyces cerevisiae. J. Cell Biol. 162: 85–97 [DOI] [PMC free article] [PubMed] [Google Scholar]
Adames N., Blundell K., Ashby M. N., Boone C., 1995. Role of yeast insulin-degrading enzyme homologs in propheromone processing and bud site selection. Science 270: 464–467 [DOI] [PubMed] [Google Scholar]
Adamo J. E., Rossi G., Brennwald P., 1999. The Rho GTPase Rho3 has a direct role in exocytosis that is distinct from its role in actin polarity. Mol. Biol. Cell 10: 4121–4133 [DOI] [PMC free article] [PubMed] [Google Scholar]
Adamo J. E., Moskow J. J., Gladfelter A. S., Viterbo D., Lew D. J., et al. , 2001. Yeast Cdc42 functions at a late step in exocytosis, specifically during polarized growth of the emerging bud. J. Cell Biol. 155: 581–592 [DOI] [PMC free article] [PubMed] [Google Scholar]
Adams A. E., Botstein D., Drubin D. G., 1989. A yeast actin-binding protein is encoded by SAC6, a gene found by suppression of an actin mutation. Science 243: 231–233 [DOI] [PubMed] [Google Scholar]
Adams A. E., Botstein D., Drubin D. G., 1991. Requirement of yeast fimbrin for actin organization and morphogenesis in vivo. Nature 354: 404–408 [DOI] [PubMed] [Google Scholar]
Adams A. E. M., Pringle J. R., 1984. Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae. J. Cell Biol. 98: 934–945 [DOI] [PMC free article] [PubMed] [Google Scholar]
Adams A. E. M., Johnson D. I., Longnecker R. M., Sloat B. F., Pringle J. R., 1990. CDC42 and CDC43, two additional genes involved in budding and the establishment of cell polarity in the yeast Saccharomyces cerevisiae. J. Cell Biol. 111: 131–142 [DOI] [PMC free article] [PubMed] [Google Scholar]
Aguilar R. C., Longhi S. A., Shaw J. D., Yeh L. Y., Kim S., et al. , 2006. From the Cover: epsin N-terminal homology domains perform an essential function regulating Cdc42 through binding Cdc42 GTPase-activating proteins. Proc. Natl. Acad. Sci. USA 103: 4116–4121 [DOI] [PMC free article] [PubMed] [Google Scholar]
Albert S., Gallwitz D., 1999. Two new members of a family of Ypt/Rab GTPase activating proteins. Promiscuity of substrate recognition. J. Biol. Chem. 274: 33186–33189 [DOI] [PubMed] [Google Scholar]
Almonacid M., Celton-Morizur S., Jakubowski J. L., Dingli F., Loew D., et al. , 2011. Temporal control of contractile ring assembly by Plo1 regulation of myosin II recruitment by Mid1/anillin. Curr. Biol. 21: 473–479 [DOI] [PMC free article] [PubMed] [Google Scholar]
Altman R., Kellogg D., 1997. Control of mitotic events by Nap1 and the Gin4 kinase. J. Cell Biol. 138: 119–130 [DOI] [PMC free article] [PubMed] [Google Scholar]
Amberg D. C., Zahner J. E., Mulholland J. W., Pringle J. R., Botstein D., 1997. Aip3p/Bud6p, a yeast actin-interacting protein that is involved in morphogenesis and the selection of bipolar budding sites. Mol. Biol. Cell 8: 729–753 [DOI] [PMC free article] [PubMed] [Google Scholar]
Anderson B. L., Boldogh I., Evangelista M., Boone C., Greene L. A., et al. , 1998. The Src homology domain 3 (SH3) of a yeast type I myosin, Myo5p, binds to verprolin and is required for targeting to sites of actin polarization. J. Cell Biol. 141: 1357–1370 [DOI] [PMC free article] [PubMed] [Google Scholar]
Andrews B. J., Herskowitz I., 1989. The yeast Swi4 protein contains a motif present in developmental regulators and is part of a complex involved in cell-cycle dependent transcription. Nature 342: 830–833 [DOI] [PubMed] [Google Scholar]
Andrews B. J., Moore L. A., 1992. Interaction of the yeast Swi4 and Swi6 cell cycle regulatory proteins in vitro. Proc. Natl. Acad. Sci. USA 89: 11852–11856 [DOI] [PMC free article] [PubMed] [Google Scholar]
Andrews P. D., Stark M. J., 2000. Dynamic, Rho1p-dependent localization of Pkc1p to sites of polarized growth. J. Cell Sci. 113: 2685–2693 [DOI] [PubMed] [Google Scholar]
Annan R. B., Wu C., Waller D. D., Whiteway M., Thomas D. Y., 2008. Rho5p is involved in mediating the osmotic stress response in Saccharomyces cerevisiae, and its activity is regulated via Msi1p and Npr1p by phosphorylation and ubiquitination. Eukaryot. Cell 7: 1441–1449 [DOI] [PMC free article] [PubMed] [Google Scholar]
Arkowitz R. A., 2009. Chemical gradients and chemotropism in yeast. Cold Spring Harb. Perspect. Biol. 1: a001958. [DOI] [PMC free article] [PubMed] [Google Scholar]
Asakura T., Sasaki T., Nagano F., Satoh A., Obaishi H., et al. , 1998. Isolation and characterization of a novel actin filament-binding protein from Saccharomyces cerevisiae. Oncogene 16: 121–130 [DOI] [PubMed] [Google Scholar]
Asano S., Park J. E., Yu L. R., Zhou M., Sakchaisri K., et al. , 2006. Direct phosphorylation and activation of a Nim1-related kinase Gin4 by Elm1 in budding yeast. J. Biol. Chem. 281: 27090–27098 [DOI] [PubMed] [Google Scholar]
Audhya A., Emr S. D., 2002. Stt4 PI 4-kinase localizes to the plasma membrane and functions in the Pkc1-mediated MAP kinase cascade. Dev. Cell 2: 593–605 [DOI] [PubMed] [Google Scholar]
Ayscough K. R., Stryker J., Pokala N., Sanders M., Crews P., et al. , 1997. High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor Latrunculin-A. J. Cell Biol. 137: 399–416 [DOI] [PMC free article] [PubMed] [Google Scholar]
Balasubramanian M. K., Bi E., Glotzer M., 2004. Comparative analysis of cytokinesis in budding yeast, fission yeast and animal cells. Curr. Biol. 14: R806–R818 [DOI] [PubMed] [Google Scholar]
Barr F. A., Gruneberg U., 2007. Cytokinesis: placing and making the final cut. Cell 131: 847–860 [DOI] [PubMed] [Google Scholar]
Bender A., 1993. Genetic evidence for the roles of the bud-site-selection genes BUD5 and BUD2 in control of the Rsr1p (Bud1p) GTPase in yeast. Proc. Natl. Acad. Sci. USA 90: 9926–9929 [DOI] [PMC free article] [PubMed] [Google Scholar]
Bender A., Pringle J. R., 1989. Multicopy suppression of the cdc24 budding defect in yeast by CDC42 and three newly identified genes including the ras-related gene RSR1. Proc. Natl. Acad. Sci. USA 86: 9976–9980 [DOI] [PMC free article] [PubMed] [Google Scholar]
Bender A., Pringle J. R., 1991. Use of a screen for synthetic lethal and multicopy suppressee mutants to identify two new genes involved in morphogenesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 11: 1295–1305 [DOI] [PMC free article] [PubMed] [Google Scholar]
Benli M., Doring F., Robinson D. G., Yang X., Gallwitz D., 1996. Two GTPase isoforms, Ypt31p and Ypt32p, are essential for Golgi function in yeast. EMBO J. 15: 6460–6475 [PMC free article] [PubMed] [Google Scholar]
Benton B., Tinkelenberg A. H., Jean D., Plump S. D., Cross F. R., 1993. Genetic analysis of Cln/Cdc28 regulation of cell morphogenesis in budding yeast. EMBO J. 12: 5267–5275 [DOI] [PMC free article] [PubMed] [Google Scholar]
Benton B. K., Tinkelenberg A., Gonzalez I., Cross F. R., 1997. Cla4p, a Saccharomyces cerevisiae Cdc42p-activated kinase involved in cytokinesis, is activated at mitosis. Mol. Cell. Biol. 17: 5067–5076 [DOI] [PMC free article] [PubMed] [Google Scholar]
Bertin A., McMurray M. A., Grob P., Park S. S., Garcia G., 3rd, et al. , 2008. Saccharomyces cerevisiae septins: supramolecular organization of heterooligomers and the mechanism of filament assembly. Proc. Natl. Acad. Sci. USA 105: 8274–8279 [DOI] [PMC free article] [PubMed] [Google Scholar]
Bertin A., McMurray M. A., Thai L., Garcia G., 3rd, Votin V., et al. , 2010. Phosphatidylinositol-4,5-bisphosphate promotes budding yeast septin filament assembly and organization. J. Mol. Biol. 404: 711–731 [DOI] [PMC free article] [PubMed] [Google Scholar]
Bi E., 2001. Cytokinesis in budding yeast: the relationship between actomyosin ring function and septum formation. Cell Struct. Funct. 26: 529–537 [DOI] [PubMed] [Google Scholar]
Bi E., Maddox P., Lew D. J., Salmon E. D., McMillan J. N., et al. , 1998. Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis. J. Cell Biol. 142: 1301–1312 [DOI] [PMC free article] [PubMed] [Google Scholar]
Bi E., Chiavetta J. B., Chen H., Chen G.-C., Chan C. S. M., et al. , 2000. Identification of novel, evolutionarily conserved Cdc42p-interacting proteins and of redundant pathways linking Cdc24p and Cdc42p to actin polarization in yeast. Mol. Biol. Cell 11: 773–793 [DOI] [PMC free article] [PubMed] [Google Scholar]
Blacketer M. J., Koehler C. M., Coats S. G., Myers A. M., Madaule P., 1993. Regulation of dimorphism in Saccharomyces cerevisiae: involvement of the novel protein kinase homolog Elm1p and protein phosphatase 2A. Mol. Cell. Biol. 13: 5567–5581 [DOI] [PMC free article] [PubMed] [Google Scholar]
Blondel M., Bach S., Bamps S., Dobbelaere J., Wiget P., et al. , 2005. Degradation of Hof1 by SCF(Grr1) is important for actomyosin contraction during cytokinesis in yeast. EMBO J. 24: 1440–1452 [DOI] [PMC free article] [PubMed] [Google Scholar]
Bobola N., Jansen R. P., Shin T. H., Nasmyth K., 1996. Asymmetric accumulation of Ash1p in postanaphase nuclei depends on a myosin and restricts yeast mating-type switching to mother cells. Cell 84: 699–709 [DOI] [PubMed] [Google Scholar]
Bose I., Irazoqui J. E., Moskow J. J., Bardes E. S. G., Zyla T. R., et al. , 2001. Assembly of scaffold-mediated complexes containing Cdc42p, the exchange factor Cdc24p, and the effector Cla4p required for cell cycle regulated phosphorylation of Cdc24p. J. Biol. Chem. 276: 7176–7186 [DOI] [PubMed] [Google Scholar]
Bouquin N., Barral Y., Courbeyrette R., Blondel M., Snyder M., et al. , 2000. Regulation of cytokinesis by the Elm1 protein kinase in Saccharomyces cerevisiae. J. Cell Sci. 113: 1435–1445 [DOI] [PubMed] [Google Scholar]
Boyd C., Hughes T., Pypaert M., Novick P., 2004. Vesicles carry most exocyst subunits to exocytic sites marked by the remaining two subunits, Sec3p and Exo70p. J. Cell Biol. 167: 889–901 [DOI] [PMC free article] [PubMed] [Google Scholar]
Boyne J. R., Yosuf H. M., Bieganowski P., Brenner C., Price C., 2000. Yeast myosin light chain, Mlc1p, interacts with both IQGAP and class II myosin to effect cytokinesis. J. Cell Sci. 113: 4533–4543 [DOI] [PubMed] [Google Scholar]
Bretscher A., 2003. Polarized growth and organelle segregation in yeast: the tracks, motors, and receptors. J. Cell Biol. 160: 811–816 [DOI] [PMC free article] [PubMed] [Google Scholar]
Brown J. L., Jaquenoud M., Gulli M. P., Chant J., Peter M., 1997. Novel Cdc42-binding proteins Gic1 and Gic2 control cell polarity in yeast. Genes Dev. 11: 2972–2982 [DOI] [PMC free article] [PubMed] [Google Scholar]
Bulawa C. E., 1992. CSD2, CSD3, and CSD4, genes required for chitin synthesis in Saccharomyces cerevisiae: the CSD2 gene product is related to chitin synthases and to developmentally regulated proteins in Rhizobium species and Xenopus laevis. Mol. Cell. Biol. 12: 1764–1776 [DOI] [PMC free article] [PubMed] [Google Scholar]
Bulawa C. E., 1993. Genetics and molecular biology of chitin synthesis in fungi. Annu. Rev. Microbiol. 47: 505–534 [DOI] [PubMed] [Google Scholar]
Burbelo P. D., Drechsel D., Hall A., 1995. A conserved binding motif defines numerous candidate target proteins for both Cdc42 and Rac GTPases. J. Biol. Chem. 270: 29071–29074 [DOI] [PubMed] [Google Scholar]
Buttery S. M., Yoshida S., Pellman D., 2007. Yeast formins Bni1 and Bnr1 utilize different modes of cortical interaction during the assembly of actin cables. Mol. Biol. Cell 18: 1826–1838 [DOI] [PMC free article] [PubMed] [Google Scholar]
Butty A. C., Perrinjaquet N., Petit A., Jaquenoud M., Segall J. E., et al. , 2002. A positive feedback loop stabilizes the guanine-nucleotide exchange factor Cdc24 at sites of polarization. EMBO J. 21: 1565–1576 [DOI] [PMC free article] [PubMed] [Google Scholar]
Byers B., Goetsch L., 1976a. A highly ordered ring of membrane-associated filaments in budding yeast. J. Cell Biol. 69: 717–721 [DOI] [PMC free article] [PubMed] [Google Scholar]
Byers B., Goetsch L., 1976b. Loss of the filamentous ring in cytokinesis-defective mutants of budding yeast. J. Cell Biol. 70: 35a. [DOI] [PMC free article] [PubMed] [Google Scholar]
Cabib E., Roh D. H., Schmidt M., Crotti L. B., Varma A., 2001. The yeast cell wall and septum as paradigms of cell growth and morphogenesis. J. Biol. Chem. 276: 19679–19682 [DOI] [PubMed] [Google Scholar]
Cabib E., Schmidt M., 2003. Chitin synthase III activity, but not the chitin ring, is required for remedial septa formation in budding yeast. FEMS Microbiol. Lett. 224: 299–305 [DOI] [PubMed] [Google Scholar]
Carlsson A. E., Shah A. D., Elking D., Karpova T. S., Cooper J. A., 2002. Quantitative analysis of actin patch movement in yeast. Biophys. J. 82: 2333–2343 [DOI] [PMC free article] [PubMed] [Google Scholar]
Casamayor A., Snyder M., 2003. Molecular dissection of a yeast septin: distinct domains are required for septin interaction, localization, and function. Mol. Cell. Biol. 23: 2762–2777 [DOI] [PMC free article] [PubMed] [Google Scholar]
Caviston J. P., Tcheperegine S. E., Bi E., 2002. Singularity in budding: a role for the evolutionarily conserved small GTPase Cdc42p. Proc. Natl. Acad. Sci. USA 99: 12185–12190 [DOI] [PMC free article] [PubMed] [Google Scholar]
Caviston J. P., Longtine M., Pringle J. R., Bi E., 2003. The role of Cdc42p GTPase-activating proteins in assembly of the septin ring in yeast. Mol. Biol. Cell 14: 4051–4066 [DOI] [PMC free article] [PubMed] [Google Scholar]
Caydasi A. K., Kurtulmus B., Orrico M. I., Hofmann A., Ibrahim B., et al. , 2010. Elm1 kinase activates the spindle position checkpoint kinase Kin4. J. Cell Biol. 190: 975–989 [DOI] [PMC free article] [PubMed] [Google Scholar]
Chant J., Herskowitz I., 1991. Genetic control of bud site selection in yeast by a set of gene products that constitute a morphogenetic pathway. Cell 65: 1203–1212 [DOI] [PubMed] [Google Scholar]
Chant J., Pringle J. R., 1995. Patterns of bud-site selection in the yeast Saccharomyces cerevisiae. J. Cell Biol. 129: 751–765 [DOI] [PMC free article] [PubMed] [Google Scholar]
Chant J., Corrado K., Pringle J. R., Herskowitz I., 1991. Yeast BUD5, encoding a putative GDP-GTP exchange factor, is necessary for bud site selection and interacts with bud formation gene BEM1. Cell 65: 1213–1224 [DOI] [PubMed] [Google Scholar]
Chant J., Mischke M., Mitchell E., Herskowitz I., Pringle J. R., 1995. Role of Bud3p in producing the axial budding pattern of yeast. J. Cell Biol. 129: 767–778 [DOI] [PMC free article] [PubMed] [Google Scholar]
Chen G.-C., Zheng L., Chan C. S. M., 1996. The LIM domain-containing Dbm1 GTPase-activating protein is required for the normal cellular morphogenesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 16: 1376–1390 [DOI] [PMC free article] [PubMed] [Google Scholar]
Chen G.-C., Kim Y.-J., Chan C. S. M., 1997. The Cdc42 GTPase-associated proteins Gic1 and Gic2 are required for polarized cell growth in Saccharomyces cerevisiae. Genes Dev. 11: 2958–2971 [DOI] [PMC free article] [PubMed] [Google Scholar]
Chen T., Hiroko T., Chaudhuri A., Inose F., Lord M., et al. , 2000. Multigenerational cortical inheritance of the Rax2 protein in orienting polarity and division in yeast. Science 290: 1975–1978 [DOI] [PubMed] [Google Scholar]
Chen W., Lim H. H., Lim L., 1993. The CDC42 homologue from Caenorhabditis elegans. Complementation of yeast mutation. J. Biol. Chem. 268: 13280–13285 [PubMed] [Google Scholar]
Chenevert J., Corrado K., Bender B., Pringle J. R., Herskowitz I., 1992. A yeast gene (BEM1) necessary for cell polarization whose product contains two SH3 domains. Nature 356: 77–79 [DOI] [PubMed] [Google Scholar]
Chenevert J., Valtz N., Herskowitz I., 1994. Identification of genes required for normal pheromone-induced cell polarization in Saccharomyces cerevisiae. Genetics 136: 1287–1296 [DOI] [PMC free article] [PubMed] [Google Scholar]
Chuang J. S., Schekman R. W., 1996. Differential trafficking and timed localization of two chitin synthase proteins, Chs2p and Chs3p. J. Cell Biol. 135: 597–610 [DOI] [PMC free article] [PubMed] [Google Scholar]
Chuang T. H., Xu X., Knaus U. G., Hart M. J., Bokoch G. M., 1993. GDP dissociation inhibitor prevents intrinsic and GTPase activating protein-stimulated GTP hydrolysis by the Rac GTP-binding protein. J. Biol. Chem. 268: 775–778 [PubMed] [Google Scholar]
Cid V. J., Adamikova L., Sanchez M., Molina M., Nombela C., 2001. Cell cycle control of septin ring dynamics in the budding yeast. Microbiology 147: 1437–1450 [DOI] [PubMed] [Google Scholar]
Cole K. C., Barbour J. E., Midkiff J. F., Marble B. M., Johnson D. I., 2009. Multiple proteins and phosphorylations regulate Saccharomyces cerevisiae Cdc24p localization. FEBS Lett. 583: 3339–3343 [DOI] [PubMed] [Google Scholar]
Corbett M., Xiong Y., Boyne J. R., Wright D. J., Munro E., et al. , 2006. IQGAP and mitotic exit network (MEN) proteins are required for cytokinesis and re-polarization of the actin cytoskeleton in the budding yeast, Saccharomyces cerevisiae. Eur. J. Cell Biol. 85: 1201–1215 [DOI] [PubMed] [Google Scholar]
Court H., Sudbery P., 2007. Regulation of Cdc42 GTPase activity in the formation of hyphae in Candida albicans. Mol. Biol. Cell 18: 265–281 [DOI] [PMC free article] [PubMed] [Google Scholar]
Cvrckova F., Nasmyth K., 1993. Yeast G1 cyclins CLN1 and CLN2 and a GAP-like protein have a role in bud formation. EMBO J. 12: 5277–5286 [DOI] [PMC free article] [PubMed] [Google Scholar]
Cvrckova F., De Virgilio C., Manser E., Pringle J. R., Nasmyth K., 1995. Ste20-like protein kinases are required for normal localization of cell growth and for cytokinesis in budding yeast. Genes Dev. 9: 1817–1830 [DOI] [PubMed] [Google Scholar]
D’Silva S., Haider S. J., Phizicky E. M., 2011. A domain of the actin binding protein Abp140 is the yeast methyltransferase responsible for 3-methylcytidine modification in the tRNA anti-codon loop. RNA 17: 1100–1110 [DOI] [PMC free article] [PubMed] [Google Scholar]
De Smet I., Beeckman T., 2011. Asymmetric cell division in land plants and algae: the driving force for differentiation. Nat. Rev. Mol. Cell Biol. 12: 177–188 [DOI] [PubMed] [Google Scholar]
Delley P. A., Hall M. N., 1999. Cell wall stress depolarizes cell growth via hyperactivation of RHO1. J. Cell Biol. 147: 163–174 [DOI] [PMC free article] [PubMed] [Google Scholar]
DeMarini D. J., Adams A. E. M., Fares H., De Virgilio C., Valle G., et al. , 1997. A septin-based hierarchy of proteins required for localized deposition of chitin in the Saccharomyces cerevisiae cell wall. J. Cell Biol. 139: 75–93 [DOI] [PMC free article] [PubMed] [Google Scholar]
Denis V., Cyert M. S., 2005. Molecular analysis reveals localization of Saccharomyces cerevisiae protein kinase C to sites of polarized growth and Pkc1p targeting to the nucleus and mitotic spindle. Eukaryot. Cell 4: 36–45 [DOI] [PMC free article] [PubMed] [Google Scholar]
Desrivieres S., Cooke F. T., Parker P. J., Hall M. N., 1998. MSS4, a phosphatidylinositol-4-phosphate 5-kinase required for organization of the actin cytoskeleton in Saccharomyces cerevisiae. J. Biol. Chem. 273: 15787–15793 [DOI] [PubMed] [Google Scholar]
Dickens N. J., Beatson S., Ponting C. P., 2002. Cadherin-like domains in [alpha]-dystroglycan, [alpha]/[epsilon]-sarcoglycan and yeast and bacterial proteins. Curr. Biol. 12: R197–R199 [DOI] [PubMed] [Google Scholar]
Dickinson J. R., 2008. Filament formation in Saccharomyces cerevisiae. Folia Microbiol. (Praha) 53: 3–14 [DOI] [PubMed] [Google Scholar]
Dobbelaere J., Barral Y., 2004. Spatial coordination of cytokinetic events by compartmentalization of the cell cortex. Science 305: 393–396 [DOI] [PubMed] [Google Scholar]
Dobbelaere J., Gentry M. S., Hallberg R. L., Barral Y., 2003. Phosphorylation-dependent regulation of septin dynamics during the cell cycle. Dev. Cell 4: 345–357 [DOI] [PubMed] [Google Scholar]
Dodou E., Treisman R., 1997. The Saccharomyces cerevisiae MADS-box transcription factor Rlm1 is a target for the Mpk1 mitogen-activated protein kinase pathway. Mol. Cell. Biol. 17: 1848–1859 [DOI] [PMC free article] [PubMed] [Google Scholar]
Doignon F., Weinachter C., Roumanie O., Crouzet M., 1999. The yeast Rgd1p is a GTPase activating protein of the Rho3 and rho4 proteins. FEBS Lett. 459: 458–462 [DOI] [PubMed] [Google Scholar]
Dong Y., Pruyne D., Bretscher A., 2003. Formin-dependent actin assembly is regulated by distinct modes of Rho signaling in yeast. J. Cell Biol. 161: 1081–1092 [DOI] [PMC free article] [PubMed] [Google Scholar]
Donnelly S. F., Pocklington M. J., Pallotta D., Orr E., 1993. A proline-rich protein, verprolin, involved in cytoskeletal organization and cellular growth in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 10: 585–596 [DOI] [PubMed] [Google Scholar]
Douglas C. M., Foor F., Marrinan J. A., Morin N., Nielsen J. B., et al. , 1994. The Saccharomyces cerevisiae FKS1 (ETG1) gene encodes an integral membrane protein which is a subunit of 1,3-β-D-glucan synthase. Proc. Natl. Acad. Sci. USA 91: 12907–12911 [DOI] [PMC free article] [PubMed] [Google Scholar]
Doyle T., Botstein D., 1996. Movement of yeast cortical actin cytoskeleton visualized in vivo. Proc. Natl. Acad. Sci. USA 93: 3886–3891 [DOI] [PMC free article] [PubMed] [Google Scholar]
Drees B., Brown C., Barrell B. G., Bretscher A., 1995. Tropomyosin is essential in yeast, yet the TPM1 and TPM2 products perform distinct functions. J. Cell Biol. 128: 383–392 [DOI] [PMC free article] [PubMed] [Google Scholar]
Drees B. L., Sundin B., Brazeau E., Caviston J. P., Chen G.-C., et al. , 2001. A protein interaction map for cell polarity development. J. Cell Biol. 154: 549–571 [DOI] [PMC free article] [PubMed] [Google Scholar]
Drgonova J., Drgon T., Tanaka K., Kollar R., Chen G. C., et al. , 1996. Rho1p, a yeast protein at the interface between cell polarization and morphogenesis. Science 272: 277–279 [DOI] [PubMed] [Google Scholar]
Drgonova J., Drgon T., Roh D. H., Cabib E., 1999. The GTP-binding protein Rho1p is required for cell cycle progression and polarization of the yeast cell. J. Cell Biol. 146: 373–387 [DOI] [PMC free article] [PubMed] [Google Scholar]
Drubin D. G., Nelson W. J., 1996. Origins of cell polarity. Cell 84: 335–344 [DOI] [PubMed] [Google Scholar]
Dunn T. M., Shortle D., 1990. Null alleles of SAC7 suppress temperature-sensitive actin mutations in Saccharomyces cerevisiae. Mol. Cell. Biol. 10: 2308–2314 [DOI] [PMC free article] [PubMed] [Google Scholar]
Eaton S., Auvinen P., Luo L., Jan Y. N., Simons K., 1995. CDC42 and Rac1 control different actin-dependent processes in the Drosophila wing disc epithelium. J. Cell Biol. 131: 151–164 [DOI] [PMC free article] [PubMed] [Google Scholar]
Egelhofer T. A., Villen J., McCusker D., Gygi S. P., Kellogg D. R., 2008. The septins function in G1 pathways that influence the pattern of cell growth in budding yeast. PLoS ONE 3: e2022. [DOI] [PMC free article] [PubMed] [Google Scholar]
Eggert U. S., Mitchison T. J., Field C. M., 2006. Animal cytokinesis: from parts list to mechanisms. Annu. Rev. Biochem. 75: 543–566 [DOI] [PubMed] [Google Scholar]
Eitzen G., Thorngren N., Wickner W., 2001. Rho1p and Cdc42p act after Ypt7p to regulate vacuole docking. EMBO J. 20: 5650–5656 [DOI] [PMC free article] [PubMed] [Google Scholar]
Engqvist-Goldstein A. E., Drubin D. G., 2003. Actin assembly and endocytosis: from yeast to mammals. Annu. Rev. Cell Dev. Biol. 19: 287–332 [DOI] [PubMed] [Google Scholar]
Epp J. A., Chant J., 1997. An IQGAP-related protein controls actin-ring formation and cytokinesis in yeast. Curr. Biol. 7: 921–929 [DOI] [PubMed] [Google Scholar]
Estrada P., Kim J., Coleman J., Walker L., Dunn B., et al. , 2003. Myo4p and She3p are required for cortical ER inheritance in Saccharomyces cerevisiae. J. Cell Biol. 163: 1255–1266 [DOI] [PMC free article] [PubMed] [Google Scholar]
Etienne-Manneville S., 2004. Cdc42–the centre of polarity. J. Cell Sci. 117: 1291–1300 [DOI] [PubMed] [Google Scholar]
Evangelista M., Blundell K., Longtine M. S., Chow C. J., Adames N., et al. , 1997. Bni1p, a yeast formin linking Cdc42p and the actin cytoskeleton during polarized morphogenesis. Science 276: 118–122 [DOI] [PubMed] [Google Scholar]
Evangelista M., Pruyne D., Amberg D. C., Boone C., Bretscher A., 2002. Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat. Cell Biol. 4: 32–41 [DOI] [PubMed] [Google Scholar]
Fang X., Luo J., Nishihama R., Wloka C., Dravis C., et al. , 2010. Biphasic targeting and cleavage furrow ingression directed by the tail of a myosin-II. J. Cell Biol. 191: 1333–1350 [DOI] [PMC free article] [PubMed] [Google Scholar]
Farkas V., Kovarik J., Kosinova A., Bauer S., 1974. Autoradiographic study of mannan incorporation into the growing cell walls of Saccharomyces cerevisiae. J. Bacteriol. 117: 265–269 [DOI] [PMC free article] [PubMed] [Google Scholar]
Finger F. P., Novick P., 1997. Sec3p is involved in secretion and morphogenesis in Saccharomyces cerevisiae. Mol. Biol. Cell 8: 647–662 [DOI] [PMC free article] [PubMed] [Google Scholar]
Finger F. P., Hughes T. E., Novick P., 1998. Sec3p is a spatial landmark for polarized secretion in budding yeast. Cell 92: 559–571 [DOI] [PubMed] [Google Scholar]
Fitch P. G., Gammie A. E., Lee D. J., de Candal V. B., Rose M. D., 2004. Lrg1p Is a Rho1 GTPase-activating protein required for efficient cell fusion in yeast. Genetics 168: 733–746 [DOI] [PMC free article] [PubMed] [Google Scholar]
Flescher E. G., Madden K., Snyder M., 1993. Components required for cytokinesis are important for bud site selection in yeast. J. Cell Biol. 122: 373–386 [DOI] [PMC free article] [PubMed] [Google Scholar]
France Y. E., Boyd C., Coleman J., Novick P. J., 2006. The polarity-establishment component Bem1p interacts with the exocyst complex through the Sec15p subunit. J. Cell Sci. 119: 876–888 [DOI] [PubMed] [Google Scholar]
Frazier J. A., Wong M. L., Longtine M. S., Pringle J. R., Mann M., et al. , 1998. Polymerization of purified yeast septins: evidence that organized filament arrays may not be required for septin function. J. Cell Biol. 143: 737–749 [DOI] [PMC free article] [PubMed] [Google Scholar]
Freifelder D., 1960. Bud position in Saccharomyces cerevisiae. J. Bacteriol. 80: 567–568 [DOI] [PMC free article] [PubMed] [Google Scholar]
Fujita A., Oka C., Arikawa Y., Katagai T., Tonouchi A., et al. , 1994. A yeast gene necessary for bud-site selection encodes a protein similar to insulin-degrading enzymes. Nature 372: 567–570 [DOI] [PubMed] [Google Scholar]
Fujita A., Lord M., Hiroko T., Hiroko F., Chen T., et al. , 2004. Rax1, a protein required for the establishment of the bipolar budding pattern in yeast. Gene 327: 161–169 [DOI] [PubMed] [Google Scholar]
Fujiwara T., Tanaka K., Mino A., Kikyo M., Takahashi K., et al. , 1998. Rho1p-Bni1p-Spa2p interactions: implication in localization of Bni1p at the bud site and regulation of the actin cytoskeleton in Saccharomyces cerevisiae. Mol. Biol. Cell 9: 1221–1233 [DOI] [PMC free article] [PubMed] [Google Scholar]
Fukumoto Y., Kaibuchi K., Hori Y., Fujioka H., Araki S., et al. , 1990. Molecular cloning and characterization of a novel type of regulatory protein (GDI) for the rho proteins, ras p21-like small GTP-binding proteins. Oncogene 5: 1321–1328 [PubMed] [Google Scholar]
Gao L., Liu W., Bretscher A., 2010. The yeast formin Bnr1p has two localization regions that show spatially and temporally distinct association with septin structures. Mol. Biol. Cell 21: 1253–1262 [DOI] [PMC free article] [PubMed] [Google Scholar]
Gao X. D., Albert S., Tcheperegine S. E., Burd C. G., Gallwitz D., et al. , 2003. The GAP activity of Msb3p and Msb4p for the Rab GTPase Sec4p is required for efficient exocytosis and actin organization. J. Cell Biol. 162: 635–646 [DOI] [PMC free article] [PubMed] [Google Scholar]
Gao X. D., Sperber L. M., Kane S. A., Tong Z., Hin Yan Tong A., et al. , 2007. Sequential and distinct roles of the cadherin domain-containing protein Axl2p in cell polarization in yeast cell cycle. Mol. Biol. Cell 18: 2542–2560 [DOI] [PMC free article] [PubMed] [Google Scholar]
Garrenton L. S., Stefan C. J., McMurray M. A., Emr S. D., Thorner J., 2010. Pheromone-induced anisotropy in yeast plasma membrane phosphatidylinositol-4,5-bisphosphate distribution is required for MAPK signaling. Proc. Natl. Acad. Sci. USA 107: 11805–11810 [DOI] [PMC free article] [PubMed] [Google Scholar]
Geli M. I., Riezman H., 1996. Role of type I myosins in receptor-mediated endocytosis in yeast. Science. 272: 533–535 [DOI] [PubMed] [Google Scholar]
Geli M. I., Lombardi R., Schmelzl B., Riezman H., 2000. An intact SH3 domain is required for myosin I-induced actin polymerization. EMBO J. 19: 4281–4291 [DOI] [PMC free article] [PubMed] [Google Scholar]
Gladfelter A. S., Pringle J. R., Lew D. J., 2001. The septin cortex at the yeast mother-bud neck. Curr. Opin. Microbiol. 4: 681–689 [DOI] [PubMed] [Google Scholar]
Gladfelter A. S., Bose I., Zyla T. R., Bardes E. S. G., Lew D. J., 2002. Septin ring assembly involves cycles of GTP loading and hydrolysis by Cdc42p. J. Cell Biol. 156: 315–326 [DOI] [PMC free article] [PubMed] [Google Scholar]
Gladfelter, A. S., T. R. Zyla, and D. J. Lew, 2004. Genetic interactions among regulators of septin organization. Eukaryot. Cell 3: 847–854 [DOI] [PMC free article] [PubMed] [Google Scholar]
Goehring A. S., Mitchell D. A., Tong A. H., Keniry M. E., Boone C., et al. , 2003. Synthetic lethal analysis implicates Ste20p, a p21-activated potein kinase, in polarisome activation. Mol. Biol. Cell 14: 1501–1516 [DOI] [PMC free article] [PubMed] [Google Scholar]
Goodman A., Goode B. L., Matsudaira P., Fink G. R., 2003. The Saccharomyces cerevisiae calponin/transgelin homolog Scp1 functions with fimbrin to regulate stability and organization of the actin cytoskeleton. Mol. Biol. Cell 14: 2617–2629 [DOI] [PMC free article] [PubMed] [Google Scholar]
Goodson H. V., Anderson B. L., Warrick H. M., Pon L. A., Spudich J. A., 1996. Synthetic lethality screen identifies a novel yeast myosin I gene (MYO5): myosin I proteins are required for polarization of the actin cytoskeleton. J. Cell Biol. 133: 1277–1291 [DOI] [PMC free article] [PubMed] [Google Scholar]
Goryachev A. B., Pokhilko A. V., 2008. Dynamics of Cdc42 network embodies a Turing-type mechanism of yeast cell polarity. FEBS Lett. 582: 1437–1443 [DOI] [PubMed] [Google Scholar]
Goud B., Salminen A., Walworth N. C., Novick P. J., 1988. A GTP-binding protein required for secretion rapidly associates with secretory vesicles and plasma membrane in yeast. Cell 53: 753–768 [DOI] [PubMed] [Google Scholar]
Govindan B., Bowser R., Novick P., 1995. The role of Myo2, a yeast class V myosin, in vesicular transport. J. Cell Biol. 128: 1055–1068 [DOI] [PMC free article] [PubMed] [Google Scholar]
Grosshans B. L., Ortiz D., Novick P., 2006. Rabs and their effectors: achieving specificity in membrane traffic. Proc. Natl. Acad. Sci. USA 103: 11821–11827 [DOI] [PMC free article] [PubMed] [Google Scholar]
Gulli M.-P., Jaquenoud M., Shimada Y., Niederhauser G., Wiget P., et al. , 2000. Phosphorylation of the Cdc42 exchange factor Cdc24 by the Pak-like kinase Cla4 may regulate polarized growth in yeast. Mol. Cell 6: 1155–1167 [DOI] [PubMed] [Google Scholar]
Guo W., Grant A., Novick P., 1999a. Exo84p is an exocyst protein essential for secretion. J. Biol. Chem. 274: 23558–23564 [DOI] [PubMed] [Google Scholar]
Guo W., Roth D., Walch-Solimena C., Novick P., 1999b. The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J. 18: 1071–1080 [DOI] [PMC free article] [PubMed] [Google Scholar]
Guo W., Sacher M., Barrowman J., Ferro-Novick S., Novick P., 2000. Protein complexes in transport vesicle targeting. Trends Cell Biol. 10: 251–255 [DOI] [PubMed] [Google Scholar]
Guo W., Tamanoi F., Novick P., 2001. Spatial regulation of the exocyst complex by Rho1 GTPase. Nat. Cell Biol. 3: 353–360 [DOI] [PubMed] [Google Scholar]
Haarer B. K., Pringle J. R., 1987. Immunofluorescence localization of the Saccharomyces cerevisiae CDC12 gene product to the vicinity of the 10-nm filaments in the mother-bud neck. Mol. Cell. Biol. 7: 3678–3687 [DOI] [PMC free article] [PubMed] [Google Scholar]
Haarer B. K., Lillie S. H., Adams A. E., Magdolen V., Bandlow W., et al. , 1990. Purification of profilin from Saccharomyces cerevisiae and analysis of profilin-deficient cells. J. Cell Biol. 110: 105–114 [DOI] [PMC free article] [PubMed] [Google Scholar]
Haarer B. K., Corbett A., Kweon Y., Petzold A. S., Silver P., et al. , 1996. SEC3 mutations are synthetically lethal with profilin mutations and cause defects in diploid-specific bud-site selection. Genetics 144: 495–510 [DOI] [PMC free article] [PubMed] [Google Scholar]
Hall P. A., Russell S. E. H., Pringle J. R., 2008. The Septins. John Wiley & Sons, New York [Google Scholar]
Halme A., Michelitch M., Mitchell E. L., Chant J., 1996. Bud10p directs axial cell polarization in budding yeast and resembles a transmembrane receptor. Curr. Biol. 6: 570–579 [DOI] [PubMed] [Google Scholar]
Hancock J. F., Hall A., 1993. A novel role for RhoGDI as an inhibitor of GAP proteins. EMBO J. 12: 1915–1921 [DOI] [PMC free article] [PubMed] [Google Scholar]
Harkins H. A., Pagé N., Schenkman L. R., De Virgilio C., Shaw S., et al. , 2001. Bud8p and Bud9p, proteins that may mark the sites for bipolar budding in yeast. Mol. Biol. Cell 12: 2497–2518 [DOI] [PMC free article] [PubMed] [Google Scholar]
Hart M. J., Maru Y., Leonard D., Witte O. N., Evans T., et al. , 1992. A GDP dissociation inhibitor that serves as a GTPase inhibitor for the Ras-like protein CDC42Hs. Science 258: 812–815 [DOI] [PubMed] [Google Scholar]
Hartwell L. H., 1971a. Genetic control of the cell division cycle in yeast II. Genes controlling DNA replication and its initiation. J. Mol. Biol. 59: 183–194 [DOI] [PubMed] [Google Scholar]
Hartwell L. H., 1971b. Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis. Exp. Cell Res. 69: 265–276 [DOI] [PubMed] [Google Scholar]
He B., Xi F., Zhang X., Zhang J., Guo W., 2007. Exo70 interacts with phospholipids and mediates the targeting of the exocyst to the plasma membrane. EMBO J. 26: 4053–4065 [DOI] [PMC free article] [PubMed] [Google Scholar]
Heinisch J. J., Lorberg A., Schmitz H. P., Jacoby J. J., 1999. The protein kinase C-mediated MAP kinase pathway involved in the maintenance of cellular integrity in Saccharomyces cerevisiae. Mol. Microbiol. 32: 671–680 [DOI] [PubMed] [Google Scholar]
Helliwell S. B., Schmidt A., Ohya Y., Hall M. N., 1998. The Rho1 effector Pkc1, but not Bni1, mediates signalling from Tor2 to the actin cytoskeleton. Curr. Biol. 8: 1211–1214 [DOI] [PubMed] [Google Scholar]
Hergovich A., Hemmings B. A., 2009. Mammalian NDR/LATS protein kinases in hippo tumor suppressor signaling. Biofactors 35: 338–345 [DOI] [PubMed] [Google Scholar]
Herskowitz I., 1988. Life cycle of the budding yeast Saccharomyces cerevisiae. Microbiol. Rev. 52: 536–553 [DOI] [PMC free article] [PubMed] [Google Scholar]
Hicks J. B., Strathern J. N., Herskowitz I., 1977. Interconversion of yeast mating types III. Action of the homothallism (HO) gene in cells homozygous for the mating type locus. Genetics 85: 395–405 [DOI] [PMC free article] [PubMed] [Google Scholar]
Hofken T., Schiebel E., 2002. A role for cell polarity proteins in mitotic exit. EMBO J. 21: 4851–4862 [DOI] [PMC free article] [PubMed] [Google Scholar]
Holt L. J., Tuch B. B., Villen J., Johnson A. D., Gygi S. P., et al. , 2009. Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution. Science 325: 1682–1686 [DOI] [PMC free article] [PubMed] [Google Scholar]
Hori Y., Kikuchi A., Isomura M., Katayama M., Miura Y., et al. , 1991. Post-translational modifications of the C-terminal region of the Rho protein are important for its interaction with membranes and the stimulatory and inhibitory GDP/GTP exchange proteins. Oncogene 6: 515–522 [PubMed] [Google Scholar]
Howell A. S., Lew D. J. 2012. Morphogenesis and the cell cycle. Genetics 190:51–77 [DOI] [PMC free article] [PubMed] [Google Scholar]
Howell A. S., Savage N. S., Johnson S. A., Bose I., Wagner A. W., et al. , 2009. Singularity in polarization: rewiring yeast cells to make two buds. Cell 139: 731–743 [DOI] [PMC free article] [PubMed] [Google Scholar]
Huckaba T. M., Lipkin T., Pon L. A., 2006. Roles of type II myosin and a tropomyosin isoform in retrograde actin flow in budding yeast. J. Cell Biol. 175: 957–969 [DOI] [PMC free article] [PubMed] [Google Scholar]
Huh W. K., Falvo J. V., Gerke L. C., Carroll A. S., Howson R. W., et al. , 2003. Global analysis of protein localization in budding yeast. Nature 425: 686–691 [DOI] [PubMed] [Google Scholar]
Hutagalung A. H., Novick P. J., 2011. Role of Rab GTPases in membrane traffic and cell physiology. Physiol. Rev. 91: 119–149 [DOI] [PMC free article] [PubMed] [Google Scholar]
Huxley H., Hanson J., 1954. Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature 173: 973–976 [DOI] [PubMed] [Google Scholar]
Huxley H. E., 1969. The mechanism of muscular contraction. Science 164: 1356–1365 [PubMed] [Google Scholar]
Imamura H., Tanaka K., Hihara T., Umikawa M., Kamei T., et al. , 1997. Bni1p and Bnr1p: downstream targets of the Rho family small G-proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae. EMBO J. 16: 2745–2755 [DOI] [PMC free article] [PubMed] [Google Scholar]
Inoue S. B., Takewaki N., Takasuka T., Mio T., Adachi M., et al. , 1995. Characterization and gene cloning of 1,3-beta-D-glucan synthase from Saccharomyces cerevisiae. Eur. J. Biochem. 231: 845–854 [DOI] [PubMed] [Google Scholar]
Irazoqui J. E., Gladfelter A. S., Lew D. J., 2003. Scaffold-mediated symmetry breaking by Cdc42p. Nat. Cell Biol. 5: 1062–1070 [DOI] [PubMed] [Google Scholar]
Irazoqui J. E., Howell A. S., Theesfeld C. L., Lew D. J., 2005. Opposing roles for actin in Cdc42p polarization. Mol. Biol. Cell 16: 1296–1304 [DOI] [PMC free article] [PubMed] [Google Scholar]
Irie K., Takase M., Lee K. S., Levin D. E., Araki H., et al. , 1993. MKK1 and MKK2, which encode Saccharomyces cerevisiae mitogen-activated protein kinase-kinase homologs, function in the pathway mediated by protein kinase C. Mol. Cell. Biol. 13: 3076–3083 [DOI] [PMC free article] [PubMed] [Google Scholar]
Ishihara S., Hirata A., Nogami S., Beauvais A., Latge J. P., et al. , 2007. Homologous subunits of 1,3-beta-glucan synthase are important for spore wall assembly in Saccharomyces cerevisiae. Eukaryot. Cell 6: 143–156 [DOI] [PMC free article] [PubMed] [Google Scholar]
Ishimi Y., Kikuchi A., 1991. Identification and molecular cloning of yeast homolog of nucleosome assembly protein I which facilitates nucleosome assembly in vitro. J. Biol. Chem. 266: 7025–7029 [PubMed] [Google Scholar]
Iwase M., Toh-e A., 2001. Nis1 encoded by YNL078W: a new neck protein of Saccharomyces cerevisiae. Genes Genet. Syst. 76: 335–343 [DOI] [PubMed] [Google Scholar]
Iwase M., Luo J., Nagaraj S., Longtine M., Kim H. B., et al. , 2006. Role of a cdc42p effector pathway in recruitment of the yeast septins to the presumptive bud site. Mol. Biol. Cell 17: 1110–1125 [DOI] [PMC free article] [PubMed] [Google Scholar]
Iwase M., Luo J., Bi E., Toh-e A., 2007. Shs1 plays separable roles in septin organization and cytokinesis in Saccharomyces cerevisiae. Genetics 177: 215–229 [DOI] [PMC free article] [PubMed] [Google Scholar]
Jaquenoud M., Peter M., 2000. Gic2p may link activated Cdc42p to components involved in actin polarization, including Bni1p and Bud6p (Aip3p). Mol. Cell. Biol. 20: 6244–6258 [DOI] [PMC free article] [PubMed] [Google Scholar]
Jaquenoud M., Gulli M. P., Peter K., Peter M., 1998. The Cdc42p effector Gic2p is targeted for ubiquitin-dependent degradation by the SCFGrr1 complex. EMBO J. 17: 5360–5373 [DOI] [PMC free article] [PubMed] [Google Scholar]
Jedd G., Mulholland J., Segev N., 1997. Two new Ypt GTPases are required for exit from the yeast trans-Golgi compartment. J. Cell Biol. 137: 563–580 [DOI] [PMC free article] [PubMed] [Google Scholar]
Jendretzki A., Ciklic I., Rodicio R., Schmitz H. P., Heinisch J. J., 2009. Cyk3 acts in actomyosin ring independent cytokinesis by recruiting Inn1 to the yeast bud neck. Mol. Genet. Genomics 282: 437–451 [DOI] [PubMed] [Google Scholar]
Joberty G., Perlungher R. R., Sheffield P. J., Kinoshita M., Noda M., et al. , 2001. Borg proteins control septin organization and are negatively regulated by Cdc42. Nat. Cell Biol. 3: 861–866 [DOI] [PubMed] [Google Scholar]
Johnson D. I., Pringle J. R., 1990. Molecular characterization of CDC42, a Saccharomyces cerevisiae gene involved in the development of cell polarity. J. Cell Biol. 111: 143–152 [DOI] [PMC free article] [PubMed] [Google Scholar]
Johnson E. S., Blobel G., 1999. Cell cycle-regulated attachment of the ubiquitin-related protein SUMO to the yeast septins. J. Cell Biol. 147: 981–993 [DOI] [PMC free article] [PubMed] [Google Scholar]
Johnson E. S., Gupta A. A., 2001. An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106: 735–744 [DOI] [PubMed] [Google Scholar]
Johnson J. L., Erickson J. W., Cerione R. A., 2009. New insights into how the Rho guanine nucleotide dissociation inhibitor regulates the interaction of Cdc42 with membranes. J. Biol. Chem. 284: 23860–23871 [DOI] [PMC free article] [PubMed] [Google Scholar]
Johnston G. C., Prendergast J. A., Singer R. A., 1991. The Saccharomyces cerevisiae MYO2 gene encodes an essential myosin for vectorial transport of vesicles. J. Cell Biol. 113: 539–551 [DOI] [PMC free article] [PubMed] [Google Scholar]
Kadota J., Yamamoto T., Yoshiuchi S., Bi E., Tanaka K., 2004. Septin ring assembly requires concerted action of polarisome components, a PAK kinase Cla4p, and the actin cytoskeleton in Saccharomyces cerevisiae. Mol. Biol. Cell 15: 5329–5345 [DOI] [PMC free article] [PubMed] [Google Scholar]
Kaksonen M., Sun Y., Drubin D. G., 2003. A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 115: 475–487 [DOI] [PubMed] [Google Scholar]
Kaksonen M., Toret C. P., Drubin D. G., 2005. A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123: 305–320 [DOI] [PubMed] [Google Scholar]
Kaksonen M., Toret C. P., Drubin D. G., 2006. Harnessing actin dynamics for clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 7: 404–414 [DOI] [PubMed] [Google Scholar]
Kamada Y., Jung U. S., Piotrowski J., Levin D. E., 1995. The protein kinase C-activated MAP kinase pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response. Genes Dev. 9: 1559–1571 [DOI] [PubMed] [Google Scholar]
Kamada Y., Qadota H., Python C. P., Anraku Y., Ohya Y., et al. , 1996. Activation of yeast protein kinase C by Rho1 GTPase. J. Biol. Chem. 271: 9193–9196 [DOI] [PubMed] [Google Scholar]
Kamei T., Tanaka K., Hihara T., Umikawa M., Imamura H., et al. , 1998. Interaction of Bnr1p with a novel Src Homology 3 domain-containing Hof1p. Implication in cytokinesis in Saccharomyces cerevisiae. J. Biol. Chem. 273: 28341–28345 [DOI] [PubMed] [Google Scholar]
Kang P. J., Sanson A., Lee B., Park H.-O., 2001. A GDP/GTP exchange factor involved in linking a spatial landmark to cell polarity. Science 292: 1376–1378 [DOI] [PMC free article] [PubMed] [Google Scholar]
Kang P. J., Angerman E., Nakashima K., Pringle J. R., Park H.-O., 2004a. Interactions among Rax1p, Rax2p, Bud8p, and Bud9p in marking cortical sites for bipolar bud-site selection in yeast. Mol. Biol. Cell 15: 5145–5157 [DOI] [PMC free article] [PubMed] [Google Scholar]
Kang P. J., Lee B., Park H.-O., 2004b. Specific residues of the GDP/GTP exchange factor Bud5p are involved in establishment of the cell type-specific budding pattern in yeast. J. Biol. Chem. 279: 27980–27985 [DOI] [PubMed] [Google Scholar]
Kang P. J., Beven L., Hariharan S., Park H.-O., 2010. The Rsr1/Bud1 GTPase interacts with itself and the Cdc42 GTPase during bud-site selection and polarity establishment in budding yeast. Mol. Biol. Cell 21: 3007–3016 [DOI] [PMC free article] [PubMed] [Google Scholar]
Kang P. J., Angerman E., Jung C.-H., Park H.-O., 2012. Bud4 mediates the cell-type-specific assembly of the axial landmark in budding yeast. J. Cell Sci. (in press) [DOI] [PMC free article] [PubMed] [Google Scholar]
Karpova T. S., McNally J. G., Moltz S. L., Cooper J. A., 1998. Assembly and function of the actin cytoskeleton of yeast: relationships between cables and patches. J. Cell Biol. 142: 1501–1517 [DOI] [PMC free article] [PubMed] [Google Scholar]
Kawasaki R., Fujimura-Kamada K., Toi H., Kato H., Tanaka K., 2003. The upstream regulator, Rsr1p, and downstream effector, Gic1p and Gic2p, of the Cdc42p small GTPase coordinately regulate initiation of budding in Saccharomyces cerevisiae. Genes Cells 8: 235–250 [DOI] [PubMed] [Google Scholar]
Kellogg D. R., Kikuchi A., Fujii-Nakata T., Turck C. W., Murray A. W., 1995. Members of the NAP/SET family of proteins interact specifically with B-type cyclins. J. Cell Biol. 130: 661–673 [DOI] [PMC free article] [PubMed] [Google Scholar]
Kikyo M., Tanaka K., Kamei T., Ozaki K., Fujiwara T., et al. , 1999. An FH domain-containing Bnr1p is a multifunctional protein interacting with a variety of cytoskeletal proteins in Saccharomyces cerevisiae. Oncogene 18: 7046–7054 [DOI] [PubMed] [Google Scholar]
Kim Y.-J., Francisco L., Chen G.-C., Marcotte E., Chan C. S. M., 1994. Control of cellular morphogenesis by the Ipl2/Bem2 GTPase-activating protein: Possible role of protein phosphorylation. J. Cell Biol. 127: 1381–1394 [DOI] [PMC free article] [PubMed] [Google Scholar]
Klis F. M., Boorsma A., De Groot P. W., 2006. Cell wall construction in Saccharomyces cerevisiae. Yeast 23: 185–202 [DOI] [PubMed] [Google Scholar]
Knaus M., Pelli-Gulli M. P., van Drogen F., Springer S., Jaquenoud M., et al. , 2007. Phosphorylation of Bem2p and Bem3p may contribute to local activation of Cdc42p at bud emergence. EMBO J. 26: 4501–4513 [DOI] [PMC free article] [PubMed] [Google Scholar]
Knoblich J. A., 2010. Asymmetric cell division: recent developments and their implications for tumour biology. Nat. Rev. Mol. Cell Biol. 11: 849–860 [DOI] [PMC free article] [PubMed] [Google Scholar]
Ko N., Nishihama R., Tully G. H., Ostapenko D., Solomon M. J., et al. , 2007. Identification of yeast IQGAP (Iqg1p) as an anaphase-promoting-complex substrate and its role in actomyosin-ring-independent cytokinesis. Mol. Biol. Cell 18: 5139–5153 [DOI] [PMC free article] [PubMed] [Google Scholar]
Koch G., Tanaka K., Masuda T., Yamochi W., Nonaka H., et al. , 1997. Association of the Rho family small GTP-binding proteins with Rho GDP dissociation inhibitor (Rho GDI) in Saccharomyces cerevisiae. Oncogene 15: 417–422 [DOI] [PubMed] [Google Scholar]
Kohno H., Tanaka K., Mino A., Umikawa M., Imamura H., et al. , 1996. Bni1p implicated in cytoskeletal control is a putative target of Rho1p small GTP binding protein in Saccharomyces cerevisiae. EMBO J. 15: 6060–6068 [PMC free article] [PubMed] [Google Scholar]
Korinek W. S., Bi E., Epp J. A., Wang L., Ho J., et al. , 2000. Cyk3, a novel SH3-domain protein, affects cytokinesis in yeast. Curr. Biol. 10: 947–950 [DOI] [PubMed] [Google Scholar]
Kost B., 2008. Spatial control of Rho (Rac-Rop) signaling in tip-growing plant cells. Trends Cell Biol. 18: 119–127 [DOI] [PubMed] [Google Scholar]
Kovar D. R., Sirotkin V., Lord M., 2011. Three’s company: the fission yeast actin cytoskeleton. Trends Cell Biol. 21: 177–187 [DOI] [PMC free article] [PubMed] [Google Scholar]
Kozminski K. G., Beven L., Angerman E., Tong A. H. Y., Boone C., et al. , 2003. Interaction between a Ras and a Rho GTPase couples selection of a growth site to the development of cell polarity in yeast. Mol. Biol. Cell 14: 4958–4970 [DOI] [PMC free article] [PubMed] [Google Scholar]
Kozubowski L., Larson J. R., Tatchell K., 2005. Role of the septin ring in the asymmetric localization of proteins at the mother-bud neck in Saccharomyces cerevisiae. Mol. Biol. Cell 16: 3455–3466 [DOI] [PMC free article] [PubMed] [Google Scholar]
Kozubowski L., Saito K., Johnson J. M., Howell A. S., Zyla T. R., et al. , 2008. Symmetry-breaking polarization driven by a Cdc42p GEF-PAK complex. Curr. Biol. 18: 1719–1726 [DOI] [PMC free article] [PubMed] [Google Scholar]
Krappmann A.-B., Taheri N., Heinrich M., Mosch H.-U., 2007. Distinct domains of yeast cortical tag proteins Bud8p and Bud9p confer polar localization and functionality. Mol. Biol. Cell 18: 3323–3339 [DOI] [PMC free article] [PubMed] [Google Scholar]
Laporte D., Coffman V. C., Lee I. J., Wu J. Q., 2011. Assembly and architecture of precursor nodes during fission yeast cytokinesis. J. Cell Biol. 192: 1005–1021 [DOI] [PMC free article] [PubMed] [Google Scholar]
Layton A. T., Savage N. S., Howell A. S., Carroll S. Y., Drubin D. G., et al. , 2011. Modeling vesicle traffic reveals unexpected consequences for cdc42p-mediated polarity establishment. Curr. Biol. 21: 184–194 [DOI] [PMC free article] [PubMed] [Google Scholar]
Leberer E., Dignard D., Harcus D., Thomas D. Y., Whiteway M., 1992. The protein kinase homologue Ste20p is required to link the yeast pheromone response G-protein βγ subunits to downstream signalling components. EMBO J. 11: 4815–4824 [DOI] [PMC free article] [PubMed] [Google Scholar]
Lechler T., Jonsdottir G. A., Klee S. K., Pellman D., Li R., 2001. A two-tiered mechanism by which Cdc42 controls the localization and activation of an Arp2/3-activating motor complex in yeast. J. Cell Biol. 155: 261–270 [DOI] [PMC free article] [PubMed] [Google Scholar]
Lee K. S., Levin D. E., 1992. Dominant mutations in a gene encoding a putative protein kinase (BCK1) bypass the requirement for a Saccharomyces cerevisiae protein kinase C homolog. Mol. Cell. Biol. 12: 172–182 [DOI] [PMC free article] [PubMed] [Google Scholar]
Lee K. S., Irie K., Gotoh Y., Watanabe Y., Araki H., et al. , 1993. A yeast mitogen-activated protein kinase homolog (Mpk1p) mediates signalling by protein kinase C. Mol. Cell. Biol. 13: 3067–3075 [DOI] [PMC free article] [PubMed] [Google Scholar]
Lee L., Klee S. K., Evangelista M., Boone C., Pellman D., 1999. Control of mitotic spindle position by the Saccharomyces cerevisiae formin Bni1p. J. Cell Biol. 144: 947–961 [DOI] [PMC free article] [PubMed] [Google Scholar]
Lee M. E., Singh K., Snider J., Shenoy A., Paumi C. M., et al. , 2011. The Rho1 GTPase acts together with a vacuolar glutathione S-conjugate transporter to protect yeast cells from oxidative stress. Genetics 188: 859–870 [DOI] [PMC free article] [PubMed] [Google Scholar]
Lee P. R., Song S., Ro H. S., Park C. J., Lippincott J., et al. , 2002. Bni5p, a septin-interacting protein, is required for normal septin function and cytokinesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 22: 6906–6920 [DOI] [PMC free article] [PubMed] [Google Scholar]
Leeuw T., Fourest-Lieuvin A., Wu C., Chenevert J., Clark K., et al. , 1995. Pheromone response in yeast: association of Bem1p with proteins of the MAP kinase cascade and actin. Science 270: 1210–1213 [DOI] [PubMed] [Google Scholar]
Leeu w, T., Wu C., Schrag J. D., Whiteway M., Thomas D. Y., et al. , 1998. Interaction of a G-protein b-subunit with a conserved sequence in Ste20/PAK family protein kinases. Nature 391: 191–195 [DOI] [PubMed] [Google Scholar]
Leonard D., Hart M. J., Platko J. V., Eva A., Henzel W., et al. , 1992. The identification and characterization of a GDP-dissociation inhibitor (GDI) for the CDC42Hs protein. J. Biol. Chem. 267: 22860–22868 [PubMed] [Google Scholar]
Lesage G., Bussey H., 2006. Cell wall assembly in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 70: 317–343 [DOI] [PMC free article] [PubMed] [Google Scholar]
Levin D. E., 2005. Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69: 262–291 [DOI] [PMC free article] [PubMed] [Google Scholar]
Levin D. E., Bartlett-Heubusch E., 1992. Mutants in the S. cerevisiae PKC1 gene display a cell cycle-specific osmotic stability defect. J. Cell Biol. 116: 1221–1229 [DOI] [PMC free article] [PubMed] [Google Scholar]
Levin D. E., Fields F. O., Kunisawa R., Bishop J. M., Thorner J., 1990. A candidate protein kinase C gene, PKC1, is required for the S. cerevisiae cell cycle. Cell 62: 213–224 [DOI] [PubMed] [Google Scholar]
Levin D. E., Bowers B., Chen C. Y., Kamada Y., Watanabe M., 1994. Dissecting the protein kinase C/MAP kinase signalling pathway of Saccharomyces cerevisiae. Cell. Mol. Biol. Res. 40: 229–239 [PubMed] [Google Scholar]
Lew D. J., Reed S. I., 1993. Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins. J. Cell Biol. 120: 1305–1320 [DOI] [PMC free article] [PubMed] [Google Scholar]
Li R., 1997. Bee1, a yeast protein with homology to Wiscott-Aldrich syndrome protein, is critical for the assembly of cortical actin cytoskeleton. J. Cell Biol. 136: 649–658 [DOI] [PMC free article] [PubMed] [Google Scholar]
Lillie S. H., Brown S. S., 1994. Immunofluorescence localization of the unconventional myosin, Myo2p, and the putative kinesin-related protein, Smy1p, to the same regions of polarized growth in Saccharomyces cerevisiae. J. Cell Biol. 125: 825–842 [DOI] [PMC free article] [PubMed] [Google Scholar]
Lin M., Unden H., Jacquier N., Schneiter R., Just U., et al. , 2009. The Cdc42 effectors Ste20, Cla4, and Skm1 down-regulate the expression of genes involved in sterol uptake by a mitogen-activated protein kinase-independent pathway. Mol. Biol. Cell 20: 4826–4837 [DOI] [PMC free article] [PubMed] [Google Scholar]
Lippincott J., Li R., 1998a. Sequential assembly of myosin II, an IQGAP-like protein, and filamentous actin to a ring structure involved in budding yeast cytokinesis. J. Cell Biol. 140: 355–366 [DOI] [PMC free article] [PubMed] [Google Scholar]
Lippincott J., Li R., 1998b. Dual function of Cyk2, a cdc15/PSTPIP family protein, in regulating actomyosin ring dynamics and septin distribution. J. Cell Biol. 143: 1947–1960 [DOI] [PMC free article] [PubMed] [Google Scholar]
Lippincott J., Shannon K. B., Shou W., Deshaies R. J., Li R., 2001. The Tem1 small GTPase controls actomyosin and septin dynamics during cytokinesis. J. Cell Sci. 114: 1379–1386 [DOI] [PubMed] [Google Scholar]
Liu H. P., Bretscher A., 1989a. Disruption of the single tropomyosin gene in yeast results in the disappearance of actin cables from the cytoskeleton. Cell 57: 233–242 [DOI] [PubMed] [Google Scholar]
Liu H. P., Bretscher A., 1989b. Purification of tropomyosin from Saccharomyces cerevisiae and identification of related proteins in Schizosaccharomyces and Physarum. Proc. Natl. Acad. Sci. USA 86: 90–93 [DOI] [PMC free article] [PubMed] [Google Scholar]
Logan M. R., Jones L., Forsberg D., Bodman A., Baier A., et al. , 2011. Functional analysis of RhoGDI inhibitory activity on vacuole membrane fusion. Biochem. J. 434: 445–457 [DOI] [PubMed] [Google Scholar]
Longtine M., Bi E., 2003. Regulation of septin organization and function in yeast. Trends Cell Biol. 13: 403–409 [DOI] [PubMed] [Google Scholar]
Longtine M. S., DeMarini D. J., Valencik M. L., Al-Awar O. S., Fares H., et al. , 1996. The septins: roles in cytokinesis and other processes. Curr. Opin. Cell Biol. 8: 106–119 [DOI] [PubMed] [Google Scholar]
Longtine M. S., Fares H., Pringle J. R., 1998. Role of the yeast Gin4p protein kinase in septin assembly and the relationship between septin assembly and septin function. J. Cell Biol. 143: 719–736 [DOI] [PMC free article] [PubMed] [Google Scholar]
Longtine M. S., Theesfeld C. L., McMillan J. N., Weaver E., Pringle J. R., et al. , 2000. Septin-dependent assembly of a cell cycle-regulatory module in Saccharomyces cerevisiae. Mol. Cell. Biol. 20: 4049–4061 [DOI] [PMC free article] [PubMed] [Google Scholar]
Lorberg A., Schmitz H. P., Jacoby J. J., Heinisch J. J., 2001. Lrg1p functions as a putative GTPase-activating protein in the Pkc1p-mediated cell integrity pathway in Saccharomyces cerevisiae. Mol. Genet. Genomics 266: 514–526 [DOI] [PubMed] [Google Scholar]
Lord M., Yang M. C., Mischke M., Chant J., 2000. Cell cycle programs of gene expression control morphogenetic protein localization. J. Cell Biol. 151: 1501–1512 [DOI] [PMC free article] [PubMed] [Google Scholar]
Lord M., Inose F., Hiroko T., Hata T., Fujita A., et al. , 2002. Subcellular localization of Axl1, the cell type-specific regulator of polarity. Curr. Biol. 12: 1347–1352 [DOI] [PubMed] [Google Scholar]
Lord M., Laves E., Pollard T. D., 2005. Cytokinesis depends on the motor domains of myosin-II in fission yeast but not in budding yeast. Mol. Biol. Cell 16: 5346–5355 [DOI] [PMC free article] [PubMed] [Google Scholar]
Luo J., Vallen E. A., Dravis C., Tcheperegine S. E., Drees B. L., et al. , 2004. Identification and functional analysis of the essential and regulatory light chains of the only type II myosin Myo1p in Saccharomyces cerevisiae. J. Cell Biol. 165: 843–855 [DOI] [PMC free article] [PubMed] [Google Scholar]
Luo L., Liao Y. J., Jan L. Y., Jan Y. N., 1994. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 8: 1787–1802 [DOI] [PubMed] [Google Scholar]
Madania A., Dumoulin P., Grava S., Kitamoto H., Scharer-Brodbeck C., et al. , 1999. The Saccharomyces cerevisiae homologue of human Wiskott-Aldrich syndrome protein Las17p interacts with the Arp2/3 complex. Mol. Biol. Cell 10: 3521–3538 [DOI] [PMC free article] [PubMed] [Google Scholar]
Madaule P., Axel R., Myers A. M., 1987. Characterization of two members of the RHO gene family from the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 84: 779–783 [DOI] [PMC free article] [PubMed] [Google Scholar]
Manning B. D., Padmanabha R., Snyder M., 1997. The Rho-GEF Rom2p localizes to sites of polarized cell growth and participates in cytoskeletal functions in Saccharomyces cerevisiae. Mol. Biol. Cell 8: 1829–1844 [DOI] [PMC free article] [PubMed] [Google Scholar]
Marquitz A. R., Harrison J. C., Bose I., Zyla T. R., McMillan J. N., et al. , 2002. The Rho-GAP Bem2p plays a GAP-independent role in the morphogenesis checkpoint. EMBO J. 21: 4012–4025 [DOI] [PMC free article] [PubMed] [Google Scholar]
Marston A. L., Chen T., Yang M. C., Belhumeur P., Chant J., 2001. A localized GTPase exchange factor, Bud5, determines the orientation of division axes in yeast. Curr. Biol. 11: 803–807 [DOI] [PubMed] [Google Scholar]
Martin H., Mendoza A., Rodriguez-Pachon J. M., Molina M., Nombela C., 1997. Characterization of SKM1, a Saccharomyces cerevisiae gene encoding a novel Ste20/PAK-like protein kinase. Mol. Microbiol. 23: 431–444 [DOI] [PubMed] [Google Scholar]
Martin H., Rodriguez-Pachon J. M., Ruiz C., Nombela C., Molina M., 2000. Regulatory mechanisms for modulation of signaling through the cell integrity Slt2-mediated pathway in Saccharomyces cerevisiae. J. Biol. Chem. 275: 1511–1519 [DOI] [PubMed] [Google Scholar]
Martinez-Rucobo F. W., Eckhardt-Strelau L., Terwisscha van Scheltinga A. C., 2009. Yeast chitin synthase 2 activity is modulated by proteolysis and phosphorylation. Biochem. J. 417: 547–554 [DOI] [PubMed] [Google Scholar]
Masuda T., Tanaka K., Nonaka H., Yamochi W., Maeda A., et al. , 1994. Molecular cloning and characterization of yeast Rho GDP dissociation inhibitor. J. Biol. Chem. 269: 19713–19718 [PubMed] [Google Scholar]
Matsui Y., Toh-e A., 1992. Yeast RHO3 and RHO4 ras superfamily genes are necessary for bud growth, and their defect is suppressed by a high dose of bud formation genes CDC42 and BEM1. Mol. Cell. Biol. 12: 5690–5699 [DOI] [PMC free article] [PubMed] [Google Scholar]
Mazur P., Baginsky W., 1996. In vitro activity of 1,3-beta-D-glucan synthase requires the GTP-binding protein Rho1. J. Biol. Chem. 271: 14604–14609 [DOI] [PubMed] [Google Scholar]
Mazur P., Morin N., Baginsky W., el-Sherbeini M., Clemas J. A., et al. , 1995. Differential expression and function of two homologous subunits of yeast 1,3-beta-D-glucan synthase. Mol. Cell. Biol. 15: 5671–5681 [DOI] [PMC free article] [PubMed] [Google Scholar]
Mazzoni C., Zarzov P., Rambourg A., Mann C., 1993. The SLT2(MPK1) map kinase homolog is involved in polarized cell growth in Saccharomyces cerevisiae. J. Cell Biol. 123: 1821–1833 [DOI] [PMC free article] [PubMed] [Google Scholar]
McCaffrey M., Johnson J. S., Goud B., Myers A. M., Rossier J., et al. , 1991. The small GTP-binding protein Rho1p is localized on the Golgi apparatus and post-Golgi vesicles in Saccharomyces cerevisiae. J. Cell Biol. 115: 309–319 [DOI] [PMC free article] [PubMed] [Google Scholar]
McMurray M. A., Thorner J., 2009. Septins: molecular partitioning and the generation of cellular asymmetry. Cell Div. 4: 18. [DOI] [PMC free article] [PubMed] [Google Scholar]
McMurray M. A., Bertin A., Garcia G., 3rd, Lam L., Nogales E., et al. , 2011. Septin filament formation is essential in budding yeast. Dev. Cell 20: 540–549 [DOI] [PMC free article] [PubMed] [Google Scholar]
Meitinger F., Petrova B., Mancini Lombardi I., Bertazzi D. T., Hub B., et al. , 2010. Targeted localization of Inn1, Cyk3 and Chs2 by the mitotic-exit network regulates cytokinesis in budding yeast. J. Cell Sci. 123: 1851–1861 [DOI] [PubMed] [Google Scholar]
Meitinger F., Boehm M. E., Hofmann A., Hub B., Zentgraf H., et al. , 2011. Phosphorylation-dependent regulation of the F-BAR protein Hof1 during cytokinesis. Genes Dev. 25: 875–888 [DOI] [PMC free article] [PubMed] [Google Scholar]
Michelitch M., Chant J., 1996. A mechanism of Bud1p GTPase action suggested by mutational analysis and immunolocalization. Curr. Biol. 6: 446–454 [DOI] [PubMed] [Google Scholar]
Miller P. J., Johnson D. I., 1994. Cdc42p GTPase is involved in controlling polarized cell growth in Schizosaccharomyces pombe. Mol. Cell. Biol. 14: 1075–1083 [DOI] [PMC free article] [PubMed] [Google Scholar]
Miller R., Matheos D., Rose M. D., 1999. The cortical localization of the microtubule orientation protein, Kar9p, is dependent upon actin and proteins required for polarization. J. Cell Biol. 144: 963–975 [DOI] [PMC free article] [PubMed] [Google Scholar]
Mino A., Tanaka K., Kamei T., Umikawa M., Fujiwara T., et al. , 1998. Shs1p: a novel member of septin that interacts with Spa2p, involved in polarized growth in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 251: 732–736 [DOI] [PubMed] [Google Scholar]
Moore J. K., Stuchell-Brereton M. D., Cooper J. A., 2009. Function of dynein in budding yeast: mitotic spindle positioning in a polarized cell. Cell Motil. Cytoskeleton 66: 546–555 [DOI] [PMC free article] [PubMed] [Google Scholar]
Moore J. K., Chudalayandi P., Heil-Chapdelaine R. A., Cooper J. A., 2010. The spindle position checkpoint is coordinated by the Elm1 kinase. J. Cell Biol. 191: 493–503 [DOI] [PMC free article] [PubMed] [Google Scholar]
Mortensen E. M., McDonald H., Yates J., 3rd, Kellogg D. R., 2002. Cell cycle-dependent assembly of a Gin4-septin complex. Mol. Biol. Cell 13: 2091–2105 [DOI] [PMC free article] [PubMed] [Google Scholar]
Mosammaparast N., Ewart C. S., Pemberton L. F., 2002. A role for nucleosome assembly protein 1 in the nuclear transport of histones H2A and H2B. EMBO J. 21: 6527–6538 [DOI] [PMC free article] [PubMed] [Google Scholar]
Moseley J. B., Goode B. L., 2005. Differential activities and regulation of Saccharomyces cerevisiae formin proteins Bni1 and Bnr1 by Bud6. J. Biol. Chem. 280: 28023–28033 [DOI] [PubMed] [Google Scholar]
Moseley J. B., Goode B. L., 2006. The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol. Mol. Biol. Rev. 70: 605–645 [DOI] [PMC free article] [PubMed] [Google Scholar]
Moseley J. B., Sagot I., Manning A. L., Xu Y., Eck M. J., et al. , 2004. A conserved mechanism for Bni1- and mDia1-induced actin assembly and dual regulation of Bni1 by Bud6 and profilin. Mol. Biol. Cell 15: 896–907 [DOI] [PMC free article] [PubMed] [Google Scholar]
Mukherjee D., Coon B. G., Edwards D. F., 3rd, Hanna C. B., Longhi S. A., et al. , 2009. The yeast endocytic protein Epsin 2 functions in a cell-division signaling pathway. J. Cell Sci. 122: 2453–2463 [DOI] [PMC free article] [PubMed] [Google Scholar]
Muller L., Xu G., Wells R., Hollenberg C. P., Piepersberg W., 1994. LRG1 is expressed during sporulation in Saccharomyces cerevisiae and contains motifs similar to LIM and rho/racGAP domains. Nucleic Acids Res. 22: 3151–3154 [DOI] [PMC free article] [PubMed] [Google Scholar]
Munemitsu S., Innis M. A., Clark R., McCormick F., Ullrich A., et al. , 1990. Molecular cloning and expression of a G25K cDNA, the human homolog of the yeast cell cycle gene CDC42. Mol. Cell. Biol. 10: 5977–5982 [DOI] [PMC free article] [PubMed] [Google Scholar]
Munn A. L., Stevenson B. J., Geli M. I., Riezman H., 1995. end5, end6, and end7: mutations that cause actin delocalization and block the internalization step of endocytosis in Saccharomyces cerevisiae. Mol. Biol. Cell 6: 1721–1742 [DOI] [PMC free article] [PubMed] [Google Scholar]
Nasmyth K., Dirick L., 1991. The role of SWI4 and SWI6 in the activity of G1 cyclins in yeast. Cell 66: 995–1013 [DOI] [PubMed] [Google Scholar]
Nelson B., Kurischko C., Horecka J., Mody M., Nair P., et al. , 2003. RAM: a conserved signaling network that regulates Ace2p transcriptional activity and polarized morphogenesis. Mol. Biol. Cell 14: 3782–3803 [DOI] [PMC free article] [PubMed] [Google Scholar]
Nern A., Arkowitz R. A., 1999. A Cdc24-Far1p-G beta gamma protein complex required for yeast orientation during mating. J. Cell Biol. 144: 1187–1202 [DOI] [PMC free article] [PubMed] [Google Scholar]
Nern A., Arkowitz R. A., 2000. Nucleocytoplasmic shuttling of the Cdc42p exchange factor Cdc24p. J. Cell Biol. 148: 1115–1122 [DOI] [PMC free article] [PubMed] [Google Scholar]
Ni L., Snyder M., 2001. A genomic study of the bipolar bud site selection pattern in Saccharomyces cerevisiae. Mol. Biol. Cell 12: 2147–2170 [DOI] [PMC free article] [PubMed] [Google Scholar]
Nishihama R., Schreiter J. H., Onishi M., Vallen E. A., Hanna J., et al. , 2009. Role of Inn1 and its interactions with Hof1 and Cyk3 in promoting cleavage furrow and septum formation in S. cerevisiae. J. Cell Biol. 185: 995–1012 [DOI] [PMC free article] [PubMed] [Google Scholar]
Noma A., Yi S., Katoh T., Takai Y., Suzuki T., 2011. Actin-binding protein Abp140 is a methyltransferase for 3-methylcytidine at position 32 of tRNAs in Saccharomyces cerevisiae. RNA 17: 1111–1119 [DOI] [PMC free article] [PubMed] [Google Scholar]
Nomanbhoy T. K., Cerione R., 1996. Characterization of the interaction between RhoGDI and Cdc42Hs using fluorescence spectroscopy. J. Biol. Chem. 271: 10004–10009 [DOI] [PubMed] [Google Scholar]
Novick P., Botstein D., 1985. Phenotypic analysis of temperature-sensitive yeast actin mutants. Cell 40: 405–416 [DOI] [PubMed] [Google Scholar]
Oh Y., Bi E., 2011. Septin structure and function in yeast and beyond. Trends Cell Biol. 21: 141–148 [DOI] [PMC free article] [PubMed] [Google Scholar]
Okuzaki D., Tanaka S., Kanazawa H., Nojima H., 1997. Gin4 of S. cerevisiae is a bud neck protein that interacts with the Cdc28 complex. Genes Cells 2: 753–770 [DOI] [PubMed] [Google Scholar]
Orlando K., Zhang J., Zhang X., Yue P., Chiang T., et al. , 2008. Regulation of Gic2 localization and function by phosphatidylinositol 4,5-bisphosphate during the establishment of cell polarity in budding yeast. J. Biol. Chem. 283: 14205–14212 [DOI] [PMC free article] [PubMed] [Google Scholar]
Orlando K., Sun X., Zhang J., Lu T., Yokomizo L., et al. , 2011. Exo-endocytic trafficking and the septin-based diffusion barrier are required for the maintenance of Cdc42p polarization during budding yeast asymmetrical growth. Mol. Biol. Cell 22: 624–633 [DOI] [PMC free article] [PubMed] [Google Scholar]
Ortiz D., Medkova M., Wach-Solimena C., Novick P., 2002. Ypt32 recruits the Sec4p guanine nucleotide exchange factor, Sec2p, to secretory vesicles; evidence for a Rab cascade in yeast. J. Cell Biol. 157: 1005–1015 [DOI] [PMC free article] [PubMed] [Google Scholar]
Ozaki K., Tanaka K., Imamura H., Hihara T., Kameyama T., et al. , 1996. Rom1p and Rom2p are GDP/GTP exchange proteins (GEPs) for the Rho1p small GTP binding proteins in Saccharomyces cerevisiae. EMBO J. 15: 2196–2207 [PMC free article] [PubMed] [Google Scholar]
Ozaki-Kuroda K., Yamamoto Y., Nohara H., Kinoshita M., Fujiwara T., et al. , 2001. Dynamic localization and function of Bni1p at the sites of directed growth in Saccharomyces cerevisiae. Mol. Cell. Biol. 21: 827–839 [DOI] [PMC free article] [PubMed] [Google Scholar]
Ozbudak E. M., Becskei A., van Oudenaarden A., 2005. A system of counteracting feedback loops regulates Cdc42p activity during spontaneous cell polarization. Dev. Cell 9: 565–571 [DOI] [PubMed] [Google Scholar]
Paciorek T., Bergmann D. C., 2010. The secret to life is being different: asymmetric divisions in plant development. Curr. Opin. Plant Biol. 13: 661–669 [DOI] [PubMed] [Google Scholar]
Padmanabhan A., Bakka K., Sevugan M., Naqvi N. I., D’Souza V., et al. , 2011. IQGAP-related Rng2p organizes cortical nodes and ensures position of cell division in fission yeast. Curr. Biol. 21: 467–472 [DOI] [PubMed] [Google Scholar]
Palmer R. E., Sullivan D. S., Huffaker T., Koshland D., 1992. Role of astral microtubules and actin in spindle orientation and migration in the budding yeast, Saccharomyces cerevisiae. J. Cell Biol. 119: 583–593 [DOI] [PMC free article] [PubMed] [Google Scholar]
Parent S. A., Nielsen J. B., Morin N., Chrebet G., Ramadan N., et al. , 1993. Calcineurin-dependent growth of an FK506- and CsA-hypersensitive mutant of Saccharomyces cerevisiae. J. Gen. Microbiol. 139: 2973–2984 [DOI] [PubMed] [Google Scholar]
Park H. O., Bi E., 2007. Central roles of small GTPases in the development of cell polarity in yeast and beyond. Microbiol. Mol. Biol. Rev. 71: 48–96 [DOI] [PMC free article] [PubMed] [Google Scholar]
Park H. O., Chant J., 1996. Bud2 protein, pp. 200–203 The Guidebook to the Small GTPases, edited by Zerial M., Huber L. Oxford Press, Oxford [Google Scholar]
Park H. O., Bi E., Pringle J. R., Herskowitz I., 1997. Two active states of the Ras-related Bud1/Rsr1 protein bind to different effectors to determine yeast cell polarity. Proc. Natl. Acad. Sci. USA 94: 4463–4468 [DOI] [PMC free article] [PubMed] [Google Scholar]
Park H.-O., Chant J., Herskowitz I., 1993. BUD2 encodes a GTPase-activating protein for Bud1/Rsr1 necessary for proper bud-site selection in yeast. Nature 365: 269–274 [DOI] [PubMed] [Google Scholar]
Park H.-O., Sanson A., Herskowitz I., 1999. Localization of Bud2p, a GTPase-activating protein necessary for programming cell polarity in yeast to the presumptive bud site. Genes Dev. 13: 1912–1917 [DOI] [PMC free article] [PubMed] [Google Scholar]
Park H.-O., Kang P. J., Rachfal A. W., 2002. Localization of the Rsr1/Bud1 GTPase involved in selection of a proper growth site in yeast. J. Biol. Chem. 277: 26721–26724 [DOI] [PubMed] [Google Scholar]
Perez P., Rincon S. A., 2010. Rho GTPases: regulation of cell polarity and growth in yeasts. Biochem. J. 426: 243–253 [DOI] [PubMed] [Google Scholar]
Peter M., Neiman A. M., Park H. O., van Lohuizen M., Herskowitz I., 1996. Functional analysis of the interaction between the small GTP binding protein Cdc42 and the Ste20 protein kinase in yeast. EMBO J. 15: 7046–7059 [PMC free article] [PubMed] [Google Scholar]
Peterson J., Zheng Y., Bender L., Myers A., Cerione R., et al. , 1994. Interactions between the bud emergence proteins Bem1p and Bem2p and rho-type GTPases in yeast. J. Cell Biol. 127: 1395–1406 [DOI] [PMC free article] [PubMed] [Google Scholar]
Philip B., Levin D. E., 2001. Wsc1 and Mid2 are cell surface sensors for cell wall integrity signaling that act through Rom2, a guanine nucleotide exchange factor for Rho1. Mol. Cell. Biol. 21: 271–280 [DOI] [PMC free article] [PubMed] [Google Scholar]
Pollard T. D., 2008. Progress towards understanding the mechanism of cytokinesis in fission yeast. Biochem. Soc. Trans. 36: 425–430 [DOI] [PMC free article] [PubMed] [Google Scholar]
Pollard T. D., 2010. Mechanics of cytokinesis in eukaryotes. Curr. Opin. Cell Biol. 22: 50–56 [DOI] [PMC free article] [PubMed] [Google Scholar]
Pollard T. D., Borisy G. G., 2003. Cellular motility driven by assembly and disassembly of actin filaments. Cell 113: 549. [DOI] [PubMed] [Google Scholar]
Powers J., Barlowe C., 2002. Erv14p directs a transmembrane secretory protein into COPII-coated transport vesicles. Mol. Biol. Cell 142: 1209–1222 [DOI] [PMC free article] [PubMed] [Google Scholar]
Powers S., Gonzales E., Christensen T., Cubert J., Broek D., 1991. Functional cloning of BUD5, a CDC25-related gene from S. cerevisiae that can suppress a dominant-negative RAS2 mutant. Cell 65: 1225–1231 [DOI] [PubMed] [Google Scholar]
Pring M., Evangelista M., Boone C., Yang C., Zigmond S. H., 2003. Mechanism of formin-induced nucleation of actin filaments. Biochemistry 42: 486–496 [DOI] [PubMed] [Google Scholar]
Pringle J. R., Hartwell L. H., 1981. The Saccharomyces cerevisiae cell cycle, pp. 97–142 The molecular biology of the yeast Saccharomyces. Life cycle and inheritance, edited by Strathern J. N., Jones E. W., Broach J. R. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y [Google Scholar]
Pringle J. R., Bi E., Harkins H. A., Zahner J. E., De Virgilio C., et al. , 1995. Establishment of cell polarity in yeast. Cold Spring Harb. Symp. Quant. Biol. 60: 729–744 [DOI] [PubMed] [Google Scholar]
Pruyne D., Bretscher A., 2000a. Polarization of cell growth in yeast. II. The role of the cortical actin cytoskeleton. J. Cell Sci. 113: 571–585 [DOI] [PubMed] [Google Scholar]
Pruyne D., Bretscher A., 2000b. Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J. Cell Sci. 113: 365–375 [DOI] [PubMed] [Google Scholar]
Pruyne D. W., Schott D. H., Bretscher A., 1998. Tropomyosin-containing actin cables direct the Myo2p-dependent polarized delivery of secretory vesicles in budding yeast. J. Cell Biol. 143: 1931–1945 [DOI] [PubMed] [Google Scholar]
Pruyne D., Evangelista M., Yang C., Bi E., Zigmond S., et al. , 2002. Role of formins in actin assembly: nucleation and barbed end association. Science 297: 612–615 [DOI] [PubMed] [Google Scholar]
Pruyne D., Gao L., Bi E., Bretscher A., 2004. Stable and dynamic axes of polarity use distinct formin isoforms in budding yeast. Mol. Biol. Cell 15: 4971–4989 [DOI] [PMC free article] [PubMed] [Google Scholar]
Qadota H., Python C. P., Inoue S. B., Arisawa M., Anraku Y., et al. , 1996. Identification of yeast Rho1p GTPase as a regulatory subunit of 1,3-β-glucan synthase. Science 272: 279–281 [DOI] [PubMed] [Google Scholar]
Ramer S. W., Davis R. W., 1993. A dominant truncation allele identifies a gene, STE20, that encodes a putative protein kinase necessary for mating in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 90: 452–456 [DOI] [PMC free article] [PubMed] [Google Scholar]
Richman T. J., Sawyer M. M., Johnson D. I., 2002. Saccharomyces cerevisiae Cdc42p localizes to cellular membranes and clusters at sites of polarized growth. Eukaryot. Cell 1: 458–468 [DOI] [PMC free article] [PubMed] [Google Scholar]
Richman T. J., Toenjes K. A., Morales S. E., Cole K. C., Wasserman B. T., et al. , 2004. Analysis of cell-cycle specific localization of the Rdi1p RhoGDI and the structural determinants required for Cdc42p membrane localization and clustering at sites of polarized growth. Curr. Genet. 45: 339–349 [DOI] [PubMed] [Google Scholar]
Riedl J., Crevenna A. H., Kessenbrock K., Yu J. H., Neukirchen D., et al. , 2008. Lifeact: a versatile marker to visualize F-actin. Nat. Methods 5: 605–607 [DOI] [PMC free article] [PubMed] [Google Scholar]
Rivera-Molina F. E., Novick P. J., 2009. A Rab GAP cascade defines the boundary between two Rab GTPases on the secretory pathway. Proc. Natl. Acad. Sci. USA 106: 14408–14413 [DOI] [PMC free article] [PubMed] [Google Scholar]
Robinson N. G., Guo L., Imai J., Toh E. A., Matsui Y., et al. , 1999. Rho3 of Saccharomyces cerevisiae, which regulates the actin cytoskeleton and exocytosis, is a GTPase which interacts with Myo2 and Exo70. Mol. Cell. Biol. 19: 3580–3587 [DOI] [PMC free article] [PubMed] [Google Scholar]
Rodal A. A., Kozubowski L., Goode B. L., Drubin D. G., Hartwig J. H., 2005. Actin and septin ultrastructures at the budding yeast cell cortex. Mol. Biol. Cell 16: 372–384 [DOI] [PMC free article] [PubMed] [Google Scholar]
Rodriguez J. R., Paterson B. M., 1990. Yeast myosin heavy chain mutant: maintenance of the cell type specific budding pattern and the normal deposition of chitin and cell wall components requires an intact myosin heavy chain gene. Cell Motil. Cytoskeleton 17: 301–308 [DOI] [PubMed] [Google Scholar]
Rodriguez-Escudero I., Roelants F. M., Thorner J., Nombela C., Molina M., et al. , 2005. Reconstitution of the mammalian PI3K/PTEN/Akt pathway in yeast. Biochem. J. 390: 613–623 [DOI] [PMC free article] [PubMed] [Google Scholar]
Roemer T., Madden K., Chang J., Snyder M., 1996. Selection of axial growth sites in yeast requires Axl2p, a novel plasma membrane glycoprotein. Genes Dev. 10: 777–793 [DOI] [PubMed] [Google Scholar]
Rothman J. E., 1996. The protein machinery of vesicle budding and fusion. Protein Sci. 5: 185–194 [DOI] [PMC free article] [PubMed] [Google Scholar]
Roumanie O., Weinachter C., Larrieu I., Crouzet M., Doignon F., 2001. Functional characterization of the Bag7, Lrg1 and Rgd2 RhoGAP proteins from Saccharomyces cerevisiae. FEBS Lett. 506: 149–156 [DOI] [PubMed] [Google Scholar]
Ruggieri R., Bender A., Matsui Y., Powers S., Takai Y., et al. , 1992. RSR1, a ras-like gene homologous to Krev-1 (smg21A/rap1A): role in the development of cell polarity and interactions with the Ras pathway in Saccharomyces cerevisiae. Mol. Cell. Biol. 12: 758–766 [DOI] [PMC free article] [PubMed] [Google Scholar]
Sagot I., Klee S. K., Pellman D., 2002a. Yeast formins regulate cell polarity by controlling the assembly of actin cables. Nat. Cell Biol. 4: 42–50 [DOI] [PubMed] [Google Scholar]
Sagot I., Rodal A. A., Moseley J., Goode B. L., Pellman D., 2002b. An actin nucleation mechanism mediated by Bni1 and profilin. Nat. Cell Biol. 4: 626–631 [DOI] [PubMed] [Google Scholar]
Sahin A., Daignan-Fornier B., Sagot I., 2008. Polarized growth in the absence of F-actin in Saccharomyces cerevisiae exiting quiescence. PLoS ONE 3: e2556. [DOI] [PMC free article] [PubMed] [Google Scholar]
Saito H., 2010. Regulation of cross-talk in yeast MAPK signaling pathways. Curr. Opin. Microbiol. 13: 677–683 [DOI] [PubMed] [Google Scholar]
Salminen A., Novick P. J., 1987. A Ras-like protein is required for a post-Golgi event in yeast secretion. Cell 49: 527–538 [DOI] [PubMed] [Google Scholar]
Sanchez-Diaz A., Marchesi V., Murray S., Jones R., Pereira G., et al. , 2008. Inn1 couples contraction of the actomyosin ring to membrane ingression during cytokinesis in budding yeast. Nat. Cell Biol. 10: 395–406 [DOI] [PubMed] [Google Scholar]
Sanders S. L., Field C. M., 1994. Cell division. Septins in common? Curr. Biol. 4: 907–910 [DOI] [PubMed] [Google Scholar]
Sanders S. L., Herskowitz I., 1996. The Bud4 protein of yeast, required for axial budding, is localized to the mother/bud neck in a cell cycle-dependent manner. J. Cell Biol. 134: 413–427 [DOI] [PMC free article] [PubMed] [Google Scholar]
Sanders S. L., Gentzsch M., Tanner W., Herskowitz I., 1999. O-glycosylation of Axl2/Bud10p by Pmt4p is required for its stability, localization, and function in daughter cells. J. Cell Biol. 145: 1177–1188 [DOI] [PMC free article] [PubMed] [Google Scholar]
Sburlati A., Cabib E., 1986. Chitin synthetase 2, a presumptive participant in septum formation in Saccharomyces cerevisiae. J. Biol. Chem. 261: 15147–15152 [PubMed] [Google Scholar]
Schenkman L. R., Caruso C., Pagé N., Pringle J. R., 2002. The role of cell cycle-regulated expression in the localization of spatial landmark proteins in yeast. J. Cell Biol. 156: 829–841 [DOI] [PMC free article] [PubMed] [Google Scholar]
Schmelzle T., Helliwell S. B., Hall M. N., 2002. Yeast protein kinases and the Rho1 exchange factor Tus1 are novel components of the cell integrity pathway in yeast. Mol. Cell. Biol. 22: 1329–1339 [DOI] [PMC free article] [PubMed] [Google Scholar]
Schmidt A., Bickle M., Beck T., Hall M. N., 1997. The yeast phosphatidylinositol kinase homolog TOR2 activates RHO1 and RHO2 via the exchange factor ROM2. Cell 88: 531–542 [DOI] [PubMed] [Google Scholar]
Schmidt A., Schmelzle T., Hall M. N., 2002. The RHO1-GAPs SAC7, BEM2 and BAG7 control distinct RHO1 functions in Saccharomyces cerevisiae. Mol. Microbiol. 45: 1433–1441 [DOI] [PubMed] [Google Scholar]
Schmidt M., Bowers B., Varma A., Roh D.-H., Cabib E., 2002. In budding yeast, contraction of the actomyosin ring and formation of the primary septum at cytokinesis depend on each other. J. Cell Sci. 115: 293–302 [DOI] [PubMed] [Google Scholar]
Schmitz H. P., Huppert S., Lorberg A., Heinisch J. J., 2002. Rho5p downregulates the yeast cell integrity pathway. J. Cell Sci. 115: 3139–3148 [DOI] [PubMed] [Google Scholar]
Schott D. H., Collins R. N., Bretscher A., 2002. Secretory vesicle transport velocity in living cells depends on the myosin-V lever arm length. J. Cell Biol. 156: 35–39 [DOI] [PMC free article] [PubMed] [Google Scholar]
Schroeder T. E., 1968. Cytokinesis: filaments in the cleavage furrow. Exp. Cell Res. 53: 272–276 [DOI] [PubMed] [Google Scholar]
Schroeder T. E., 1972. The contractile ring II: determining its brief existence, volumetric changes, and vital role in cleaving arbacia eggs. J. Cell Biol. 53: 419–434 [DOI] [PMC free article] [PubMed] [Google Scholar]
Sekiguchi T., Hirose E., Nakashima N., Ii M., Nishimoto T., 2001. Novel G proteins, Rag C and Rag D, interact with GTP-binding proteins, Rag A and Rag B. J. Biol. Chem. 276: 7246–7257 [DOI] [PubMed] [Google Scholar]
Shan S.-o., Stroud R. M., Walter P., 2004. Mechanism of association and reciprocal activation of two GTPases. PLoS Biol. 2: e320. [DOI] [PMC free article] [PubMed] [Google Scholar]
Shannon K. B., Li R., 1999. The multiple roles of Cyk1p in the assembly and function of the actomyosin ring in budding yeast. Mol. Biol. Cell 10: 283–296 [DOI] [PMC free article] [PubMed] [Google Scholar]
Shannon K. B., Li R., 2000. A myosin light chain mediates the localization of the budding yeast IQGAP-like protein during contractile ring formation. Curr. Biol. 10: 727–730 [DOI] [PubMed] [Google Scholar]
Shaw J. A., Mol P. C., Bowers B., Silverman S. J., Valdivieso M. H., et al. , 1991. The function of chitin synthases 2 and 3 in the Saccharomyces cerevisiae cell cycle. J. Cell Biol. 114: 111–123 [DOI] [PMC free article] [PubMed] [Google Scholar]
Sheu Y. J., Barral Y., Snyder M., 2000. Polarized growth controls cell shape and bipolar bud site selection in Saccharomyces cerevisiae. Mol. Cell. Biol. 20: 5235–5247 [DOI] [PMC free article] [PubMed] [Google Scholar]
Sheu Y. J., Santos B., Fortin N., Costigan C., Snyder M., 1998. Spa2p interacts with cell polarity proteins and signaling components involved in yeast cell morphogenesis. Mol. Cell. Biol. 18: 4053–4069 [DOI] [PMC free article] [PubMed] [Google Scholar]
Shimada Y., Gulli M. P., Peter M., 2000. Nuclear sequestration of the exchange factor Cdc24 by Far1 regulates cell polarity during yeast mating. Nat. Cell Biol. 2: 117–124 [DOI] [PubMed] [Google Scholar]
Shimada Y., Wiget P., Gulli M. P., Bi E., Peter M., 2004. The nucleotide exchange factor Cdc24p may be regulated by auto-inhibition. EMBO J. 23: 1051–1062 [DOI] [PMC free article] [PubMed] [Google Scholar]
Shinjo K., Koland J. G., Hart M. J., Narasimhan V., Johnson D. I., et al. , 1990. Molecular cloning of the gene for the human placental GTP-binding protein Gp (G25K): identification of this GTP-binding protein as the human homolog of the yeast cell-division-cycle protein CDC42. Proc. Natl. Acad. Sci. USA 87: 9853–9857 [DOI] [PMC free article] [PubMed] [Google Scholar]
Sidorova J., Breeden L., 1993. Analysis of the SWI4/SWI6 protein complex, which directs G1/S-specific transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 13: 1069–1077 [DOI] [PMC free article] [PubMed] [Google Scholar]
Singer J. M., Shaw J. M., 2003. Mdm20 protein functions with Nat3 protein to acetylate Tpm1 protein and regulate tropomyosin-actin interactions in budding yeast. Proc. Natl. Acad. Sci. USA 100: 7644–7649 [DOI] [PMC free article] [PubMed] [Google Scholar]
Singh K., Kang P. J., Park H. O., 2008. The Rho5 GTPase is necessary for oxidant-induced cell death in budding yeast. Proc. Natl. Acad. Sci. USA 105: 1522–1527 [DOI] [PMC free article] [PubMed] [Google Scholar]
Sivadon P., Bauer F., Aigle M., Crouzet M., 1995. Actin cytoskeleton and budding pattern are altered in the yeast rvs161 mutant: the Rvs161 protein shares common domains with the brain protein amphiphysin. Mol. Gen. Genet. 246: 485–495 [DOI] [PubMed] [Google Scholar]
Slaughter B. D., Das A., Schwartz J. W., Rubinstein B., Li R., 2009. Dual modes of cdc42 recycling fine-tune polarized morphogenesis. Dev. Cell 17: 823–835 [DOI] [PMC free article] [PubMed] [Google Scholar]
Sloat B. F., Pringle J. R., 1978. A mutant of yeast defective in cellular morphogenesis. Science 200: 1171–1173 [DOI] [PubMed] [Google Scholar]
Sloat B. F., Adams A., Pringle J. R., 1981. Roles of the CDC24 gene product in cellular morphogenesis during the Saccharomyces cerevisiae cell cycle. J. Cell Biol. 89: 395–405 [DOI] [PMC free article] [PubMed] [Google Scholar]
Smith G. R., Givan S. A., Cullen P., Sprague G. F., Jr, 2002. GTPase-activating proteins for Cdc42. Eukaryot. Cell 1: 469–480 [DOI] [PMC free article] [PubMed] [Google Scholar]
Smith M. G., Swamy S. R., Pon L. A., 2001. The life cycle of actin patches in mating yeast. J. Cell Sci. 114: 1505–1513 [DOI] [PubMed] [Google Scholar]
Snyder M., 1989. The SPA2 protein of yeast localizes to sites of cell growth. J. Cell Biol. 108: 1419–1429 [DOI] [PMC free article] [PubMed] [Google Scholar]
Sopko R., Huang D., Smith J. C., Figeys D., Andrews B. J., 2007. Activation of the Cdc42p GTPase by cyclin-dependent protein kinases in budding yeast. EMBO J. 26: 4487–4500 [DOI] [PMC free article] [PubMed] [Google Scholar]
Stevens R. C., Davis T. N., 1998. Mlc1p is a light chain for the unconventional myosin Myo2p in Saccharomyces cerevisiae. J. Cell Biol. 142: 711–722 [DOI] [PMC free article] [PubMed] [Google Scholar]
Stevenson B. J., Ferguson B., De Virgilio C., Bi E., Pringle J. R., et al. , 1995. Mutation of RGA1, which encodes a putative GTPase-activating protein for the polarity-establishment protein Cdc42p, activates the pheromone-response pathway in the yeast Saccharomyces cerevisiae. Genes Dev. 9: 2949–2963 [DOI] [PubMed] [Google Scholar]
Sullivan D. S., Huffaker T. C., 1992. Astral microtubules are not required for anaphase B in Saccharomyces cerevisiae. J. Cell Biol. 119: 379–388 [DOI] [PMC free article] [PubMed] [Google Scholar]
Szkotnicki L., Crutchley J. M., Zyla T. R., Bardes E. S., Lew D. J., 2008. The checkpoint kinase Hsl1p is activated by Elm1p-dependent phosphorylation. Mol. Biol. Cell 19: 4675–4686 [DOI] [PMC free article] [PubMed] [Google Scholar]
Taheri N., Köhler T., Braus G. H., Mösch H.-U., 2000. Asymmetrically localized Bud8p and Bud9p proteins control yeast cell polarity and development. EMBO J. 19: 6686–6696 [DOI] [PMC free article] [PubMed] [Google Scholar]
Takahashi S., Pryciak P. M., 2007. Identification of novel membrane-binding domains in multiple yeast Cdc42 effectors. Mol. Biol. Cell 18: 4945–4956 [DOI] [PMC free article] [PubMed] [Google Scholar]
Tanaka-Takiguchi Y., Kinoshita M., Takiguchi K., 2009. Septin-mediated uniform bracing of phospholipid membranes. Curr. Biol. 19: 140–145 [DOI] [PubMed] [Google Scholar]
Tcheperegine S. E., Gao X. D., Bi E., 2005. Regulation of cell polarity by interactions of Msb3 and Msb4 with Cdc42 and polarisome components. Mol. Cell. Biol. 25: 8567–8580 [DOI] [PMC free article] [PubMed] [Google Scholar]
Teh E. M., Chai C. C., Yeong F. M., 2009. Retention of Chs2p in the ER requires N-terminal CDK1-phosphorylation sites. Cell Cycle 8: 2964–2974 [PubMed] [Google Scholar]
Tennyson C. N., Lee J., Andrews B., 1998. A role for the Pcl9-Pho85 cyclin-cdk complex at the M/G1 boundary in Saccharomyces cerevisiae. Mol. Microbiol. 28: 69–79 [DOI] [PubMed] [Google Scholar]
TerBush D. R., Maurice T., Roth D., Novick P., 1996. The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J. 15: 6483–6494 [PMC free article] [PubMed] [Google Scholar]
Thanabalu T., Munn A. L., 2001. Functions of Vrp1p in cytokinesis and actin patches are distinct and neither requires a WH2/V domain. EMBO J. 20: 6979–6989 [DOI] [PMC free article] [PubMed] [Google Scholar]
Tiedje C., Sakwa I., Just U., Hofken T., 2008. The Rho GDI Rdi1 regulates Rho GTPases by distinct mechanisms. Mol. Biol. Cell 19: 2885–2896 [DOI] [PMC free article] [PubMed] [Google Scholar]
Toenjes K. A., Sawyer M. M., Johnson D. I., 1999. The guanine-nucleotide-exchange factor Cdc24p is targeted to the nucleus and polarized growth sites. Curr. Biol. 9: 1183–1186 [DOI] [PubMed] [Google Scholar]
Toenjes K. A., Simpson D., Johnson D. I., 2004. 2004 Separate membrane targeting and anchoring domains function in the localization of the S. cerevisiae Cdc24p guanine nucleotide exchange factor. Curr. Genet. 45: 257–264 [DOI] [PubMed] [Google Scholar]
Tolliday N., VerPlank L., Li R., 2002. Rho1 directs formin-mediated actin ring assembly during budding yeast cytokinesis. Curr. Biol. 12: 1864–1870 [DOI] [PubMed] [Google Scholar]
Tong Z., Gao X. D., Howell A. S., Bose I., Lew D. J., et al. , 2007. Adjacent positioning of cellular structures enabled by a Cdc42 GTPase-activating protein-mediated zone of inhibition. J. Cell Biol. 179: 1375–1384 [DOI] [PMC free article] [PubMed] [Google Scholar]
Torres L., Martin H., Garcia-Saez M. I., Arroyo J., Molina M., et al. , 1991. A protein kinase gene complements the lytic phenotype of Saccharomyces cerevisiae lyt2 mutants. Mol. Microbiol. 5: 2845–2854 [DOI] [PubMed] [Google Scholar]
Tully G. H., Nishihama R., Pringle J. R., Morgan D. O., 2009. The anaphase-promoting complex promotes actomyosin-ring disassembly during cytokinesis in yeast. Mol. Biol. Cell 20: 1201–1212 [DOI] [PMC free article] [PubMed] [Google Scholar]
Uchida Y., Shimmi O., Sudoh M., Arisawa M., Yamada-Okabe H., 1996. Characterization of chitin synthase 2 of Saccharomyces cerevisiae. II: Both full size and processed enzymes are active for chitin synthesis. J. Biochem. 119: 659–666 [DOI] [PubMed] [Google Scholar]
Vaduva G., Martin N. C., Hopper A. K., 1997. Actin-binding verprolin is a polarity development protein required for the morphogenesis and function of the yeast actin cytoskeleton. J. Cell Biol. 139: 1821–1833 [DOI] [PMC free article] [PubMed] [Google Scholar]
Valdivia R. H., Schekman R., 2003. The yeasts Rho1p and Pkc1p regulate the transport of chitin synthase III (Chs3p) from internal stores to the plasma membrane. Proc. Natl. Acad. Sci. USA 100: 10287–10292 [DOI] [PMC free article] [PubMed] [Google Scholar]
Valdivia R. H., Baggott D., Chuang J. S., Schekman R. W., 2002. The yeast clathrin adaptor protein complex 1 is required for the efficient retention of a subset of late Golgi membrane proteins. Dev. Cell 2: 283–294 [DOI] [PubMed] [Google Scholar]
Vallen E. A., Caviston J., Bi E., 2000. Roles of Hof1p, Bni1p, Bnr1p, and Myo1p in cytokinesis in Saccharomyces cerevisiae. Mol. Biol. Cell 11: 593–611 [DOI] [PMC free article] [PubMed] [Google Scholar]
Valtz N., Herskowitz I., 1996. Pea2 protein of yeast is localized to sites of polarized growth and is required for efficient mating and bipolar budding. J. Cell Biol. 135: 725–739 [DOI] [PMC free article] [PubMed] [Google Scholar]
van Drogen F., Peter M., 2002. Spa2p functions as a scaffold-like protein to recruit the Mpk1p MAP kinase module to sites of polarized growth. Curr. Biol. 12: 1698–1703 [DOI] [PubMed] [Google Scholar]
VerPlank L., Li R., 2005. Cell cycle-regulated trafficking of Chs2 controls actomyosin ring stability during cytokinesis. Mol. Biol. Cell 16: 2529–2543 [DOI] [PMC free article] [PubMed] [Google Scholar]
Versele M., Thorner J., 2004. Septin collar formation in budding yeast requires GTP binding and direct phosphorylation by the PAK, Cla4. J. Cell Biol. 164: 701–715 [DOI] [PMC free article] [PubMed] [Google Scholar]
Vrabioiu A. M., Gerber S. A., Gygi S. P., Field C. M., Mitchison T. J., 2004. The majority of the Saccharomyces cerevisiae septin complexes do not exchange guanine nucleotides. J. Biol. Chem. 279: 3111–3118 [DOI] [PubMed] [Google Scholar]
Waddle J. A., Karpova T. S., Waterston R. H., Cooper J. A., 1996. Movement of cortical actin patches in yeast. J. Cell Biol. 132: 861–870 [DOI] [PMC free article] [PubMed] [Google Scholar]
Wai S. C., Gerber S. A., Li R., 2009. Multisite phosphorylation of the guanine nucleotide exchange factor Cdc24 during yeast cell polarization. PLoS ONE 4: e6563. [DOI] [PMC free article] [PubMed] [Google Scholar]
Walch-Solimena C., Collins R. N., Novick P. J., 1997. Sec2p mediates nucleotide exchange on Sec4p and is involved in polarized delivery of post-Golgi vesicles. J. Cell Biol. 137: 1495–1509 [DOI] [PMC free article] [PubMed] [Google Scholar]
Waltermann C., Klipp E., 2010. Signal integration in budding yeast. Biochem. Soc. Trans. 38: 1257–1264 [DOI] [PubMed] [Google Scholar]
Walworth N. C., Goud B., Kabcenell A. K., Novick P. J., 1989. Mutational analysis of SEC4 suggests a cyclical mechanism for the regulation of vesicular traffic. EMBO J. 8: 1685–1693 [DOI] [PMC free article] [PubMed] [Google Scholar]
Watanabe D., Abe M., Ohya Y., 2001. Yeast Lrg1p acts as a specialized RhoGAP regulating 1,3-beta-glucan synthesis. Yeast 18: 943–951 [DOI] [PubMed] [Google Scholar]
Watanabe Y., Takaesu G., Hagiwara M., Irie K., Matsumoto K., 1997. Characterization of a serum response factor-like protein in Saccharomyces cerevisiae, Rlm1, which has transcriptional activity regulated by the Mpk1 (Slt2) mitogen-activated protein kinase pathway. Mol. Cell. Biol. 17: 2615–2623 [DOI] [PMC free article] [PubMed] [Google Scholar]
Watts F. Z., Shiels G., Orr E., 1987. The yeast MYO1 gene encoding a myosin-like protein required for cell division. EMBO J. 6: 3499–3505 [DOI] [PMC free article] [PubMed] [Google Scholar]
Wedlich-Soldner R., Altschuler S., Wu L., Li R., 2003. Spontaneous cell polarization through actomyosin-based delivery of the Cdc42 GTPase. Science 299: 1231–1235 [DOI] [PubMed] [Google Scholar]
Wedlich-Soldner R., Wai S. C., Schmidt T., Li R., 2004. Robust cell polarity is a dynamic state established by coupling transport and GTPase signaling. J. Cell Biol. 166: 889–900 [DOI] [PMC free article] [PubMed] [Google Scholar]
Weibel P., Hiltbrunner A., Brand L., Kessler F., 2003. Dimerization of Toc-GTPases at the Chloroplast Protein Import Machinery. J. Biol. Chem. 278: 37321–37329 [DOI] [PubMed] [Google Scholar]
Weirich C. S., Erzberger J. P., Barral Y., 2008. The septin family of GTPases: architecture and dynamics. Nat. Rev. Mol. Cell Biol. 9: 478–489 [DOI] [PubMed] [Google Scholar]
Weiss E. L., Bishop A. C., Shokat K. M., Drubin D. G., 2000. Chemical genetic analysis of the budding-yeast p21-activated kinase Cla4p. Nat. Cell Biol. 2: 677–685 [DOI] [PubMed] [Google Scholar]
Wendland B., Steece K. E., Emr S. D., 1999. Yeast epsins contain an essential N-terminal ENTH domain, bind clathrin and are required for endocytosis. EMBO J. 18: 4383–4393 [DOI] [PMC free article] [PubMed] [Google Scholar]
Wiget P., Shimada Y., Butty A. C., Bi E., Peter M., 2004. Site-specific regulation of the GEF Cdc24p by the scaffold protein Far1p during yeast mating. EMBO J. 23: 1063–1074 [DOI] [PMC free article] [PubMed] [Google Scholar]
Wild A. C., Yu J. W., Lemmon M. A., Blumer K. J., 2004. The p21-activated protein kinase-related kinase Cla4 is a coincidence detector of signaling by Cdc42 and phosphatidylinositol 4-phosphate. J. Biol. Chem. 279: 17101–17110 [DOI] [PubMed] [Google Scholar]
Winder S. J., Jess T., Ayscough K. R., 2003. SCP1 encodes an actin-bundling protein in yeast. Biochem. J. 375: 287–295 [DOI] [PMC free article] [PubMed] [Google Scholar]
Winter D., Podtelejnikov A. V., Mann M., Li R., 1997. The complex containing actin-related proteins Arp2 and Arp3 is required for the motility and integrity of yeast actin patches. Curr. Biol. 7: 519–529 [DOI] [PubMed] [Google Scholar]
Winter D., Lechler T., Li R., 1999a. Activation of the yeast Arp2/3 complex by Bee1p, a WASP-family protein. Curr. Biol. 9: 501–504 [DOI] [PubMed] [Google Scholar]
Winter D. C., Choe E. Y., Li R., 1999b. Genetic dissection of the budding yeast Arp2/3 complex: a comparison of the in vivo and structural roles of individual subunits. Proc. Natl. Acad. Sci. USA 96: 7288–7293 [DOI] [PMC free article] [PubMed] [Google Scholar]
Witte H., Bradke F., 2008. The role of the cytoskeleton during neuronal polarization. Curr. Opin. Neurobiol. 18: 479–487 [DOI] [PubMed] [Google Scholar]
Wloka C., Nishihama R., Onishi M., Oh Y., Hanna J., et al. , 2011. Evidence that septin diffusion barriers are dispensable for cytokiensis in budding yeast. Biol. Chem. 392: 813–829 [DOI] [PubMed] [Google Scholar]
Woods A., Johnstone S. R., Dickerson K., Leiper F. C., Fryer L. G., et al. , 2003. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr. Biol. 13: 2004–2008 [DOI] [PubMed] [Google Scholar]
Wu H., Brennwald P., 2010. The function of two Rho family GTPases is determined by distinct patterns of cell surface localization. Mol. Cell. Biol. 30: 5207–5217 [DOI] [PMC free article] [PubMed] [Google Scholar]
Wu H., Turner C., Gardner J., Temple B., Brennwald P., 2010. The Exo70 subunit of the exocyst is an effector for both Cdc42 and Rho3 function in polarized exocytosis. Mol. Biol. Cell 21: 430–442 [DOI] [PMC free article] [PubMed] [Google Scholar]
Yamamoto T., Mochida J., Kadota J., Takeda M., Bi E., et al. , 2010. Initial polarized bud growth by endocytic recycling in the absence of actin cable-dependent vesicle transport in yeast. Mol. Biol. Cell 21: 1237–1252 [DOI] [PMC free article] [PubMed] [Google Scholar]
Yamashita M., Kurokawa K., Sato Y., Yamagata A., Mimura H., et al. , 2010. Structural basis for the Rho- and phosphoinositide-dependent localization of the exocyst subunit Sec3. Nat. Struct. Mol. Biol. 17: 180–186 [DOI] [PubMed] [Google Scholar]
Yamochi W., Tanaka K., Nonaka H., Maeda A., Musha T., et al. , 1994. Growth site localization of Rho1 small GTP-binding protein and its involvement in bud formation in Saccharomyces cerevisiae. J. Cell Biol. 125: 1077–1093 [DOI] [PMC free article] [PubMed] [Google Scholar]
Yang H. C., Pon L. A., 2002. Actin cable dynamics in budding yeast. Proc. Natl. Acad. Sci. USA 99: 751–756 [DOI] [PMC free article] [PubMed] [Google Scholar]
Yang S., Ayscough K. R., Drubin D. G., 1997. A role for the actin cytoskeleton of Saccharomyces cerevisiae in bipolar bud-site selection. J. Cell Biol. 136: 111–123 [DOI] [PMC free article] [PubMed] [Google Scholar]
Yoshida S., Kono K., Lowery D. M., Bartolini S., Yaffe M. B., et al. , 2006. Polo-like kinase Cdc5 controls the local activation of Rho1 to promote cytokinesis. Science 313: 108–111 [DOI] [PubMed] [Google Scholar]
Yoshida S., Bartolini S., Pellman D., 2009. Mechanisms for concentrating Rho1 during cytokinesis. Genes Dev. 23: 810–823 [DOI] [PMC free article] [PubMed] [Google Scholar]
Young M. E., Cooper J. A., Bridgman P. C., 2004. Yeast actin patches are networks of branched actin filaments. J. Cell Biol. 166: 629–635 [DOI] [PMC free article] [PubMed] [Google Scholar]
Zahner J. E., Harkins H. A., Pringle J. R., 1996. Genetic analysis of the bipolar pattern of bud-site selection in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 16: 1857–1870 [DOI] [PMC free article] [PubMed] [Google Scholar]
Zajac A., Sun X., Zhang J., Guo W., 2005. Cyclical regulation of the exocyst and cell polarity determinants for polarized cell growth. Mol. Biol. Cell 16: 1500–1512 [DOI] [PMC free article] [PubMed] [Google Scholar]
Zhang G., Kashimshetty R., Ng K. E., Tan H. B., Yeong F. M., 2006. Exit from mitosis triggers Chs2p transport from the endoplasmic reticulum to mother-daughter neck via the secretory pathway in budding yeast. J. Cell Biol. 174: 207–220 [DOI] [PMC free article] [PubMed] [Google Scholar]
Zhang J., Kong C., Xie H., McPherson P. S., Grinstein S., et al. , 1999. Phosphatidylinositol polyphosphate binding to the mammalian septin H5 is modulated by GTP. Curr. Biol. 9: 1458–1467 [DOI] [PubMed] [Google Scholar]
Zhang X., Bi E., Novick P., Du L., Kozminski K. G., et al. , 2001. Cdc42 interacts with the exocyst and regulates polarized secretion. J. Biol. Chem. 276: 46745–46750 [DOI] [PubMed] [Google Scholar]
Zhang X., Orlando K., He B., Xi F., Zhang J., et al. , 2008. Membrane association and functional regulation of Sec3 by phospholipids and Cdc42. J. Cell Biol. 180: 145–158 [DOI] [PMC free article] [PubMed] [Google Scholar]
Zheng Y., Hart M. J., Shinjo K., Evans T., Bender A., et al. , 1993. Biochemical comparisons of the Saccharomyces cerevisiae Bem2 and Bem3 proteins. Delineation of a limit Cdc42 GTPase-activating protein domain. J. Biol. Chem. 268: 24629–24634 [PubMed] [Google Scholar]
Zheng Y., Cerione R., Bender A., 1994. Control of the yeast bud-site assembly GTPase Cdc42. Catalysis of guanine nucleotide exchange by Cdc24 and stimulation of GTPase activity by Bem3. J. Biol. Chem. 269: 2369–2372 [PubMed] [Google Scholar]
Zheng Y., Bender A., Cerione R. A., 1995. Interactions among proteins involved in bud-site selection and bud-site assembly in Saccharomyces cerevisiae. J. Biol. Chem. 270: 626–630 [DOI] [PubMed] [Google Scholar]
Zigmond S. H., Evangelista M., Boone C., Yang C., Dar A. C., et al. , 2003. Formin leaky cap allows elongation in the presence of tight capping proteins. Curr. Biol. 13: 1820–1823 [DOI] [PubMed] [Google Scholar]
Ziman M., O’Brien J. M., Ouellette L. A., Church W. R., Johnson D. I., 1991. Mutational analysis of CDC42Sc, a Saccharomyces cerevisiae gene that encodes a putative GTP-binding protein involved in the control of cell polarity. Mol. Cell. Biol. 11: 3537–3544 [DOI] [PMC free article] [PubMed] [Google Scholar]
Ziman M., Preuss D., Mulholland J., O’Brien J. M., Botstein D., et al. , 1993. Subcellular localization of Cdc42p, a Saccharomyces cerevisiae GTP-binding protein involved in the control of cell polarity. Mol. Biol. Cell 4: 1307–1316 [DOI] [PMC free article] [PubMed] [Google Scholar]
Ziman M., Chuang J. S., Schekman R. W., 1996. Chs1p and Chs3p, two proteins involved in chitin synthesis, populate a compartment of the Saccharomyces cerevisiae endocytic pathway. Mol. Biol. Cell 7: 1909–1919 [DOI] [PMC free article] [PubMed] [Google Scholar]
Ziman M., Chuang J. S., Tsung M., Hamamoto S., Schekman R., 1998. Chs6p-dependent anterograde transport of Chs3p from the chitosome to the plasma membrane in Saccharomyces cerevisiae. Mol. Biol. Cell 9: 1565–1576 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib1] Abe M., Qadota H., Hirata A., Ohya Y., 2003. Lack of GTP-bound Rho1p in secretory vesicles of Saccharomyces cerevisiae. J. Cell Biol. 162: 85–97 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib2] Adames N., Blundell K., Ashby M. N., Boone C., 1995. Role of yeast insulin-degrading enzyme homologs in propheromone processing and bud site selection. Science 270: 464–467 [DOI] [PubMed] [Google Scholar]

[bib461] Adamo J. E., Rossi G., Brennwald P., 1999. The Rho GTPase Rho3 has a direct role in exocytosis that is distinct from its role in actin polarity. Mol. Biol. Cell 10: 4121–4133 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib3] Adamo J. E., Moskow J. J., Gladfelter A. S., Viterbo D., Lew D. J., et al. , 2001. Yeast Cdc42 functions at a late step in exocytosis, specifically during polarized growth of the emerging bud. J. Cell Biol. 155: 581–592 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib4] Adams A. E., Botstein D., Drubin D. G., 1989. A yeast actin-binding protein is encoded by SAC6, a gene found by suppression of an actin mutation. Science 243: 231–233 [DOI] [PubMed] [Google Scholar]

[bib5] Adams A. E., Botstein D., Drubin D. G., 1991. Requirement of yeast fimbrin for actin organization and morphogenesis in vivo. Nature 354: 404–408 [DOI] [PubMed] [Google Scholar]

[bib6] Adams A. E. M., Pringle J. R., 1984. Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae. J. Cell Biol. 98: 934–945 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib7] Adams A. E. M., Johnson D. I., Longnecker R. M., Sloat B. F., Pringle J. R., 1990. CDC42 and CDC43, two additional genes involved in budding and the establishment of cell polarity in the yeast Saccharomyces cerevisiae. J. Cell Biol. 111: 131–142 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib8] Aguilar R. C., Longhi S. A., Shaw J. D., Yeh L. Y., Kim S., et al. , 2006. From the Cover: epsin N-terminal homology domains perform an essential function regulating Cdc42 through binding Cdc42 GTPase-activating proteins. Proc. Natl. Acad. Sci. USA 103: 4116–4121 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib9] Albert S., Gallwitz D., 1999. Two new members of a family of Ypt/Rab GTPase activating proteins. Promiscuity of substrate recognition. J. Biol. Chem. 274: 33186–33189 [DOI] [PubMed] [Google Scholar]

[bib10] Almonacid M., Celton-Morizur S., Jakubowski J. L., Dingli F., Loew D., et al. , 2011. Temporal control of contractile ring assembly by Plo1 regulation of myosin II recruitment by Mid1/anillin. Curr. Biol. 21: 473–479 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib11] Altman R., Kellogg D., 1997. Control of mitotic events by Nap1 and the Gin4 kinase. J. Cell Biol. 138: 119–130 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib12] Amberg D. C., Zahner J. E., Mulholland J. W., Pringle J. R., Botstein D., 1997. Aip3p/Bud6p, a yeast actin-interacting protein that is involved in morphogenesis and the selection of bipolar budding sites. Mol. Biol. Cell 8: 729–753 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib13] Anderson B. L., Boldogh I., Evangelista M., Boone C., Greene L. A., et al. , 1998. The Src homology domain 3 (SH3) of a yeast type I myosin, Myo5p, binds to verprolin and is required for targeting to sites of actin polarization. J. Cell Biol. 141: 1357–1370 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib14] Andrews B. J., Herskowitz I., 1989. The yeast Swi4 protein contains a motif present in developmental regulators and is part of a complex involved in cell-cycle dependent transcription. Nature 342: 830–833 [DOI] [PubMed] [Google Scholar]

[bib15] Andrews B. J., Moore L. A., 1992. Interaction of the yeast Swi4 and Swi6 cell cycle regulatory proteins in vitro. Proc. Natl. Acad. Sci. USA 89: 11852–11856 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib16] Andrews P. D., Stark M. J., 2000. Dynamic, Rho1p-dependent localization of Pkc1p to sites of polarized growth. J. Cell Sci. 113: 2685–2693 [DOI] [PubMed] [Google Scholar]

[bib462] Annan R. B., Wu C., Waller D. D., Whiteway M., Thomas D. Y., 2008. Rho5p is involved in mediating the osmotic stress response in Saccharomyces cerevisiae, and its activity is regulated via Msi1p and Npr1p by phosphorylation and ubiquitination. Eukaryot. Cell 7: 1441–1449 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib17] Arkowitz R. A., 2009. Chemical gradients and chemotropism in yeast. Cold Spring Harb. Perspect. Biol. 1: a001958. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib19] Asakura T., Sasaki T., Nagano F., Satoh A., Obaishi H., et al. , 1998. Isolation and characterization of a novel actin filament-binding protein from Saccharomyces cerevisiae. Oncogene 16: 121–130 [DOI] [PubMed] [Google Scholar]

[bib20] Asano S., Park J. E., Yu L. R., Zhou M., Sakchaisri K., et al. , 2006. Direct phosphorylation and activation of a Nim1-related kinase Gin4 by Elm1 in budding yeast. J. Biol. Chem. 281: 27090–27098 [DOI] [PubMed] [Google Scholar]

[bib21] Audhya A., Emr S. D., 2002. Stt4 PI 4-kinase localizes to the plasma membrane and functions in the Pkc1-mediated MAP kinase cascade. Dev. Cell 2: 593–605 [DOI] [PubMed] [Google Scholar]

[bib22] Ayscough K. R., Stryker J., Pokala N., Sanders M., Crews P., et al. , 1997. High rates of actin filament turnover in budding yeast and roles for actin in establishment and maintenance of cell polarity revealed using the actin inhibitor Latrunculin-A. J. Cell Biol. 137: 399–416 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib23] Balasubramanian M. K., Bi E., Glotzer M., 2004. Comparative analysis of cytokinesis in budding yeast, fission yeast and animal cells. Curr. Biol. 14: R806–R818 [DOI] [PubMed] [Google Scholar]

[bib463] Barr F. A., Gruneberg U., 2007. Cytokinesis: placing and making the final cut. Cell 131: 847–860 [DOI] [PubMed] [Google Scholar]

[bib24] Bender A., 1993. Genetic evidence for the roles of the bud-site-selection genes BUD5 and BUD2 in control of the Rsr1p (Bud1p) GTPase in yeast. Proc. Natl. Acad. Sci. USA 90: 9926–9929 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib25] Bender A., Pringle J. R., 1989. Multicopy suppression of the cdc24 budding defect in yeast by CDC42 and three newly identified genes including the ras-related gene RSR1. Proc. Natl. Acad. Sci. USA 86: 9976–9980 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib26] Bender A., Pringle J. R., 1991. Use of a screen for synthetic lethal and multicopy suppressee mutants to identify two new genes involved in morphogenesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 11: 1295–1305 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib27] Benli M., Doring F., Robinson D. G., Yang X., Gallwitz D., 1996. Two GTPase isoforms, Ypt31p and Ypt32p, are essential for Golgi function in yeast. EMBO J. 15: 6460–6475 [PMC free article] [PubMed] [Google Scholar]

[bib28] Benton B., Tinkelenberg A. H., Jean D., Plump S. D., Cross F. R., 1993. Genetic analysis of Cln/Cdc28 regulation of cell morphogenesis in budding yeast. EMBO J. 12: 5267–5275 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib29] Benton B. K., Tinkelenberg A., Gonzalez I., Cross F. R., 1997. Cla4p, a Saccharomyces cerevisiae Cdc42p-activated kinase involved in cytokinesis, is activated at mitosis. Mol. Cell. Biol. 17: 5067–5076 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib30] Bertin A., McMurray M. A., Grob P., Park S. S., Garcia G., 3rd, et al. , 2008. Saccharomyces cerevisiae septins: supramolecular organization of heterooligomers and the mechanism of filament assembly. Proc. Natl. Acad. Sci. USA 105: 8274–8279 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib31] Bertin A., McMurray M. A., Thai L., Garcia G., 3rd, Votin V., et al. , 2010. Phosphatidylinositol-4,5-bisphosphate promotes budding yeast septin filament assembly and organization. J. Mol. Biol. 404: 711–731 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib32] Bi E., 2001. Cytokinesis in budding yeast: the relationship between actomyosin ring function and septum formation. Cell Struct. Funct. 26: 529–537 [DOI] [PubMed] [Google Scholar]

[bib33] Bi E., Maddox P., Lew D. J., Salmon E. D., McMillan J. N., et al. , 1998. Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis. J. Cell Biol. 142: 1301–1312 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib34] Bi E., Chiavetta J. B., Chen H., Chen G.-C., Chan C. S. M., et al. , 2000. Identification of novel, evolutionarily conserved Cdc42p-interacting proteins and of redundant pathways linking Cdc24p and Cdc42p to actin polarization in yeast. Mol. Biol. Cell 11: 773–793 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib35] Blacketer M. J., Koehler C. M., Coats S. G., Myers A. M., Madaule P., 1993. Regulation of dimorphism in Saccharomyces cerevisiae: involvement of the novel protein kinase homolog Elm1p and protein phosphatase 2A. Mol. Cell. Biol. 13: 5567–5581 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib36] Blondel M., Bach S., Bamps S., Dobbelaere J., Wiget P., et al. , 2005. Degradation of Hof1 by SCF(Grr1) is important for actomyosin contraction during cytokinesis in yeast. EMBO J. 24: 1440–1452 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib37] Bobola N., Jansen R. P., Shin T. H., Nasmyth K., 1996. Asymmetric accumulation of Ash1p in postanaphase nuclei depends on a myosin and restricts yeast mating-type switching to mother cells. Cell 84: 699–709 [DOI] [PubMed] [Google Scholar]

[bib38] Bose I., Irazoqui J. E., Moskow J. J., Bardes E. S. G., Zyla T. R., et al. , 2001. Assembly of scaffold-mediated complexes containing Cdc42p, the exchange factor Cdc24p, and the effector Cla4p required for cell cycle regulated phosphorylation of Cdc24p. J. Biol. Chem. 276: 7176–7186 [DOI] [PubMed] [Google Scholar]

[bib39] Bouquin N., Barral Y., Courbeyrette R., Blondel M., Snyder M., et al. , 2000. Regulation of cytokinesis by the Elm1 protein kinase in Saccharomyces cerevisiae. J. Cell Sci. 113: 1435–1445 [DOI] [PubMed] [Google Scholar]

[bib40] Boyd C., Hughes T., Pypaert M., Novick P., 2004. Vesicles carry most exocyst subunits to exocytic sites marked by the remaining two subunits, Sec3p and Exo70p. J. Cell Biol. 167: 889–901 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib41] Boyne J. R., Yosuf H. M., Bieganowski P., Brenner C., Price C., 2000. Yeast myosin light chain, Mlc1p, interacts with both IQGAP and class II myosin to effect cytokinesis. J. Cell Sci. 113: 4533–4543 [DOI] [PubMed] [Google Scholar]

[bib42] Bretscher A., 2003. Polarized growth and organelle segregation in yeast: the tracks, motors, and receptors. J. Cell Biol. 160: 811–816 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib43] Brown J. L., Jaquenoud M., Gulli M. P., Chant J., Peter M., 1997. Novel Cdc42-binding proteins Gic1 and Gic2 control cell polarity in yeast. Genes Dev. 11: 2972–2982 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib44] Bulawa C. E., 1992. CSD2, CSD3, and CSD4, genes required for chitin synthesis in Saccharomyces cerevisiae: the CSD2 gene product is related to chitin synthases and to developmentally regulated proteins in Rhizobium species and Xenopus laevis. Mol. Cell. Biol. 12: 1764–1776 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib45] Bulawa C. E., 1993. Genetics and molecular biology of chitin synthesis in fungi. Annu. Rev. Microbiol. 47: 505–534 [DOI] [PubMed] [Google Scholar]

[bib46] Burbelo P. D., Drechsel D., Hall A., 1995. A conserved binding motif defines numerous candidate target proteins for both Cdc42 and Rac GTPases. J. Biol. Chem. 270: 29071–29074 [DOI] [PubMed] [Google Scholar]

[bib47] Buttery S. M., Yoshida S., Pellman D., 2007. Yeast formins Bni1 and Bnr1 utilize different modes of cortical interaction during the assembly of actin cables. Mol. Biol. Cell 18: 1826–1838 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib48] Butty A. C., Perrinjaquet N., Petit A., Jaquenoud M., Segall J. E., et al. , 2002. A positive feedback loop stabilizes the guanine-nucleotide exchange factor Cdc24 at sites of polarization. EMBO J. 21: 1565–1576 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib49] Byers B., Goetsch L., 1976a. A highly ordered ring of membrane-associated filaments in budding yeast. J. Cell Biol. 69: 717–721 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib50] Byers B., Goetsch L., 1976b. Loss of the filamentous ring in cytokinesis-defective mutants of budding yeast. J. Cell Biol. 70: 35a. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib51] Cabib E., Roh D. H., Schmidt M., Crotti L. B., Varma A., 2001. The yeast cell wall and septum as paradigms of cell growth and morphogenesis. J. Biol. Chem. 276: 19679–19682 [DOI] [PubMed] [Google Scholar]

[bib52] Cabib E., Schmidt M., 2003. Chitin synthase III activity, but not the chitin ring, is required for remedial septa formation in budding yeast. FEMS Microbiol. Lett. 224: 299–305 [DOI] [PubMed] [Google Scholar]

[bib53] Carlsson A. E., Shah A. D., Elking D., Karpova T. S., Cooper J. A., 2002. Quantitative analysis of actin patch movement in yeast. Biophys. J. 82: 2333–2343 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib54] Casamayor A., Snyder M., 2003. Molecular dissection of a yeast septin: distinct domains are required for septin interaction, localization, and function. Mol. Cell. Biol. 23: 2762–2777 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib55] Caviston J. P., Tcheperegine S. E., Bi E., 2002. Singularity in budding: a role for the evolutionarily conserved small GTPase Cdc42p. Proc. Natl. Acad. Sci. USA 99: 12185–12190 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib56] Caviston J. P., Longtine M., Pringle J. R., Bi E., 2003. The role of Cdc42p GTPase-activating proteins in assembly of the septin ring in yeast. Mol. Biol. Cell 14: 4051–4066 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib57] Caydasi A. K., Kurtulmus B., Orrico M. I., Hofmann A., Ibrahim B., et al. , 2010. Elm1 kinase activates the spindle position checkpoint kinase Kin4. J. Cell Biol. 190: 975–989 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib58] Chant J., Herskowitz I., 1991. Genetic control of bud site selection in yeast by a set of gene products that constitute a morphogenetic pathway. Cell 65: 1203–1212 [DOI] [PubMed] [Google Scholar]

[bib59] Chant J., Pringle J. R., 1995. Patterns of bud-site selection in the yeast Saccharomyces cerevisiae. J. Cell Biol. 129: 751–765 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib60] Chant J., Corrado K., Pringle J. R., Herskowitz I., 1991. Yeast BUD5, encoding a putative GDP-GTP exchange factor, is necessary for bud site selection and interacts with bud formation gene BEM1. Cell 65: 1213–1224 [DOI] [PubMed] [Google Scholar]

[bib61] Chant J., Mischke M., Mitchell E., Herskowitz I., Pringle J. R., 1995. Role of Bud3p in producing the axial budding pattern of yeast. J. Cell Biol. 129: 767–778 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib62] Chen G.-C., Zheng L., Chan C. S. M., 1996. The LIM domain-containing Dbm1 GTPase-activating protein is required for the normal cellular morphogenesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 16: 1376–1390 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib63] Chen G.-C., Kim Y.-J., Chan C. S. M., 1997. The Cdc42 GTPase-associated proteins Gic1 and Gic2 are required for polarized cell growth in Saccharomyces cerevisiae. Genes Dev. 11: 2958–2971 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib64] Chen T., Hiroko T., Chaudhuri A., Inose F., Lord M., et al. , 2000. Multigenerational cortical inheritance of the Rax2 protein in orienting polarity and division in yeast. Science 290: 1975–1978 [DOI] [PubMed] [Google Scholar]

[bib65] Chen W., Lim H. H., Lim L., 1993. The CDC42 homologue from Caenorhabditis elegans. Complementation of yeast mutation. J. Biol. Chem. 268: 13280–13285 [PubMed] [Google Scholar]

[bib66] Chenevert J., Corrado K., Bender B., Pringle J. R., Herskowitz I., 1992. A yeast gene (BEM1) necessary for cell polarization whose product contains two SH3 domains. Nature 356: 77–79 [DOI] [PubMed] [Google Scholar]

[bib67] Chenevert J., Valtz N., Herskowitz I., 1994. Identification of genes required for normal pheromone-induced cell polarization in Saccharomyces cerevisiae. Genetics 136: 1287–1296 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib68] Chuang J. S., Schekman R. W., 1996. Differential trafficking and timed localization of two chitin synthase proteins, Chs2p and Chs3p. J. Cell Biol. 135: 597–610 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib69] Chuang T. H., Xu X., Knaus U. G., Hart M. J., Bokoch G. M., 1993. GDP dissociation inhibitor prevents intrinsic and GTPase activating protein-stimulated GTP hydrolysis by the Rac GTP-binding protein. J. Biol. Chem. 268: 775–778 [PubMed] [Google Scholar]

[bib70] Cid V. J., Adamikova L., Sanchez M., Molina M., Nombela C., 2001. Cell cycle control of septin ring dynamics in the budding yeast. Microbiology 147: 1437–1450 [DOI] [PubMed] [Google Scholar]

[bib72] Cole K. C., Barbour J. E., Midkiff J. F., Marble B. M., Johnson D. I., 2009. Multiple proteins and phosphorylations regulate Saccharomyces cerevisiae Cdc24p localization. FEBS Lett. 583: 3339–3343 [DOI] [PubMed] [Google Scholar]

[bib73] Corbett M., Xiong Y., Boyne J. R., Wright D. J., Munro E., et al. , 2006. IQGAP and mitotic exit network (MEN) proteins are required for cytokinesis and re-polarization of the actin cytoskeleton in the budding yeast, Saccharomyces cerevisiae. Eur. J. Cell Biol. 85: 1201–1215 [DOI] [PubMed] [Google Scholar]

[bib74] Court H., Sudbery P., 2007. Regulation of Cdc42 GTPase activity in the formation of hyphae in Candida albicans. Mol. Biol. Cell 18: 265–281 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib75] Cvrckova F., Nasmyth K., 1993. Yeast G1 cyclins CLN1 and CLN2 and a GAP-like protein have a role in bud formation. EMBO J. 12: 5277–5286 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib76] Cvrckova F., De Virgilio C., Manser E., Pringle J. R., Nasmyth K., 1995. Ste20-like protein kinases are required for normal localization of cell growth and for cytokinesis in budding yeast. Genes Dev. 9: 1817–1830 [DOI] [PubMed] [Google Scholar]

[bib77] D’Silva S., Haider S. J., Phizicky E. M., 2011. A domain of the actin binding protein Abp140 is the yeast methyltransferase responsible for 3-methylcytidine modification in the tRNA anti-codon loop. RNA 17: 1100–1110 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib78] De Smet I., Beeckman T., 2011. Asymmetric cell division in land plants and algae: the driving force for differentiation. Nat. Rev. Mol. Cell Biol. 12: 177–188 [DOI] [PubMed] [Google Scholar]

[bib80] Delley P. A., Hall M. N., 1999. Cell wall stress depolarizes cell growth via hyperactivation of RHO1. J. Cell Biol. 147: 163–174 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib81] DeMarini D. J., Adams A. E. M., Fares H., De Virgilio C., Valle G., et al. , 1997. A septin-based hierarchy of proteins required for localized deposition of chitin in the Saccharomyces cerevisiae cell wall. J. Cell Biol. 139: 75–93 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib82] Denis V., Cyert M. S., 2005. Molecular analysis reveals localization of Saccharomyces cerevisiae protein kinase C to sites of polarized growth and Pkc1p targeting to the nucleus and mitotic spindle. Eukaryot. Cell 4: 36–45 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib83] Desrivieres S., Cooke F. T., Parker P. J., Hall M. N., 1998. MSS4, a phosphatidylinositol-4-phosphate 5-kinase required for organization of the actin cytoskeleton in Saccharomyces cerevisiae. J. Biol. Chem. 273: 15787–15793 [DOI] [PubMed] [Google Scholar]

[bib84] Dickens N. J., Beatson S., Ponting C. P., 2002. Cadherin-like domains in [alpha]-dystroglycan, [alpha]/[epsilon]-sarcoglycan and yeast and bacterial proteins. Curr. Biol. 12: R197–R199 [DOI] [PubMed] [Google Scholar]

[bib85] Dickinson J. R., 2008. Filament formation in Saccharomyces cerevisiae. Folia Microbiol. (Praha) 53: 3–14 [DOI] [PubMed] [Google Scholar]

[bib86] Dobbelaere J., Barral Y., 2004. Spatial coordination of cytokinetic events by compartmentalization of the cell cortex. Science 305: 393–396 [DOI] [PubMed] [Google Scholar]

[bib87] Dobbelaere J., Gentry M. S., Hallberg R. L., Barral Y., 2003. Phosphorylation-dependent regulation of septin dynamics during the cell cycle. Dev. Cell 4: 345–357 [DOI] [PubMed] [Google Scholar]

[bib88] Dodou E., Treisman R., 1997. The Saccharomyces cerevisiae MADS-box transcription factor Rlm1 is a target for the Mpk1 mitogen-activated protein kinase pathway. Mol. Cell. Biol. 17: 1848–1859 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib89] Doignon F., Weinachter C., Roumanie O., Crouzet M., 1999. The yeast Rgd1p is a GTPase activating protein of the Rho3 and rho4 proteins. FEBS Lett. 459: 458–462 [DOI] [PubMed] [Google Scholar]

[bib90] Dong Y., Pruyne D., Bretscher A., 2003. Formin-dependent actin assembly is regulated by distinct modes of Rho signaling in yeast. J. Cell Biol. 161: 1081–1092 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib91] Donnelly S. F., Pocklington M. J., Pallotta D., Orr E., 1993. A proline-rich protein, verprolin, involved in cytoskeletal organization and cellular growth in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 10: 585–596 [DOI] [PubMed] [Google Scholar]

[bib92] Douglas C. M., Foor F., Marrinan J. A., Morin N., Nielsen J. B., et al. , 1994. The Saccharomyces cerevisiae FKS1 (ETG1) gene encodes an integral membrane protein which is a subunit of 1,3-β-D-glucan synthase. Proc. Natl. Acad. Sci. USA 91: 12907–12911 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib93] Doyle T., Botstein D., 1996. Movement of yeast cortical actin cytoskeleton visualized in vivo. Proc. Natl. Acad. Sci. USA 93: 3886–3891 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib94] Drees B., Brown C., Barrell B. G., Bretscher A., 1995. Tropomyosin is essential in yeast, yet the TPM1 and TPM2 products perform distinct functions. J. Cell Biol. 128: 383–392 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib95] Drees B. L., Sundin B., Brazeau E., Caviston J. P., Chen G.-C., et al. , 2001. A protein interaction map for cell polarity development. J. Cell Biol. 154: 549–571 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib96] Drgonova J., Drgon T., Tanaka K., Kollar R., Chen G. C., et al. , 1996. Rho1p, a yeast protein at the interface between cell polarization and morphogenesis. Science 272: 277–279 [DOI] [PubMed] [Google Scholar]

[bib97] Drgonova J., Drgon T., Roh D. H., Cabib E., 1999. The GTP-binding protein Rho1p is required for cell cycle progression and polarization of the yeast cell. J. Cell Biol. 146: 373–387 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib98] Drubin D. G., Nelson W. J., 1996. Origins of cell polarity. Cell 84: 335–344 [DOI] [PubMed] [Google Scholar]

[bib99] Dunn T. M., Shortle D., 1990. Null alleles of SAC7 suppress temperature-sensitive actin mutations in Saccharomyces cerevisiae. Mol. Cell. Biol. 10: 2308–2314 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib100] Eaton S., Auvinen P., Luo L., Jan Y. N., Simons K., 1995. CDC42 and Rac1 control different actin-dependent processes in the Drosophila wing disc epithelium. J. Cell Biol. 131: 151–164 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib101] Egelhofer T. A., Villen J., McCusker D., Gygi S. P., Kellogg D. R., 2008. The septins function in G1 pathways that influence the pattern of cell growth in budding yeast. PLoS ONE 3: e2022. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib102] Eggert U. S., Mitchison T. J., Field C. M., 2006. Animal cytokinesis: from parts list to mechanisms. Annu. Rev. Biochem. 75: 543–566 [DOI] [PubMed] [Google Scholar]

[bib103] Eitzen G., Thorngren N., Wickner W., 2001. Rho1p and Cdc42p act after Ypt7p to regulate vacuole docking. EMBO J. 20: 5650–5656 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib104] Engqvist-Goldstein A. E., Drubin D. G., 2003. Actin assembly and endocytosis: from yeast to mammals. Annu. Rev. Cell Dev. Biol. 19: 287–332 [DOI] [PubMed] [Google Scholar]

[bib105] Epp J. A., Chant J., 1997. An IQGAP-related protein controls actin-ring formation and cytokinesis in yeast. Curr. Biol. 7: 921–929 [DOI] [PubMed] [Google Scholar]

[bib106] Estrada P., Kim J., Coleman J., Walker L., Dunn B., et al. , 2003. Myo4p and She3p are required for cortical ER inheritance in Saccharomyces cerevisiae. J. Cell Biol. 163: 1255–1266 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib107] Etienne-Manneville S., 2004. Cdc42–the centre of polarity. J. Cell Sci. 117: 1291–1300 [DOI] [PubMed] [Google Scholar]

[bib108] Evangelista M., Blundell K., Longtine M. S., Chow C. J., Adames N., et al. , 1997. Bni1p, a yeast formin linking Cdc42p and the actin cytoskeleton during polarized morphogenesis. Science 276: 118–122 [DOI] [PubMed] [Google Scholar]

[bib109] Evangelista M., Pruyne D., Amberg D. C., Boone C., Bretscher A., 2002. Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat. Cell Biol. 4: 32–41 [DOI] [PubMed] [Google Scholar]

[bib110] Fang X., Luo J., Nishihama R., Wloka C., Dravis C., et al. , 2010. Biphasic targeting and cleavage furrow ingression directed by the tail of a myosin-II. J. Cell Biol. 191: 1333–1350 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib111] Farkas V., Kovarik J., Kosinova A., Bauer S., 1974. Autoradiographic study of mannan incorporation into the growing cell walls of Saccharomyces cerevisiae. J. Bacteriol. 117: 265–269 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib112] Finger F. P., Novick P., 1997. Sec3p is involved in secretion and morphogenesis in Saccharomyces cerevisiae. Mol. Biol. Cell 8: 647–662 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib113] Finger F. P., Hughes T. E., Novick P., 1998. Sec3p is a spatial landmark for polarized secretion in budding yeast. Cell 92: 559–571 [DOI] [PubMed] [Google Scholar]

[bib114] Fitch P. G., Gammie A. E., Lee D. J., de Candal V. B., Rose M. D., 2004. Lrg1p Is a Rho1 GTPase-activating protein required for efficient cell fusion in yeast. Genetics 168: 733–746 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib115] Flescher E. G., Madden K., Snyder M., 1993. Components required for cytokinesis are important for bud site selection in yeast. J. Cell Biol. 122: 373–386 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib116] France Y. E., Boyd C., Coleman J., Novick P. J., 2006. The polarity-establishment component Bem1p interacts with the exocyst complex through the Sec15p subunit. J. Cell Sci. 119: 876–888 [DOI] [PubMed] [Google Scholar]

[bib117] Frazier J. A., Wong M. L., Longtine M. S., Pringle J. R., Mann M., et al. , 1998. Polymerization of purified yeast septins: evidence that organized filament arrays may not be required for septin function. J. Cell Biol. 143: 737–749 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib118] Freifelder D., 1960. Bud position in Saccharomyces cerevisiae. J. Bacteriol. 80: 567–568 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib119] Fujita A., Oka C., Arikawa Y., Katagai T., Tonouchi A., et al. , 1994. A yeast gene necessary for bud-site selection encodes a protein similar to insulin-degrading enzymes. Nature 372: 567–570 [DOI] [PubMed] [Google Scholar]

[bib120] Fujita A., Lord M., Hiroko T., Hiroko F., Chen T., et al. , 2004. Rax1, a protein required for the establishment of the bipolar budding pattern in yeast. Gene 327: 161–169 [DOI] [PubMed] [Google Scholar]

[bib121] Fujiwara T., Tanaka K., Mino A., Kikyo M., Takahashi K., et al. , 1998. Rho1p-Bni1p-Spa2p interactions: implication in localization of Bni1p at the bud site and regulation of the actin cytoskeleton in Saccharomyces cerevisiae. Mol. Biol. Cell 9: 1221–1233 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib122] Fukumoto Y., Kaibuchi K., Hori Y., Fujioka H., Araki S., et al. , 1990. Molecular cloning and characterization of a novel type of regulatory protein (GDI) for the rho proteins, ras p21-like small GTP-binding proteins. Oncogene 5: 1321–1328 [PubMed] [Google Scholar]

[bib123] Gao L., Liu W., Bretscher A., 2010. The yeast formin Bnr1p has two localization regions that show spatially and temporally distinct association with septin structures. Mol. Biol. Cell 21: 1253–1262 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib124] Gao X. D., Albert S., Tcheperegine S. E., Burd C. G., Gallwitz D., et al. , 2003. The GAP activity of Msb3p and Msb4p for the Rab GTPase Sec4p is required for efficient exocytosis and actin organization. J. Cell Biol. 162: 635–646 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib126] Gao X. D., Sperber L. M., Kane S. A., Tong Z., Hin Yan Tong A., et al. , 2007. Sequential and distinct roles of the cadherin domain-containing protein Axl2p in cell polarization in yeast cell cycle. Mol. Biol. Cell 18: 2542–2560 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib127] Garrenton L. S., Stefan C. J., McMurray M. A., Emr S. D., Thorner J., 2010. Pheromone-induced anisotropy in yeast plasma membrane phosphatidylinositol-4,5-bisphosphate distribution is required for MAPK signaling. Proc. Natl. Acad. Sci. USA 107: 11805–11810 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib464] Geli M. I., Riezman H., 1996. Role of type I myosins in receptor-mediated endocytosis in yeast. Science. 272: 533–535 [DOI] [PubMed] [Google Scholar]

[bib465] Geli M. I., Lombardi R., Schmelzl B., Riezman H., 2000. An intact SH3 domain is required for myosin I-induced actin polymerization. EMBO J. 19: 4281–4291 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib128] Gladfelter A. S., Pringle J. R., Lew D. J., 2001. The septin cortex at the yeast mother-bud neck. Curr. Opin. Microbiol. 4: 681–689 [DOI] [PubMed] [Google Scholar]

[bib129] Gladfelter A. S., Bose I., Zyla T. R., Bardes E. S. G., Lew D. J., 2002. Septin ring assembly involves cycles of GTP loading and hydrolysis by Cdc42p. J. Cell Biol. 156: 315–326 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib130] Gladfelter, A. S., T. R. Zyla, and D. J. Lew, 2004. Genetic interactions among regulators of septin organization. Eukaryot. Cell 3: 847–854 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib131] Goehring A. S., Mitchell D. A., Tong A. H., Keniry M. E., Boone C., et al. , 2003. Synthetic lethal analysis implicates Ste20p, a p21-activated potein kinase, in polarisome activation. Mol. Biol. Cell 14: 1501–1516 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib132] Goodman A., Goode B. L., Matsudaira P., Fink G. R., 2003. The Saccharomyces cerevisiae calponin/transgelin homolog Scp1 functions with fimbrin to regulate stability and organization of the actin cytoskeleton. Mol. Biol. Cell 14: 2617–2629 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib466] Goodson H. V., Anderson B. L., Warrick H. M., Pon L. A., Spudich J. A., 1996. Synthetic lethality screen identifies a novel yeast myosin I gene (MYO5): myosin I proteins are required for polarization of the actin cytoskeleton. J. Cell Biol. 133: 1277–1291 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib133] Goryachev A. B., Pokhilko A. V., 2008. Dynamics of Cdc42 network embodies a Turing-type mechanism of yeast cell polarity. FEBS Lett. 582: 1437–1443 [DOI] [PubMed] [Google Scholar]

[bib134] Goud B., Salminen A., Walworth N. C., Novick P. J., 1988. A GTP-binding protein required for secretion rapidly associates with secretory vesicles and plasma membrane in yeast. Cell 53: 753–768 [DOI] [PubMed] [Google Scholar]

[bib135] Govindan B., Bowser R., Novick P., 1995. The role of Myo2, a yeast class V myosin, in vesicular transport. J. Cell Biol. 128: 1055–1068 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib136] Grosshans B. L., Ortiz D., Novick P., 2006. Rabs and their effectors: achieving specificity in membrane traffic. Proc. Natl. Acad. Sci. USA 103: 11821–11827 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib137] Gulli M.-P., Jaquenoud M., Shimada Y., Niederhauser G., Wiget P., et al. , 2000. Phosphorylation of the Cdc42 exchange factor Cdc24 by the Pak-like kinase Cla4 may regulate polarized growth in yeast. Mol. Cell 6: 1155–1167 [DOI] [PubMed] [Google Scholar]

[bib138] Guo W., Grant A., Novick P., 1999a. Exo84p is an exocyst protein essential for secretion. J. Biol. Chem. 274: 23558–23564 [DOI] [PubMed] [Google Scholar]

[bib139] Guo W., Roth D., Walch-Solimena C., Novick P., 1999b. The exocyst is an effector for Sec4p, targeting secretory vesicles to sites of exocytosis. EMBO J. 18: 1071–1080 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib140] Guo W., Sacher M., Barrowman J., Ferro-Novick S., Novick P., 2000. Protein complexes in transport vesicle targeting. Trends Cell Biol. 10: 251–255 [DOI] [PubMed] [Google Scholar]

[bib141] Guo W., Tamanoi F., Novick P., 2001. Spatial regulation of the exocyst complex by Rho1 GTPase. Nat. Cell Biol. 3: 353–360 [DOI] [PubMed] [Google Scholar]

[bib142] Haarer B. K., Pringle J. R., 1987. Immunofluorescence localization of the Saccharomyces cerevisiae CDC12 gene product to the vicinity of the 10-nm filaments in the mother-bud neck. Mol. Cell. Biol. 7: 3678–3687 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib143] Haarer B. K., Lillie S. H., Adams A. E., Magdolen V., Bandlow W., et al. , 1990. Purification of profilin from Saccharomyces cerevisiae and analysis of profilin-deficient cells. J. Cell Biol. 110: 105–114 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib144] Haarer B. K., Corbett A., Kweon Y., Petzold A. S., Silver P., et al. , 1996. SEC3 mutations are synthetically lethal with profilin mutations and cause defects in diploid-specific bud-site selection. Genetics 144: 495–510 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib145] Hall P. A., Russell S. E. H., Pringle J. R., 2008. The Septins. John Wiley & Sons, New York [Google Scholar]

[bib146] Halme A., Michelitch M., Mitchell E. L., Chant J., 1996. Bud10p directs axial cell polarization in budding yeast and resembles a transmembrane receptor. Curr. Biol. 6: 570–579 [DOI] [PubMed] [Google Scholar]

[bib147] Hancock J. F., Hall A., 1993. A novel role for RhoGDI as an inhibitor of GAP proteins. EMBO J. 12: 1915–1921 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib148] Harkins H. A., Pagé N., Schenkman L. R., De Virgilio C., Shaw S., et al. , 2001. Bud8p and Bud9p, proteins that may mark the sites for bipolar budding in yeast. Mol. Biol. Cell 12: 2497–2518 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib149] Hart M. J., Maru Y., Leonard D., Witte O. N., Evans T., et al. , 1992. A GDP dissociation inhibitor that serves as a GTPase inhibitor for the Ras-like protein CDC42Hs. Science 258: 812–815 [DOI] [PubMed] [Google Scholar]

[bib150] Hartwell L. H., 1971a. Genetic control of the cell division cycle in yeast II. Genes controlling DNA replication and its initiation. J. Mol. Biol. 59: 183–194 [DOI] [PubMed] [Google Scholar]

[bib151] Hartwell L. H., 1971b. Genetic control of the cell division cycle in yeast. IV. Genes controlling bud emergence and cytokinesis. Exp. Cell Res. 69: 265–276 [DOI] [PubMed] [Google Scholar]

[bib152] He B., Xi F., Zhang X., Zhang J., Guo W., 2007. Exo70 interacts with phospholipids and mediates the targeting of the exocyst to the plasma membrane. EMBO J. 26: 4053–4065 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib153] Heinisch J. J., Lorberg A., Schmitz H. P., Jacoby J. J., 1999. The protein kinase C-mediated MAP kinase pathway involved in the maintenance of cellular integrity in Saccharomyces cerevisiae. Mol. Microbiol. 32: 671–680 [DOI] [PubMed] [Google Scholar]

[bib154] Helliwell S. B., Schmidt A., Ohya Y., Hall M. N., 1998. The Rho1 effector Pkc1, but not Bni1, mediates signalling from Tor2 to the actin cytoskeleton. Curr. Biol. 8: 1211–1214 [DOI] [PubMed] [Google Scholar]

[bib155] Hergovich A., Hemmings B. A., 2009. Mammalian NDR/LATS protein kinases in hippo tumor suppressor signaling. Biofactors 35: 338–345 [DOI] [PubMed] [Google Scholar]

[bib156] Herskowitz I., 1988. Life cycle of the budding yeast Saccharomyces cerevisiae. Microbiol. Rev. 52: 536–553 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib157] Hicks J. B., Strathern J. N., Herskowitz I., 1977. Interconversion of yeast mating types III. Action of the homothallism (HO) gene in cells homozygous for the mating type locus. Genetics 85: 395–405 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib158] Hofken T., Schiebel E., 2002. A role for cell polarity proteins in mitotic exit. EMBO J. 21: 4851–4862 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib159] Holt L. J., Tuch B. B., Villen J., Johnson A. D., Gygi S. P., et al. , 2009. Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution. Science 325: 1682–1686 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib160] Hori Y., Kikuchi A., Isomura M., Katayama M., Miura Y., et al. , 1991. Post-translational modifications of the C-terminal region of the Rho protein are important for its interaction with membranes and the stimulatory and inhibitory GDP/GTP exchange proteins. Oncogene 6: 515–522 [PubMed] [Google Scholar]

[bib161] Howell A. S., Lew D. J. 2012. Morphogenesis and the cell cycle. Genetics 190:51–77 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib162] Howell A. S., Savage N. S., Johnson S. A., Bose I., Wagner A. W., et al. , 2009. Singularity in polarization: rewiring yeast cells to make two buds. Cell 139: 731–743 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib164] Huckaba T. M., Lipkin T., Pon L. A., 2006. Roles of type II myosin and a tropomyosin isoform in retrograde actin flow in budding yeast. J. Cell Biol. 175: 957–969 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib165] Huh W. K., Falvo J. V., Gerke L. C., Carroll A. S., Howson R. W., et al. , 2003. Global analysis of protein localization in budding yeast. Nature 425: 686–691 [DOI] [PubMed] [Google Scholar]

[bib166] Hutagalung A. H., Novick P. J., 2011. Role of Rab GTPases in membrane traffic and cell physiology. Physiol. Rev. 91: 119–149 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib167] Huxley H., Hanson J., 1954. Changes in the cross-striations of muscle during contraction and stretch and their structural interpretation. Nature 173: 973–976 [DOI] [PubMed] [Google Scholar]

[bib168] Huxley H. E., 1969. The mechanism of muscular contraction. Science 164: 1356–1365 [PubMed] [Google Scholar]

[bib169] Imamura H., Tanaka K., Hihara T., Umikawa M., Kamei T., et al. , 1997. Bni1p and Bnr1p: downstream targets of the Rho family small G-proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae. EMBO J. 16: 2745–2755 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib170] Inoue S. B., Takewaki N., Takasuka T., Mio T., Adachi M., et al. , 1995. Characterization and gene cloning of 1,3-beta-D-glucan synthase from Saccharomyces cerevisiae. Eur. J. Biochem. 231: 845–854 [DOI] [PubMed] [Google Scholar]

[bib171] Irazoqui J. E., Gladfelter A. S., Lew D. J., 2003. Scaffold-mediated symmetry breaking by Cdc42p. Nat. Cell Biol. 5: 1062–1070 [DOI] [PubMed] [Google Scholar]

[bib172] Irazoqui J. E., Howell A. S., Theesfeld C. L., Lew D. J., 2005. Opposing roles for actin in Cdc42p polarization. Mol. Biol. Cell 16: 1296–1304 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib173] Irie K., Takase M., Lee K. S., Levin D. E., Araki H., et al. , 1993. MKK1 and MKK2, which encode Saccharomyces cerevisiae mitogen-activated protein kinase-kinase homologs, function in the pathway mediated by protein kinase C. Mol. Cell. Biol. 13: 3076–3083 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib174] Ishihara S., Hirata A., Nogami S., Beauvais A., Latge J. P., et al. , 2007. Homologous subunits of 1,3-beta-glucan synthase are important for spore wall assembly in Saccharomyces cerevisiae. Eukaryot. Cell 6: 143–156 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib175] Ishimi Y., Kikuchi A., 1991. Identification and molecular cloning of yeast homolog of nucleosome assembly protein I which facilitates nucleosome assembly in vitro. J. Biol. Chem. 266: 7025–7029 [PubMed] [Google Scholar]

[bib176] Iwase M., Toh-e A., 2001. Nis1 encoded by YNL078W: a new neck protein of Saccharomyces cerevisiae. Genes Genet. Syst. 76: 335–343 [DOI] [PubMed] [Google Scholar]

[bib177] Iwase M., Luo J., Nagaraj S., Longtine M., Kim H. B., et al. , 2006. Role of a cdc42p effector pathway in recruitment of the yeast septins to the presumptive bud site. Mol. Biol. Cell 17: 1110–1125 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib178] Iwase M., Luo J., Bi E., Toh-e A., 2007. Shs1 plays separable roles in septin organization and cytokinesis in Saccharomyces cerevisiae. Genetics 177: 215–229 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib179] Jaquenoud M., Peter M., 2000. Gic2p may link activated Cdc42p to components involved in actin polarization, including Bni1p and Bud6p (Aip3p). Mol. Cell. Biol. 20: 6244–6258 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib180] Jaquenoud M., Gulli M. P., Peter K., Peter M., 1998. The Cdc42p effector Gic2p is targeted for ubiquitin-dependent degradation by the SCFGrr1 complex. EMBO J. 17: 5360–5373 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib181] Jedd G., Mulholland J., Segev N., 1997. Two new Ypt GTPases are required for exit from the yeast trans-Golgi compartment. J. Cell Biol. 137: 563–580 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib182] Jendretzki A., Ciklic I., Rodicio R., Schmitz H. P., Heinisch J. J., 2009. Cyk3 acts in actomyosin ring independent cytokinesis by recruiting Inn1 to the yeast bud neck. Mol. Genet. Genomics 282: 437–451 [DOI] [PubMed] [Google Scholar]

[bib183] Joberty G., Perlungher R. R., Sheffield P. J., Kinoshita M., Noda M., et al. , 2001. Borg proteins control septin organization and are negatively regulated by Cdc42. Nat. Cell Biol. 3: 861–866 [DOI] [PubMed] [Google Scholar]

[bib184] Johnson D. I., Pringle J. R., 1990. Molecular characterization of CDC42, a Saccharomyces cerevisiae gene involved in the development of cell polarity. J. Cell Biol. 111: 143–152 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib185] Johnson E. S., Blobel G., 1999. Cell cycle-regulated attachment of the ubiquitin-related protein SUMO to the yeast septins. J. Cell Biol. 147: 981–993 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib186] Johnson E. S., Gupta A. A., 2001. An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106: 735–744 [DOI] [PubMed] [Google Scholar]

[bib187] Johnson J. L., Erickson J. W., Cerione R. A., 2009. New insights into how the Rho guanine nucleotide dissociation inhibitor regulates the interaction of Cdc42 with membranes. J. Biol. Chem. 284: 23860–23871 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib188] Johnston G. C., Prendergast J. A., Singer R. A., 1991. The Saccharomyces cerevisiae MYO2 gene encodes an essential myosin for vectorial transport of vesicles. J. Cell Biol. 113: 539–551 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib189] Kadota J., Yamamoto T., Yoshiuchi S., Bi E., Tanaka K., 2004. Septin ring assembly requires concerted action of polarisome components, a PAK kinase Cla4p, and the actin cytoskeleton in Saccharomyces cerevisiae. Mol. Biol. Cell 15: 5329–5345 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib467] Kaksonen M., Sun Y., Drubin D. G., 2003. A pathway for association of receptors, adaptors, and actin during endocytic internalization. Cell 115: 475–487 [DOI] [PubMed] [Google Scholar]

[bib190] Kaksonen M., Toret C. P., Drubin D. G., 2005. A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123: 305–320 [DOI] [PubMed] [Google Scholar]

[bib191] Kaksonen M., Toret C. P., Drubin D. G., 2006. Harnessing actin dynamics for clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 7: 404–414 [DOI] [PubMed] [Google Scholar]

[bib192] Kamada Y., Jung U. S., Piotrowski J., Levin D. E., 1995. The protein kinase C-activated MAP kinase pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response. Genes Dev. 9: 1559–1571 [DOI] [PubMed] [Google Scholar]

[bib193] Kamada Y., Qadota H., Python C. P., Anraku Y., Ohya Y., et al. , 1996. Activation of yeast protein kinase C by Rho1 GTPase. J. Biol. Chem. 271: 9193–9196 [DOI] [PubMed] [Google Scholar]

[bib194] Kamei T., Tanaka K., Hihara T., Umikawa M., Imamura H., et al. , 1998. Interaction of Bnr1p with a novel Src Homology 3 domain-containing Hof1p. Implication in cytokinesis in Saccharomyces cerevisiae. J. Biol. Chem. 273: 28341–28345 [DOI] [PubMed] [Google Scholar]

[bib196] Kang P. J., Sanson A., Lee B., Park H.-O., 2001. A GDP/GTP exchange factor involved in linking a spatial landmark to cell polarity. Science 292: 1376–1378 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib197] Kang P. J., Angerman E., Nakashima K., Pringle J. R., Park H.-O., 2004a. Interactions among Rax1p, Rax2p, Bud8p, and Bud9p in marking cortical sites for bipolar bud-site selection in yeast. Mol. Biol. Cell 15: 5145–5157 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib198] Kang P. J., Lee B., Park H.-O., 2004b. Specific residues of the GDP/GTP exchange factor Bud5p are involved in establishment of the cell type-specific budding pattern in yeast. J. Biol. Chem. 279: 27980–27985 [DOI] [PubMed] [Google Scholar]

[bib199] Kang P. J., Beven L., Hariharan S., Park H.-O., 2010. The Rsr1/Bud1 GTPase interacts with itself and the Cdc42 GTPase during bud-site selection and polarity establishment in budding yeast. Mol. Biol. Cell 21: 3007–3016 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib468] Kang P. J., Angerman E., Jung C.-H., Park H.-O., 2012. Bud4 mediates the cell-type-specific assembly of the axial landmark in budding yeast. J. Cell Sci. (in press) [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib200] Karpova T. S., McNally J. G., Moltz S. L., Cooper J. A., 1998. Assembly and function of the actin cytoskeleton of yeast: relationships between cables and patches. J. Cell Biol. 142: 1501–1517 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib201] Kawasaki R., Fujimura-Kamada K., Toi H., Kato H., Tanaka K., 2003. The upstream regulator, Rsr1p, and downstream effector, Gic1p and Gic2p, of the Cdc42p small GTPase coordinately regulate initiation of budding in Saccharomyces cerevisiae. Genes Cells 8: 235–250 [DOI] [PubMed] [Google Scholar]

[bib202] Kellogg D. R., Kikuchi A., Fujii-Nakata T., Turck C. W., Murray A. W., 1995. Members of the NAP/SET family of proteins interact specifically with B-type cyclins. J. Cell Biol. 130: 661–673 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib203] Kikyo M., Tanaka K., Kamei T., Ozaki K., Fujiwara T., et al. , 1999. An FH domain-containing Bnr1p is a multifunctional protein interacting with a variety of cytoskeletal proteins in Saccharomyces cerevisiae. Oncogene 18: 7046–7054 [DOI] [PubMed] [Google Scholar]

[bib205] Kim Y.-J., Francisco L., Chen G.-C., Marcotte E., Chan C. S. M., 1994. Control of cellular morphogenesis by the Ipl2/Bem2 GTPase-activating protein: Possible role of protein phosphorylation. J. Cell Biol. 127: 1381–1394 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib206] Klis F. M., Boorsma A., De Groot P. W., 2006. Cell wall construction in Saccharomyces cerevisiae. Yeast 23: 185–202 [DOI] [PubMed] [Google Scholar]

[bib207] Knaus M., Pelli-Gulli M. P., van Drogen F., Springer S., Jaquenoud M., et al. , 2007. Phosphorylation of Bem2p and Bem3p may contribute to local activation of Cdc42p at bud emergence. EMBO J. 26: 4501–4513 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib208] Knoblich J. A., 2010. Asymmetric cell division: recent developments and their implications for tumour biology. Nat. Rev. Mol. Cell Biol. 11: 849–860 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib209] Ko N., Nishihama R., Tully G. H., Ostapenko D., Solomon M. J., et al. , 2007. Identification of yeast IQGAP (Iqg1p) as an anaphase-promoting-complex substrate and its role in actomyosin-ring-independent cytokinesis. Mol. Biol. Cell 18: 5139–5153 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib210] Koch G., Tanaka K., Masuda T., Yamochi W., Nonaka H., et al. , 1997. Association of the Rho family small GTP-binding proteins with Rho GDP dissociation inhibitor (Rho GDI) in Saccharomyces cerevisiae. Oncogene 15: 417–422 [DOI] [PubMed] [Google Scholar]

[bib211] Kohno H., Tanaka K., Mino A., Umikawa M., Imamura H., et al. , 1996. Bni1p implicated in cytoskeletal control is a putative target of Rho1p small GTP binding protein in Saccharomyces cerevisiae. EMBO J. 15: 6060–6068 [PMC free article] [PubMed] [Google Scholar]

[bib212] Korinek W. S., Bi E., Epp J. A., Wang L., Ho J., et al. , 2000. Cyk3, a novel SH3-domain protein, affects cytokinesis in yeast. Curr. Biol. 10: 947–950 [DOI] [PubMed] [Google Scholar]

[bib213] Kost B., 2008. Spatial control of Rho (Rac-Rop) signaling in tip-growing plant cells. Trends Cell Biol. 18: 119–127 [DOI] [PubMed] [Google Scholar]

[bib214] Kovar D. R., Sirotkin V., Lord M., 2011. Three’s company: the fission yeast actin cytoskeleton. Trends Cell Biol. 21: 177–187 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib215] Kozminski K. G., Beven L., Angerman E., Tong A. H. Y., Boone C., et al. , 2003. Interaction between a Ras and a Rho GTPase couples selection of a growth site to the development of cell polarity in yeast. Mol. Biol. Cell 14: 4958–4970 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib216] Kozubowski L., Larson J. R., Tatchell K., 2005. Role of the septin ring in the asymmetric localization of proteins at the mother-bud neck in Saccharomyces cerevisiae. Mol. Biol. Cell 16: 3455–3466 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib217] Kozubowski L., Saito K., Johnson J. M., Howell A. S., Zyla T. R., et al. , 2008. Symmetry-breaking polarization driven by a Cdc42p GEF-PAK complex. Curr. Biol. 18: 1719–1726 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib218] Krappmann A.-B., Taheri N., Heinrich M., Mosch H.-U., 2007. Distinct domains of yeast cortical tag proteins Bud8p and Bud9p confer polar localization and functionality. Mol. Biol. Cell 18: 3323–3339 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib219] Laporte D., Coffman V. C., Lee I. J., Wu J. Q., 2011. Assembly and architecture of precursor nodes during fission yeast cytokinesis. J. Cell Biol. 192: 1005–1021 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib220] Layton A. T., Savage N. S., Howell A. S., Carroll S. Y., Drubin D. G., et al. , 2011. Modeling vesicle traffic reveals unexpected consequences for cdc42p-mediated polarity establishment. Curr. Biol. 21: 184–194 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib221] Leberer E., Dignard D., Harcus D., Thomas D. Y., Whiteway M., 1992. The protein kinase homologue Ste20p is required to link the yeast pheromone response G-protein βγ subunits to downstream signalling components. EMBO J. 11: 4815–4824 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib222] Lechler T., Jonsdottir G. A., Klee S. K., Pellman D., Li R., 2001. A two-tiered mechanism by which Cdc42 controls the localization and activation of an Arp2/3-activating motor complex in yeast. J. Cell Biol. 155: 261–270 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib223] Lee K. S., Levin D. E., 1992. Dominant mutations in a gene encoding a putative protein kinase (BCK1) bypass the requirement for a Saccharomyces cerevisiae protein kinase C homolog. Mol. Cell. Biol. 12: 172–182 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib224] Lee K. S., Irie K., Gotoh Y., Watanabe Y., Araki H., et al. , 1993. A yeast mitogen-activated protein kinase homolog (Mpk1p) mediates signalling by protein kinase C. Mol. Cell. Biol. 13: 3067–3075 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib225] Lee L., Klee S. K., Evangelista M., Boone C., Pellman D., 1999. Control of mitotic spindle position by the Saccharomyces cerevisiae formin Bni1p. J. Cell Biol. 144: 947–961 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib226] Lee M. E., Singh K., Snider J., Shenoy A., Paumi C. M., et al. , 2011. The Rho1 GTPase acts together with a vacuolar glutathione S-conjugate transporter to protect yeast cells from oxidative stress. Genetics 188: 859–870 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib227] Lee P. R., Song S., Ro H. S., Park C. J., Lippincott J., et al. , 2002. Bni5p, a septin-interacting protein, is required for normal septin function and cytokinesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 22: 6906–6920 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib228] Leeuw T., Fourest-Lieuvin A., Wu C., Chenevert J., Clark K., et al. , 1995. Pheromone response in yeast: association of Bem1p with proteins of the MAP kinase cascade and actin. Science 270: 1210–1213 [DOI] [PubMed] [Google Scholar]

[bib229] Leeu w, T., Wu C., Schrag J. D., Whiteway M., Thomas D. Y., et al. , 1998. Interaction of a G-protein b-subunit with a conserved sequence in Ste20/PAK family protein kinases. Nature 391: 191–195 [DOI] [PubMed] [Google Scholar]

[bib230] Leonard D., Hart M. J., Platko J. V., Eva A., Henzel W., et al. , 1992. The identification and characterization of a GDP-dissociation inhibitor (GDI) for the CDC42Hs protein. J. Biol. Chem. 267: 22860–22868 [PubMed] [Google Scholar]

[bib231] Lesage G., Bussey H., 2006. Cell wall assembly in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 70: 317–343 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib232] Levin D. E., 2005. Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69: 262–291 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib233] Levin D. E., Bartlett-Heubusch E., 1992. Mutants in the S. cerevisiae PKC1 gene display a cell cycle-specific osmotic stability defect. J. Cell Biol. 116: 1221–1229 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib234] Levin D. E., Fields F. O., Kunisawa R., Bishop J. M., Thorner J., 1990. A candidate protein kinase C gene, PKC1, is required for the S. cerevisiae cell cycle. Cell 62: 213–224 [DOI] [PubMed] [Google Scholar]

[bib235] Levin D. E., Bowers B., Chen C. Y., Kamada Y., Watanabe M., 1994. Dissecting the protein kinase C/MAP kinase signalling pathway of Saccharomyces cerevisiae. Cell. Mol. Biol. Res. 40: 229–239 [PubMed] [Google Scholar]

[bib236] Lew D. J., Reed S. I., 1993. Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins. J. Cell Biol. 120: 1305–1320 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib237] Li R., 1997. Bee1, a yeast protein with homology to Wiscott-Aldrich syndrome protein, is critical for the assembly of cortical actin cytoskeleton. J. Cell Biol. 136: 649–658 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib238] Lillie S. H., Brown S. S., 1994. Immunofluorescence localization of the unconventional myosin, Myo2p, and the putative kinesin-related protein, Smy1p, to the same regions of polarized growth in Saccharomyces cerevisiae. J. Cell Biol. 125: 825–842 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib239] Lin M., Unden H., Jacquier N., Schneiter R., Just U., et al. , 2009. The Cdc42 effectors Ste20, Cla4, and Skm1 down-regulate the expression of genes involved in sterol uptake by a mitogen-activated protein kinase-independent pathway. Mol. Biol. Cell 20: 4826–4837 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib240] Lippincott J., Li R., 1998a. Sequential assembly of myosin II, an IQGAP-like protein, and filamentous actin to a ring structure involved in budding yeast cytokinesis. J. Cell Biol. 140: 355–366 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib241] Lippincott J., Li R., 1998b. Dual function of Cyk2, a cdc15/PSTPIP family protein, in regulating actomyosin ring dynamics and septin distribution. J. Cell Biol. 143: 1947–1960 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib242] Lippincott J., Shannon K. B., Shou W., Deshaies R. J., Li R., 2001. The Tem1 small GTPase controls actomyosin and septin dynamics during cytokinesis. J. Cell Sci. 114: 1379–1386 [DOI] [PubMed] [Google Scholar]

[bib243] Liu H. P., Bretscher A., 1989a. Disruption of the single tropomyosin gene in yeast results in the disappearance of actin cables from the cytoskeleton. Cell 57: 233–242 [DOI] [PubMed] [Google Scholar]

[bib244] Liu H. P., Bretscher A., 1989b. Purification of tropomyosin from Saccharomyces cerevisiae and identification of related proteins in Schizosaccharomyces and Physarum. Proc. Natl. Acad. Sci. USA 86: 90–93 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib245] Logan M. R., Jones L., Forsberg D., Bodman A., Baier A., et al. , 2011. Functional analysis of RhoGDI inhibitory activity on vacuole membrane fusion. Biochem. J. 434: 445–457 [DOI] [PubMed] [Google Scholar]

[bib246] Longtine M., Bi E., 2003. Regulation of septin organization and function in yeast. Trends Cell Biol. 13: 403–409 [DOI] [PubMed] [Google Scholar]

[bib247] Longtine M. S., DeMarini D. J., Valencik M. L., Al-Awar O. S., Fares H., et al. , 1996. The septins: roles in cytokinesis and other processes. Curr. Opin. Cell Biol. 8: 106–119 [DOI] [PubMed] [Google Scholar]

[bib248] Longtine M. S., Fares H., Pringle J. R., 1998. Role of the yeast Gin4p protein kinase in septin assembly and the relationship between septin assembly and septin function. J. Cell Biol. 143: 719–736 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib249] Longtine M. S., Theesfeld C. L., McMillan J. N., Weaver E., Pringle J. R., et al. , 2000. Septin-dependent assembly of a cell cycle-regulatory module in Saccharomyces cerevisiae. Mol. Cell. Biol. 20: 4049–4061 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib250] Lorberg A., Schmitz H. P., Jacoby J. J., Heinisch J. J., 2001. Lrg1p functions as a putative GTPase-activating protein in the Pkc1p-mediated cell integrity pathway in Saccharomyces cerevisiae. Mol. Genet. Genomics 266: 514–526 [DOI] [PubMed] [Google Scholar]

[bib251] Lord M., Yang M. C., Mischke M., Chant J., 2000. Cell cycle programs of gene expression control morphogenetic protein localization. J. Cell Biol. 151: 1501–1512 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib252] Lord M., Inose F., Hiroko T., Hata T., Fujita A., et al. , 2002. Subcellular localization of Axl1, the cell type-specific regulator of polarity. Curr. Biol. 12: 1347–1352 [DOI] [PubMed] [Google Scholar]

[bib253] Lord M., Laves E., Pollard T. D., 2005. Cytokinesis depends on the motor domains of myosin-II in fission yeast but not in budding yeast. Mol. Biol. Cell 16: 5346–5355 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib254] Luo J., Vallen E. A., Dravis C., Tcheperegine S. E., Drees B. L., et al. , 2004. Identification and functional analysis of the essential and regulatory light chains of the only type II myosin Myo1p in Saccharomyces cerevisiae. J. Cell Biol. 165: 843–855 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib255] Luo L., Liao Y. J., Jan L. Y., Jan Y. N., 1994. Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 8: 1787–1802 [DOI] [PubMed] [Google Scholar]

[bib256] Madania A., Dumoulin P., Grava S., Kitamoto H., Scharer-Brodbeck C., et al. , 1999. The Saccharomyces cerevisiae homologue of human Wiskott-Aldrich syndrome protein Las17p interacts with the Arp2/3 complex. Mol. Biol. Cell 10: 3521–3538 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib469] Madaule P., Axel R., Myers A. M., 1987. Characterization of two members of the RHO gene family from the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 84: 779–783 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib257] Manning B. D., Padmanabha R., Snyder M., 1997. The Rho-GEF Rom2p localizes to sites of polarized cell growth and participates in cytoskeletal functions in Saccharomyces cerevisiae. Mol. Biol. Cell 8: 1829–1844 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib258] Marquitz A. R., Harrison J. C., Bose I., Zyla T. R., McMillan J. N., et al. , 2002. The Rho-GAP Bem2p plays a GAP-independent role in the morphogenesis checkpoint. EMBO J. 21: 4012–4025 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib259] Marston A. L., Chen T., Yang M. C., Belhumeur P., Chant J., 2001. A localized GTPase exchange factor, Bud5, determines the orientation of division axes in yeast. Curr. Biol. 11: 803–807 [DOI] [PubMed] [Google Scholar]

[bib260] Martin H., Mendoza A., Rodriguez-Pachon J. M., Molina M., Nombela C., 1997. Characterization of SKM1, a Saccharomyces cerevisiae gene encoding a novel Ste20/PAK-like protein kinase. Mol. Microbiol. 23: 431–444 [DOI] [PubMed] [Google Scholar]

[bib261] Martin H., Rodriguez-Pachon J. M., Ruiz C., Nombela C., Molina M., 2000. Regulatory mechanisms for modulation of signaling through the cell integrity Slt2-mediated pathway in Saccharomyces cerevisiae. J. Biol. Chem. 275: 1511–1519 [DOI] [PubMed] [Google Scholar]

[bib262] Martinez-Rucobo F. W., Eckhardt-Strelau L., Terwisscha van Scheltinga A. C., 2009. Yeast chitin synthase 2 activity is modulated by proteolysis and phosphorylation. Biochem. J. 417: 547–554 [DOI] [PubMed] [Google Scholar]

[bib263] Masuda T., Tanaka K., Nonaka H., Yamochi W., Maeda A., et al. , 1994. Molecular cloning and characterization of yeast Rho GDP dissociation inhibitor. J. Biol. Chem. 269: 19713–19718 [PubMed] [Google Scholar]

[bib470] Matsui Y., Toh-e A., 1992. Yeast RHO3 and RHO4 ras superfamily genes are necessary for bud growth, and their defect is suppressed by a high dose of bud formation genes CDC42 and BEM1. Mol. Cell. Biol. 12: 5690–5699 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib264] Mazur P., Baginsky W., 1996. In vitro activity of 1,3-beta-D-glucan synthase requires the GTP-binding protein Rho1. J. Biol. Chem. 271: 14604–14609 [DOI] [PubMed] [Google Scholar]

[bib265] Mazur P., Morin N., Baginsky W., el-Sherbeini M., Clemas J. A., et al. , 1995. Differential expression and function of two homologous subunits of yeast 1,3-beta-D-glucan synthase. Mol. Cell. Biol. 15: 5671–5681 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib266] Mazzoni C., Zarzov P., Rambourg A., Mann C., 1993. The SLT2(MPK1) map kinase homolog is involved in polarized cell growth in Saccharomyces cerevisiae. J. Cell Biol. 123: 1821–1833 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib267] McCaffrey M., Johnson J. S., Goud B., Myers A. M., Rossier J., et al. , 1991. The small GTP-binding protein Rho1p is localized on the Golgi apparatus and post-Golgi vesicles in Saccharomyces cerevisiae. J. Cell Biol. 115: 309–319 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib268] McMurray M. A., Thorner J., 2009. Septins: molecular partitioning and the generation of cellular asymmetry. Cell Div. 4: 18. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib269] McMurray M. A., Bertin A., Garcia G., 3rd, Lam L., Nogales E., et al. , 2011. Septin filament formation is essential in budding yeast. Dev. Cell 20: 540–549 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib270] Meitinger F., Petrova B., Mancini Lombardi I., Bertazzi D. T., Hub B., et al. , 2010. Targeted localization of Inn1, Cyk3 and Chs2 by the mitotic-exit network regulates cytokinesis in budding yeast. J. Cell Sci. 123: 1851–1861 [DOI] [PubMed] [Google Scholar]

[bib271] Meitinger F., Boehm M. E., Hofmann A., Hub B., Zentgraf H., et al. , 2011. Phosphorylation-dependent regulation of the F-BAR protein Hof1 during cytokinesis. Genes Dev. 25: 875–888 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib272] Michelitch M., Chant J., 1996. A mechanism of Bud1p GTPase action suggested by mutational analysis and immunolocalization. Curr. Biol. 6: 446–454 [DOI] [PubMed] [Google Scholar]

[bib273] Miller P. J., Johnson D. I., 1994. Cdc42p GTPase is involved in controlling polarized cell growth in Schizosaccharomyces pombe. Mol. Cell. Biol. 14: 1075–1083 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib274] Miller R., Matheos D., Rose M. D., 1999. The cortical localization of the microtubule orientation protein, Kar9p, is dependent upon actin and proteins required for polarization. J. Cell Biol. 144: 963–975 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib275] Mino A., Tanaka K., Kamei T., Umikawa M., Fujiwara T., et al. , 1998. Shs1p: a novel member of septin that interacts with Spa2p, involved in polarized growth in Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 251: 732–736 [DOI] [PubMed] [Google Scholar]

[bib276] Moore J. K., Stuchell-Brereton M. D., Cooper J. A., 2009. Function of dynein in budding yeast: mitotic spindle positioning in a polarized cell. Cell Motil. Cytoskeleton 66: 546–555 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib277] Moore J. K., Chudalayandi P., Heil-Chapdelaine R. A., Cooper J. A., 2010. The spindle position checkpoint is coordinated by the Elm1 kinase. J. Cell Biol. 191: 493–503 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib278] Mortensen E. M., McDonald H., Yates J., 3rd, Kellogg D. R., 2002. Cell cycle-dependent assembly of a Gin4-septin complex. Mol. Biol. Cell 13: 2091–2105 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib279] Mosammaparast N., Ewart C. S., Pemberton L. F., 2002. A role for nucleosome assembly protein 1 in the nuclear transport of histones H2A and H2B. EMBO J. 21: 6527–6538 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib280] Moseley J. B., Goode B. L., 2005. Differential activities and regulation of Saccharomyces cerevisiae formin proteins Bni1 and Bnr1 by Bud6. J. Biol. Chem. 280: 28023–28033 [DOI] [PubMed] [Google Scholar]

[bib281] Moseley J. B., Goode B. L., 2006. The yeast actin cytoskeleton: from cellular function to biochemical mechanism. Microbiol. Mol. Biol. Rev. 70: 605–645 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib282] Moseley J. B., Sagot I., Manning A. L., Xu Y., Eck M. J., et al. , 2004. A conserved mechanism for Bni1- and mDia1-induced actin assembly and dual regulation of Bni1 by Bud6 and profilin. Mol. Biol. Cell 15: 896–907 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib283] Mukherjee D., Coon B. G., Edwards D. F., 3rd, Hanna C. B., Longhi S. A., et al. , 2009. The yeast endocytic protein Epsin 2 functions in a cell-division signaling pathway. J. Cell Sci. 122: 2453–2463 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib284] Muller L., Xu G., Wells R., Hollenberg C. P., Piepersberg W., 1994. LRG1 is expressed during sporulation in Saccharomyces cerevisiae and contains motifs similar to LIM and rho/racGAP domains. Nucleic Acids Res. 22: 3151–3154 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib285] Munemitsu S., Innis M. A., Clark R., McCormick F., Ullrich A., et al. , 1990. Molecular cloning and expression of a G25K cDNA, the human homolog of the yeast cell cycle gene CDC42. Mol. Cell. Biol. 10: 5977–5982 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib471] Munn A. L., Stevenson B. J., Geli M. I., Riezman H., 1995. end5, end6, and end7: mutations that cause actin delocalization and block the internalization step of endocytosis in Saccharomyces cerevisiae. Mol. Biol. Cell 6: 1721–1742 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib286] Nasmyth K., Dirick L., 1991. The role of SWI4 and SWI6 in the activity of G1 cyclins in yeast. Cell 66: 995–1013 [DOI] [PubMed] [Google Scholar]

[bib287] Nelson B., Kurischko C., Horecka J., Mody M., Nair P., et al. , 2003. RAM: a conserved signaling network that regulates Ace2p transcriptional activity and polarized morphogenesis. Mol. Biol. Cell 14: 3782–3803 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib288] Nern A., Arkowitz R. A., 1999. A Cdc24-Far1p-G beta gamma protein complex required for yeast orientation during mating. J. Cell Biol. 144: 1187–1202 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib289] Nern A., Arkowitz R. A., 2000. Nucleocytoplasmic shuttling of the Cdc42p exchange factor Cdc24p. J. Cell Biol. 148: 1115–1122 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib290] Ni L., Snyder M., 2001. A genomic study of the bipolar bud site selection pattern in Saccharomyces cerevisiae. Mol. Biol. Cell 12: 2147–2170 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib291] Nishihama R., Schreiter J. H., Onishi M., Vallen E. A., Hanna J., et al. , 2009. Role of Inn1 and its interactions with Hof1 and Cyk3 in promoting cleavage furrow and septum formation in S. cerevisiae. J. Cell Biol. 185: 995–1012 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib292] Noma A., Yi S., Katoh T., Takai Y., Suzuki T., 2011. Actin-binding protein Abp140 is a methyltransferase for 3-methylcytidine at position 32 of tRNAs in Saccharomyces cerevisiae. RNA 17: 1111–1119 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib293] Nomanbhoy T. K., Cerione R., 1996. Characterization of the interaction between RhoGDI and Cdc42Hs using fluorescence spectroscopy. J. Biol. Chem. 271: 10004–10009 [DOI] [PubMed] [Google Scholar]

[bib294] Novick P., Botstein D., 1985. Phenotypic analysis of temperature-sensitive yeast actin mutants. Cell 40: 405–416 [DOI] [PubMed] [Google Scholar]

[bib296] Oh Y., Bi E., 2011. Septin structure and function in yeast and beyond. Trends Cell Biol. 21: 141–148 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib297] Okuzaki D., Tanaka S., Kanazawa H., Nojima H., 1997. Gin4 of S. cerevisiae is a bud neck protein that interacts with the Cdc28 complex. Genes Cells 2: 753–770 [DOI] [PubMed] [Google Scholar]

[bib298] Orlando K., Zhang J., Zhang X., Yue P., Chiang T., et al. , 2008. Regulation of Gic2 localization and function by phosphatidylinositol 4,5-bisphosphate during the establishment of cell polarity in budding yeast. J. Biol. Chem. 283: 14205–14212 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib299] Orlando K., Sun X., Zhang J., Lu T., Yokomizo L., et al. , 2011. Exo-endocytic trafficking and the septin-based diffusion barrier are required for the maintenance of Cdc42p polarization during budding yeast asymmetrical growth. Mol. Biol. Cell 22: 624–633 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib300] Ortiz D., Medkova M., Wach-Solimena C., Novick P., 2002. Ypt32 recruits the Sec4p guanine nucleotide exchange factor, Sec2p, to secretory vesicles; evidence for a Rab cascade in yeast. J. Cell Biol. 157: 1005–1015 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib301] Ozaki K., Tanaka K., Imamura H., Hihara T., Kameyama T., et al. , 1996. Rom1p and Rom2p are GDP/GTP exchange proteins (GEPs) for the Rho1p small GTP binding proteins in Saccharomyces cerevisiae. EMBO J. 15: 2196–2207 [PMC free article] [PubMed] [Google Scholar]

[bib302] Ozaki-Kuroda K., Yamamoto Y., Nohara H., Kinoshita M., Fujiwara T., et al. , 2001. Dynamic localization and function of Bni1p at the sites of directed growth in Saccharomyces cerevisiae. Mol. Cell. Biol. 21: 827–839 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib303] Ozbudak E. M., Becskei A., van Oudenaarden A., 2005. A system of counteracting feedback loops regulates Cdc42p activity during spontaneous cell polarization. Dev. Cell 9: 565–571 [DOI] [PubMed] [Google Scholar]

[bib304] Paciorek T., Bergmann D. C., 2010. The secret to life is being different: asymmetric divisions in plant development. Curr. Opin. Plant Biol. 13: 661–669 [DOI] [PubMed] [Google Scholar]

[bib305] Padmanabhan A., Bakka K., Sevugan M., Naqvi N. I., D’Souza V., et al. , 2011. IQGAP-related Rng2p organizes cortical nodes and ensures position of cell division in fission yeast. Curr. Biol. 21: 467–472 [DOI] [PubMed] [Google Scholar]

[bib306] Palmer R. E., Sullivan D. S., Huffaker T., Koshland D., 1992. Role of astral microtubules and actin in spindle orientation and migration in the budding yeast, Saccharomyces cerevisiae. J. Cell Biol. 119: 583–593 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib307] Parent S. A., Nielsen J. B., Morin N., Chrebet G., Ramadan N., et al. , 1993. Calcineurin-dependent growth of an FK506- and CsA-hypersensitive mutant of Saccharomyces cerevisiae. J. Gen. Microbiol. 139: 2973–2984 [DOI] [PubMed] [Google Scholar]

[bib308] Park H. O., Bi E., 2007. Central roles of small GTPases in the development of cell polarity in yeast and beyond. Microbiol. Mol. Biol. Rev. 71: 48–96 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib309] Park H. O., Chant J., 1996. Bud2 protein, pp. 200–203 The Guidebook to the Small GTPases, edited by Zerial M., Huber L. Oxford Press, Oxford [Google Scholar]

[bib310] Park H. O., Bi E., Pringle J. R., Herskowitz I., 1997. Two active states of the Ras-related Bud1/Rsr1 protein bind to different effectors to determine yeast cell polarity. Proc. Natl. Acad. Sci. USA 94: 4463–4468 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib311] Park H.-O., Chant J., Herskowitz I., 1993. BUD2 encodes a GTPase-activating protein for Bud1/Rsr1 necessary for proper bud-site selection in yeast. Nature 365: 269–274 [DOI] [PubMed] [Google Scholar]

[bib312] Park H.-O., Sanson A., Herskowitz I., 1999. Localization of Bud2p, a GTPase-activating protein necessary for programming cell polarity in yeast to the presumptive bud site. Genes Dev. 13: 1912–1917 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib313] Park H.-O., Kang P. J., Rachfal A. W., 2002. Localization of the Rsr1/Bud1 GTPase involved in selection of a proper growth site in yeast. J. Biol. Chem. 277: 26721–26724 [DOI] [PubMed] [Google Scholar]

[bib314] Perez P., Rincon S. A., 2010. Rho GTPases: regulation of cell polarity and growth in yeasts. Biochem. J. 426: 243–253 [DOI] [PubMed] [Google Scholar]

[bib315] Peter M., Neiman A. M., Park H. O., van Lohuizen M., Herskowitz I., 1996. Functional analysis of the interaction between the small GTP binding protein Cdc42 and the Ste20 protein kinase in yeast. EMBO J. 15: 7046–7059 [PMC free article] [PubMed] [Google Scholar]

[bib316] Peterson J., Zheng Y., Bender L., Myers A., Cerione R., et al. , 1994. Interactions between the bud emergence proteins Bem1p and Bem2p and rho-type GTPases in yeast. J. Cell Biol. 127: 1395–1406 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib317] Philip B., Levin D. E., 2001. Wsc1 and Mid2 are cell surface sensors for cell wall integrity signaling that act through Rom2, a guanine nucleotide exchange factor for Rho1. Mol. Cell. Biol. 21: 271–280 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib318] Pollard T. D., 2008. Progress towards understanding the mechanism of cytokinesis in fission yeast. Biochem. Soc. Trans. 36: 425–430 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib319] Pollard T. D., 2010. Mechanics of cytokinesis in eukaryotes. Curr. Opin. Cell Biol. 22: 50–56 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib320] Pollard T. D., Borisy G. G., 2003. Cellular motility driven by assembly and disassembly of actin filaments. Cell 113: 549. [DOI] [PubMed] [Google Scholar]

[bib321] Powers J., Barlowe C., 2002. Erv14p directs a transmembrane secretory protein into COPII-coated transport vesicles. Mol. Biol. Cell 142: 1209–1222 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib322] Powers S., Gonzales E., Christensen T., Cubert J., Broek D., 1991. Functional cloning of BUD5, a CDC25-related gene from S. cerevisiae that can suppress a dominant-negative RAS2 mutant. Cell 65: 1225–1231 [DOI] [PubMed] [Google Scholar]

[bib323] Pring M., Evangelista M., Boone C., Yang C., Zigmond S. H., 2003. Mechanism of formin-induced nucleation of actin filaments. Biochemistry 42: 486–496 [DOI] [PubMed] [Google Scholar]

[bib324] Pringle J. R., Hartwell L. H., 1981. The Saccharomyces cerevisiae cell cycle, pp. 97–142 The molecular biology of the yeast Saccharomyces. Life cycle and inheritance, edited by Strathern J. N., Jones E. W., Broach J. R. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y [Google Scholar]

[bib325] Pringle J. R., Bi E., Harkins H. A., Zahner J. E., De Virgilio C., et al. , 1995. Establishment of cell polarity in yeast. Cold Spring Harb. Symp. Quant. Biol. 60: 729–744 [DOI] [PubMed] [Google Scholar]

[bib326] Pruyne D., Bretscher A., 2000a. Polarization of cell growth in yeast. II. The role of the cortical actin cytoskeleton. J. Cell Sci. 113: 571–585 [DOI] [PubMed] [Google Scholar]

[bib327] Pruyne D., Bretscher A., 2000b. Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J. Cell Sci. 113: 365–375 [DOI] [PubMed] [Google Scholar]

[bib328] Pruyne D. W., Schott D. H., Bretscher A., 1998. Tropomyosin-containing actin cables direct the Myo2p-dependent polarized delivery of secretory vesicles in budding yeast. J. Cell Biol. 143: 1931–1945 [DOI] [PubMed] [Google Scholar]

[bib329] Pruyne D., Evangelista M., Yang C., Bi E., Zigmond S., et al. , 2002. Role of formins in actin assembly: nucleation and barbed end association. Science 297: 612–615 [DOI] [PubMed] [Google Scholar]

[bib330] Pruyne D., Gao L., Bi E., Bretscher A., 2004. Stable and dynamic axes of polarity use distinct formin isoforms in budding yeast. Mol. Biol. Cell 15: 4971–4989 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib331] Qadota H., Python C. P., Inoue S. B., Arisawa M., Anraku Y., et al. , 1996. Identification of yeast Rho1p GTPase as a regulatory subunit of 1,3-β-glucan synthase. Science 272: 279–281 [DOI] [PubMed] [Google Scholar]

[bib332] Ramer S. W., Davis R. W., 1993. A dominant truncation allele identifies a gene, STE20, that encodes a putative protein kinase necessary for mating in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 90: 452–456 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib335] Richman T. J., Sawyer M. M., Johnson D. I., 2002. Saccharomyces cerevisiae Cdc42p localizes to cellular membranes and clusters at sites of polarized growth. Eukaryot. Cell 1: 458–468 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib336] Richman T. J., Toenjes K. A., Morales S. E., Cole K. C., Wasserman B. T., et al. , 2004. Analysis of cell-cycle specific localization of the Rdi1p RhoGDI and the structural determinants required for Cdc42p membrane localization and clustering at sites of polarized growth. Curr. Genet. 45: 339–349 [DOI] [PubMed] [Google Scholar]

[bib337] Riedl J., Crevenna A. H., Kessenbrock K., Yu J. H., Neukirchen D., et al. , 2008. Lifeact: a versatile marker to visualize F-actin. Nat. Methods 5: 605–607 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib338] Rivera-Molina F. E., Novick P. J., 2009. A Rab GAP cascade defines the boundary between two Rab GTPases on the secretory pathway. Proc. Natl. Acad. Sci. USA 106: 14408–14413 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib339] Robinson N. G., Guo L., Imai J., Toh E. A., Matsui Y., et al. , 1999. Rho3 of Saccharomyces cerevisiae, which regulates the actin cytoskeleton and exocytosis, is a GTPase which interacts with Myo2 and Exo70. Mol. Cell. Biol. 19: 3580–3587 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib475] Rodal A. A., Kozubowski L., Goode B. L., Drubin D. G., Hartwig J. H., 2005. Actin and septin ultrastructures at the budding yeast cell cortex. Mol. Biol. Cell 16: 372–384 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib340] Rodriguez J. R., Paterson B. M., 1990. Yeast myosin heavy chain mutant: maintenance of the cell type specific budding pattern and the normal deposition of chitin and cell wall components requires an intact myosin heavy chain gene. Cell Motil. Cytoskeleton 17: 301–308 [DOI] [PubMed] [Google Scholar]

[bib341] Rodriguez-Escudero I., Roelants F. M., Thorner J., Nombela C., Molina M., et al. , 2005. Reconstitution of the mammalian PI3K/PTEN/Akt pathway in yeast. Biochem. J. 390: 613–623 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib342] Roemer T., Madden K., Chang J., Snyder M., 1996. Selection of axial growth sites in yeast requires Axl2p, a novel plasma membrane glycoprotein. Genes Dev. 10: 777–793 [DOI] [PubMed] [Google Scholar]

[bib343] Rothman J. E., 1996. The protein machinery of vesicle budding and fusion. Protein Sci. 5: 185–194 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib344] Roumanie O., Weinachter C., Larrieu I., Crouzet M., Doignon F., 2001. Functional characterization of the Bag7, Lrg1 and Rgd2 RhoGAP proteins from Saccharomyces cerevisiae. FEBS Lett. 506: 149–156 [DOI] [PubMed] [Google Scholar]

[bib345] Ruggieri R., Bender A., Matsui Y., Powers S., Takai Y., et al. , 1992. RSR1, a ras-like gene homologous to Krev-1 (smg21A/rap1A): role in the development of cell polarity and interactions with the Ras pathway in Saccharomyces cerevisiae. Mol. Cell. Biol. 12: 758–766 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib346] Sagot I., Klee S. K., Pellman D., 2002a. Yeast formins regulate cell polarity by controlling the assembly of actin cables. Nat. Cell Biol. 4: 42–50 [DOI] [PubMed] [Google Scholar]

[bib347] Sagot I., Rodal A. A., Moseley J., Goode B. L., Pellman D., 2002b. An actin nucleation mechanism mediated by Bni1 and profilin. Nat. Cell Biol. 4: 626–631 [DOI] [PubMed] [Google Scholar]

[bib348] Sahin A., Daignan-Fornier B., Sagot I., 2008. Polarized growth in the absence of F-actin in Saccharomyces cerevisiae exiting quiescence. PLoS ONE 3: e2556. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib349] Saito H., 2010. Regulation of cross-talk in yeast MAPK signaling pathways. Curr. Opin. Microbiol. 13: 677–683 [DOI] [PubMed] [Google Scholar]

[bib350] Salminen A., Novick P. J., 1987. A Ras-like protein is required for a post-Golgi event in yeast secretion. Cell 49: 527–538 [DOI] [PubMed] [Google Scholar]

[bib351] Sanchez-Diaz A., Marchesi V., Murray S., Jones R., Pereira G., et al. , 2008. Inn1 couples contraction of the actomyosin ring to membrane ingression during cytokinesis in budding yeast. Nat. Cell Biol. 10: 395–406 [DOI] [PubMed] [Google Scholar]

[bib352] Sanders S. L., Field C. M., 1994. Cell division. Septins in common? Curr. Biol. 4: 907–910 [DOI] [PubMed] [Google Scholar]

[bib353] Sanders S. L., Herskowitz I., 1996. The Bud4 protein of yeast, required for axial budding, is localized to the mother/bud neck in a cell cycle-dependent manner. J. Cell Biol. 134: 413–427 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib354] Sanders S. L., Gentzsch M., Tanner W., Herskowitz I., 1999. O-glycosylation of Axl2/Bud10p by Pmt4p is required for its stability, localization, and function in daughter cells. J. Cell Biol. 145: 1177–1188 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib355] Sburlati A., Cabib E., 1986. Chitin synthetase 2, a presumptive participant in septum formation in Saccharomyces cerevisiae. J. Biol. Chem. 261: 15147–15152 [PubMed] [Google Scholar]

[bib356] Schenkman L. R., Caruso C., Pagé N., Pringle J. R., 2002. The role of cell cycle-regulated expression in the localization of spatial landmark proteins in yeast. J. Cell Biol. 156: 829–841 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib357] Schmelzle T., Helliwell S. B., Hall M. N., 2002. Yeast protein kinases and the Rho1 exchange factor Tus1 are novel components of the cell integrity pathway in yeast. Mol. Cell. Biol. 22: 1329–1339 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib358] Schmidt A., Bickle M., Beck T., Hall M. N., 1997. The yeast phosphatidylinositol kinase homolog TOR2 activates RHO1 and RHO2 via the exchange factor ROM2. Cell 88: 531–542 [DOI] [PubMed] [Google Scholar]

[bib359] Schmidt A., Schmelzle T., Hall M. N., 2002. The RHO1-GAPs SAC7, BEM2 and BAG7 control distinct RHO1 functions in Saccharomyces cerevisiae. Mol. Microbiol. 45: 1433–1441 [DOI] [PubMed] [Google Scholar]

[bib360] Schmidt M., Bowers B., Varma A., Roh D.-H., Cabib E., 2002. In budding yeast, contraction of the actomyosin ring and formation of the primary septum at cytokinesis depend on each other. J. Cell Sci. 115: 293–302 [DOI] [PubMed] [Google Scholar]

[bib472] Schmitz H. P., Huppert S., Lorberg A., Heinisch J. J., 2002. Rho5p downregulates the yeast cell integrity pathway. J. Cell Sci. 115: 3139–3148 [DOI] [PubMed] [Google Scholar]

[bib361] Schott D. H., Collins R. N., Bretscher A., 2002. Secretory vesicle transport velocity in living cells depends on the myosin-V lever arm length. J. Cell Biol. 156: 35–39 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib362] Schroeder T. E., 1968. Cytokinesis: filaments in the cleavage furrow. Exp. Cell Res. 53: 272–276 [DOI] [PubMed] [Google Scholar]

[bib363] Schroeder T. E., 1972. The contractile ring II: determining its brief existence, volumetric changes, and vital role in cleaving arbacia eggs. J. Cell Biol. 53: 419–434 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib364] Sekiguchi T., Hirose E., Nakashima N., Ii M., Nishimoto T., 2001. Novel G proteins, Rag C and Rag D, interact with GTP-binding proteins, Rag A and Rag B. J. Biol. Chem. 276: 7246–7257 [DOI] [PubMed] [Google Scholar]

[bib365] Shan S.-o., Stroud R. M., Walter P., 2004. Mechanism of association and reciprocal activation of two GTPases. PLoS Biol. 2: e320. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib366] Shannon K. B., Li R., 1999. The multiple roles of Cyk1p in the assembly and function of the actomyosin ring in budding yeast. Mol. Biol. Cell 10: 283–296 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib367] Shannon K. B., Li R., 2000. A myosin light chain mediates the localization of the budding yeast IQGAP-like protein during contractile ring formation. Curr. Biol. 10: 727–730 [DOI] [PubMed] [Google Scholar]

[bib368] Shaw J. A., Mol P. C., Bowers B., Silverman S. J., Valdivieso M. H., et al. , 1991. The function of chitin synthases 2 and 3 in the Saccharomyces cerevisiae cell cycle. J. Cell Biol. 114: 111–123 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib369] Sheu Y. J., Barral Y., Snyder M., 2000. Polarized growth controls cell shape and bipolar bud site selection in Saccharomyces cerevisiae. Mol. Cell. Biol. 20: 5235–5247 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib370] Sheu Y. J., Santos B., Fortin N., Costigan C., Snyder M., 1998. Spa2p interacts with cell polarity proteins and signaling components involved in yeast cell morphogenesis. Mol. Cell. Biol. 18: 4053–4069 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib371] Shimada Y., Gulli M. P., Peter M., 2000. Nuclear sequestration of the exchange factor Cdc24 by Far1 regulates cell polarity during yeast mating. Nat. Cell Biol. 2: 117–124 [DOI] [PubMed] [Google Scholar]

[bib372] Shimada Y., Wiget P., Gulli M. P., Bi E., Peter M., 2004. The nucleotide exchange factor Cdc24p may be regulated by auto-inhibition. EMBO J. 23: 1051–1062 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib373] Shinjo K., Koland J. G., Hart M. J., Narasimhan V., Johnson D. I., et al. , 1990. Molecular cloning of the gene for the human placental GTP-binding protein Gp (G25K): identification of this GTP-binding protein as the human homolog of the yeast cell-division-cycle protein CDC42. Proc. Natl. Acad. Sci. USA 87: 9853–9857 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib375] Sidorova J., Breeden L., 1993. Analysis of the SWI4/SWI6 protein complex, which directs G1/S-specific transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 13: 1069–1077 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib376] Singer J. M., Shaw J. M., 2003. Mdm20 protein functions with Nat3 protein to acetylate Tpm1 protein and regulate tropomyosin-actin interactions in budding yeast. Proc. Natl. Acad. Sci. USA 100: 7644–7649 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib473] Singh K., Kang P. J., Park H. O., 2008. The Rho5 GTPase is necessary for oxidant-induced cell death in budding yeast. Proc. Natl. Acad. Sci. USA 105: 1522–1527 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib377] Sivadon P., Bauer F., Aigle M., Crouzet M., 1995. Actin cytoskeleton and budding pattern are altered in the yeast rvs161 mutant: the Rvs161 protein shares common domains with the brain protein amphiphysin. Mol. Gen. Genet. 246: 485–495 [DOI] [PubMed] [Google Scholar]

[bib378] Slaughter B. D., Das A., Schwartz J. W., Rubinstein B., Li R., 2009. Dual modes of cdc42 recycling fine-tune polarized morphogenesis. Dev. Cell 17: 823–835 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib379] Sloat B. F., Pringle J. R., 1978. A mutant of yeast defective in cellular morphogenesis. Science 200: 1171–1173 [DOI] [PubMed] [Google Scholar]

[bib380] Sloat B. F., Adams A., Pringle J. R., 1981. Roles of the CDC24 gene product in cellular morphogenesis during the Saccharomyces cerevisiae cell cycle. J. Cell Biol. 89: 395–405 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib381] Smith G. R., Givan S. A., Cullen P., Sprague G. F., Jr, 2002. GTPase-activating proteins for Cdc42. Eukaryot. Cell 1: 469–480 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib382] Smith M. G., Swamy S. R., Pon L. A., 2001. The life cycle of actin patches in mating yeast. J. Cell Sci. 114: 1505–1513 [DOI] [PubMed] [Google Scholar]

[bib383] Snyder M., 1989. The SPA2 protein of yeast localizes to sites of cell growth. J. Cell Biol. 108: 1419–1429 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib384] Sopko R., Huang D., Smith J. C., Figeys D., Andrews B. J., 2007. Activation of the Cdc42p GTPase by cyclin-dependent protein kinases in budding yeast. EMBO J. 26: 4487–4500 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib386] Stevens R. C., Davis T. N., 1998. Mlc1p is a light chain for the unconventional myosin Myo2p in Saccharomyces cerevisiae. J. Cell Biol. 142: 711–722 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib387] Stevenson B. J., Ferguson B., De Virgilio C., Bi E., Pringle J. R., et al. , 1995. Mutation of RGA1, which encodes a putative GTPase-activating protein for the polarity-establishment protein Cdc42p, activates the pheromone-response pathway in the yeast Saccharomyces cerevisiae. Genes Dev. 9: 2949–2963 [DOI] [PubMed] [Google Scholar]

[bib388] Sullivan D. S., Huffaker T. C., 1992. Astral microtubules are not required for anaphase B in Saccharomyces cerevisiae. J. Cell Biol. 119: 379–388 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib389] Szkotnicki L., Crutchley J. M., Zyla T. R., Bardes E. S., Lew D. J., 2008. The checkpoint kinase Hsl1p is activated by Elm1p-dependent phosphorylation. Mol. Biol. Cell 19: 4675–4686 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib390] Taheri N., Köhler T., Braus G. H., Mösch H.-U., 2000. Asymmetrically localized Bud8p and Bud9p proteins control yeast cell polarity and development. EMBO J. 19: 6686–6696 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib391] Takahashi S., Pryciak P. M., 2007. Identification of novel membrane-binding domains in multiple yeast Cdc42 effectors. Mol. Biol. Cell 18: 4945–4956 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib392] Tanaka-Takiguchi Y., Kinoshita M., Takiguchi K., 2009. Septin-mediated uniform bracing of phospholipid membranes. Curr. Biol. 19: 140–145 [DOI] [PubMed] [Google Scholar]

[bib393] Tcheperegine S. E., Gao X. D., Bi E., 2005. Regulation of cell polarity by interactions of Msb3 and Msb4 with Cdc42 and polarisome components. Mol. Cell. Biol. 25: 8567–8580 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib394] Teh E. M., Chai C. C., Yeong F. M., 2009. Retention of Chs2p in the ER requires N-terminal CDK1-phosphorylation sites. Cell Cycle 8: 2964–2974 [PubMed] [Google Scholar]

[bib395] Tennyson C. N., Lee J., Andrews B., 1998. A role for the Pcl9-Pho85 cyclin-cdk complex at the M/G1 boundary in Saccharomyces cerevisiae. Mol. Microbiol. 28: 69–79 [DOI] [PubMed] [Google Scholar]

[bib396] TerBush D. R., Maurice T., Roth D., Novick P., 1996. The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J. 15: 6483–6494 [PMC free article] [PubMed] [Google Scholar]

[bib397] Thanabalu T., Munn A. L., 2001. Functions of Vrp1p in cytokinesis and actin patches are distinct and neither requires a WH2/V domain. EMBO J. 20: 6979–6989 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib398] Tiedje C., Sakwa I., Just U., Hofken T., 2008. The Rho GDI Rdi1 regulates Rho GTPases by distinct mechanisms. Mol. Biol. Cell 19: 2885–2896 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib399] Toenjes K. A., Sawyer M. M., Johnson D. I., 1999. The guanine-nucleotide-exchange factor Cdc24p is targeted to the nucleus and polarized growth sites. Curr. Biol. 9: 1183–1186 [DOI] [PubMed] [Google Scholar]

[bib400] Toenjes K. A., Simpson D., Johnson D. I., 2004. 2004 Separate membrane targeting and anchoring domains function in the localization of the S. cerevisiae Cdc24p guanine nucleotide exchange factor. Curr. Genet. 45: 257–264 [DOI] [PubMed] [Google Scholar]

[bib401] Tolliday N., VerPlank L., Li R., 2002. Rho1 directs formin-mediated actin ring assembly during budding yeast cytokinesis. Curr. Biol. 12: 1864–1870 [DOI] [PubMed] [Google Scholar]

[bib402] Tong Z., Gao X. D., Howell A. S., Bose I., Lew D. J., et al. , 2007. Adjacent positioning of cellular structures enabled by a Cdc42 GTPase-activating protein-mediated zone of inhibition. J. Cell Biol. 179: 1375–1384 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib403] Torres L., Martin H., Garcia-Saez M. I., Arroyo J., Molina M., et al. , 1991. A protein kinase gene complements the lytic phenotype of Saccharomyces cerevisiae lyt2 mutants. Mol. Microbiol. 5: 2845–2854 [DOI] [PubMed] [Google Scholar]

[bib404] Tully G. H., Nishihama R., Pringle J. R., Morgan D. O., 2009. The anaphase-promoting complex promotes actomyosin-ring disassembly during cytokinesis in yeast. Mol. Biol. Cell 20: 1201–1212 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib405] Uchida Y., Shimmi O., Sudoh M., Arisawa M., Yamada-Okabe H., 1996. Characterization of chitin synthase 2 of Saccharomyces cerevisiae. II: Both full size and processed enzymes are active for chitin synthesis. J. Biochem. 119: 659–666 [DOI] [PubMed] [Google Scholar]

[bib406] Vaduva G., Martin N. C., Hopper A. K., 1997. Actin-binding verprolin is a polarity development protein required for the morphogenesis and function of the yeast actin cytoskeleton. J. Cell Biol. 139: 1821–1833 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib407] Valdivia R. H., Schekman R., 2003. The yeasts Rho1p and Pkc1p regulate the transport of chitin synthase III (Chs3p) from internal stores to the plasma membrane. Proc. Natl. Acad. Sci. USA 100: 10287–10292 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib408] Valdivia R. H., Baggott D., Chuang J. S., Schekman R. W., 2002. The yeast clathrin adaptor protein complex 1 is required for the efficient retention of a subset of late Golgi membrane proteins. Dev. Cell 2: 283–294 [DOI] [PubMed] [Google Scholar]

[bib409] Vallen E. A., Caviston J., Bi E., 2000. Roles of Hof1p, Bni1p, Bnr1p, and Myo1p in cytokinesis in Saccharomyces cerevisiae. Mol. Biol. Cell 11: 593–611 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib410] Valtz N., Herskowitz I., 1996. Pea2 protein of yeast is localized to sites of polarized growth and is required for efficient mating and bipolar budding. J. Cell Biol. 135: 725–739 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib411] van Drogen F., Peter M., 2002. Spa2p functions as a scaffold-like protein to recruit the Mpk1p MAP kinase module to sites of polarized growth. Curr. Biol. 12: 1698–1703 [DOI] [PubMed] [Google Scholar]

[bib412] VerPlank L., Li R., 2005. Cell cycle-regulated trafficking of Chs2 controls actomyosin ring stability during cytokinesis. Mol. Biol. Cell 16: 2529–2543 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib413] Versele M., Thorner J., 2004. Septin collar formation in budding yeast requires GTP binding and direct phosphorylation by the PAK, Cla4. J. Cell Biol. 164: 701–715 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib474] Vrabioiu A. M., Gerber S. A., Gygi S. P., Field C. M., Mitchison T. J., 2004. The majority of the Saccharomyces cerevisiae septin complexes do not exchange guanine nucleotides. J. Biol. Chem. 279: 3111–3118 [DOI] [PubMed] [Google Scholar]

[bib414] Waddle J. A., Karpova T. S., Waterston R. H., Cooper J. A., 1996. Movement of cortical actin patches in yeast. J. Cell Biol. 132: 861–870 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib415] Wai S. C., Gerber S. A., Li R., 2009. Multisite phosphorylation of the guanine nucleotide exchange factor Cdc24 during yeast cell polarization. PLoS ONE 4: e6563. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib416] Walch-Solimena C., Collins R. N., Novick P. J., 1997. Sec2p mediates nucleotide exchange on Sec4p and is involved in polarized delivery of post-Golgi vesicles. J. Cell Biol. 137: 1495–1509 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib417] Waltermann C., Klipp E., 2010. Signal integration in budding yeast. Biochem. Soc. Trans. 38: 1257–1264 [DOI] [PubMed] [Google Scholar]

[bib418] Walworth N. C., Goud B., Kabcenell A. K., Novick P. J., 1989. Mutational analysis of SEC4 suggests a cyclical mechanism for the regulation of vesicular traffic. EMBO J. 8: 1685–1693 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib419] Watanabe D., Abe M., Ohya Y., 2001. Yeast Lrg1p acts as a specialized RhoGAP regulating 1,3-beta-glucan synthesis. Yeast 18: 943–951 [DOI] [PubMed] [Google Scholar]

[bib420] Watanabe Y., Takaesu G., Hagiwara M., Irie K., Matsumoto K., 1997. Characterization of a serum response factor-like protein in Saccharomyces cerevisiae, Rlm1, which has transcriptional activity regulated by the Mpk1 (Slt2) mitogen-activated protein kinase pathway. Mol. Cell. Biol. 17: 2615–2623 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib421] Watts F. Z., Shiels G., Orr E., 1987. The yeast MYO1 gene encoding a myosin-like protein required for cell division. EMBO J. 6: 3499–3505 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib422] Wedlich-Soldner R., Altschuler S., Wu L., Li R., 2003. Spontaneous cell polarization through actomyosin-based delivery of the Cdc42 GTPase. Science 299: 1231–1235 [DOI] [PubMed] [Google Scholar]

[bib423] Wedlich-Soldner R., Wai S. C., Schmidt T., Li R., 2004. Robust cell polarity is a dynamic state established by coupling transport and GTPase signaling. J. Cell Biol. 166: 889–900 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib424] Weibel P., Hiltbrunner A., Brand L., Kessler F., 2003. Dimerization of Toc-GTPases at the Chloroplast Protein Import Machinery. J. Biol. Chem. 278: 37321–37329 [DOI] [PubMed] [Google Scholar]

[bib425] Weirich C. S., Erzberger J. P., Barral Y., 2008. The septin family of GTPases: architecture and dynamics. Nat. Rev. Mol. Cell Biol. 9: 478–489 [DOI] [PubMed] [Google Scholar]

[bib426] Weiss E. L., Bishop A. C., Shokat K. M., Drubin D. G., 2000. Chemical genetic analysis of the budding-yeast p21-activated kinase Cla4p. Nat. Cell Biol. 2: 677–685 [DOI] [PubMed] [Google Scholar]

[bib427] Wendland B., Steece K. E., Emr S. D., 1999. Yeast epsins contain an essential N-terminal ENTH domain, bind clathrin and are required for endocytosis. EMBO J. 18: 4383–4393 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib428] Wiget P., Shimada Y., Butty A. C., Bi E., Peter M., 2004. Site-specific regulation of the GEF Cdc24p by the scaffold protein Far1p during yeast mating. EMBO J. 23: 1063–1074 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib429] Wild A. C., Yu J. W., Lemmon M. A., Blumer K. J., 2004. The p21-activated protein kinase-related kinase Cla4 is a coincidence detector of signaling by Cdc42 and phosphatidylinositol 4-phosphate. J. Biol. Chem. 279: 17101–17110 [DOI] [PubMed] [Google Scholar]

[bib430] Winder S. J., Jess T., Ayscough K. R., 2003. SCP1 encodes an actin-bundling protein in yeast. Biochem. J. 375: 287–295 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib431] Winter D., Podtelejnikov A. V., Mann M., Li R., 1997. The complex containing actin-related proteins Arp2 and Arp3 is required for the motility and integrity of yeast actin patches. Curr. Biol. 7: 519–529 [DOI] [PubMed] [Google Scholar]

[bib432] Winter D., Lechler T., Li R., 1999a. Activation of the yeast Arp2/3 complex by Bee1p, a WASP-family protein. Curr. Biol. 9: 501–504 [DOI] [PubMed] [Google Scholar]

[bib433] Winter D. C., Choe E. Y., Li R., 1999b. Genetic dissection of the budding yeast Arp2/3 complex: a comparison of the in vivo and structural roles of individual subunits. Proc. Natl. Acad. Sci. USA 96: 7288–7293 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib434] Witte H., Bradke F., 2008. The role of the cytoskeleton during neuronal polarization. Curr. Opin. Neurobiol. 18: 479–487 [DOI] [PubMed] [Google Scholar]

[bib435] Wloka C., Nishihama R., Onishi M., Oh Y., Hanna J., et al. , 2011. Evidence that septin diffusion barriers are dispensable for cytokiensis in budding yeast. Biol. Chem. 392: 813–829 [DOI] [PubMed] [Google Scholar]

[bib436] Woods A., Johnstone S. R., Dickerson K., Leiper F. C., Fryer L. G., et al. , 2003. LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr. Biol. 13: 2004–2008 [DOI] [PubMed] [Google Scholar]

[bib437] Wu H., Brennwald P., 2010. The function of two Rho family GTPases is determined by distinct patterns of cell surface localization. Mol. Cell. Biol. 30: 5207–5217 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib438] Wu H., Turner C., Gardner J., Temple B., Brennwald P., 2010. The Exo70 subunit of the exocyst is an effector for both Cdc42 and Rho3 function in polarized exocytosis. Mol. Biol. Cell 21: 430–442 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib439] Yamamoto T., Mochida J., Kadota J., Takeda M., Bi E., et al. , 2010. Initial polarized bud growth by endocytic recycling in the absence of actin cable-dependent vesicle transport in yeast. Mol. Biol. Cell 21: 1237–1252 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib440] Yamashita M., Kurokawa K., Sato Y., Yamagata A., Mimura H., et al. , 2010. Structural basis for the Rho- and phosphoinositide-dependent localization of the exocyst subunit Sec3. Nat. Struct. Mol. Biol. 17: 180–186 [DOI] [PubMed] [Google Scholar]

[bib441] Yamochi W., Tanaka K., Nonaka H., Maeda A., Musha T., et al. , 1994. Growth site localization of Rho1 small GTP-binding protein and its involvement in bud formation in Saccharomyces cerevisiae. J. Cell Biol. 125: 1077–1093 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib442] Yang H. C., Pon L. A., 2002. Actin cable dynamics in budding yeast. Proc. Natl. Acad. Sci. USA 99: 751–756 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib443] Yang S., Ayscough K. R., Drubin D. G., 1997. A role for the actin cytoskeleton of Saccharomyces cerevisiae in bipolar bud-site selection. J. Cell Biol. 136: 111–123 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib444] Yoshida S., Kono K., Lowery D. M., Bartolini S., Yaffe M. B., et al. , 2006. Polo-like kinase Cdc5 controls the local activation of Rho1 to promote cytokinesis. Science 313: 108–111 [DOI] [PubMed] [Google Scholar]

[bib445] Yoshida S., Bartolini S., Pellman D., 2009. Mechanisms for concentrating Rho1 during cytokinesis. Genes Dev. 23: 810–823 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib446] Young M. E., Cooper J. A., Bridgman P. C., 2004. Yeast actin patches are networks of branched actin filaments. J. Cell Biol. 166: 629–635 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib447] Zahner J. E., Harkins H. A., Pringle J. R., 1996. Genetic analysis of the bipolar pattern of bud-site selection in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 16: 1857–1870 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib448] Zajac A., Sun X., Zhang J., Guo W., 2005. Cyclical regulation of the exocyst and cell polarity determinants for polarized cell growth. Mol. Biol. Cell 16: 1500–1512 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib449] Zhang G., Kashimshetty R., Ng K. E., Tan H. B., Yeong F. M., 2006. Exit from mitosis triggers Chs2p transport from the endoplasmic reticulum to mother-daughter neck via the secretory pathway in budding yeast. J. Cell Biol. 174: 207–220 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib450] Zhang J., Kong C., Xie H., McPherson P. S., Grinstein S., et al. , 1999. Phosphatidylinositol polyphosphate binding to the mammalian septin H5 is modulated by GTP. Curr. Biol. 9: 1458–1467 [DOI] [PubMed] [Google Scholar]

[bib451] Zhang X., Bi E., Novick P., Du L., Kozminski K. G., et al. , 2001. Cdc42 interacts with the exocyst and regulates polarized secretion. J. Biol. Chem. 276: 46745–46750 [DOI] [PubMed] [Google Scholar]

[bib452] Zhang X., Orlando K., He B., Xi F., Zhang J., et al. , 2008. Membrane association and functional regulation of Sec3 by phospholipids and Cdc42. J. Cell Biol. 180: 145–158 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib453] Zheng Y., Hart M. J., Shinjo K., Evans T., Bender A., et al. , 1993. Biochemical comparisons of the Saccharomyces cerevisiae Bem2 and Bem3 proteins. Delineation of a limit Cdc42 GTPase-activating protein domain. J. Biol. Chem. 268: 24629–24634 [PubMed] [Google Scholar]

[bib454] Zheng Y., Cerione R., Bender A., 1994. Control of the yeast bud-site assembly GTPase Cdc42. Catalysis of guanine nucleotide exchange by Cdc24 and stimulation of GTPase activity by Bem3. J. Biol. Chem. 269: 2369–2372 [PubMed] [Google Scholar]

[bib455] Zheng Y., Bender A., Cerione R. A., 1995. Interactions among proteins involved in bud-site selection and bud-site assembly in Saccharomyces cerevisiae. J. Biol. Chem. 270: 626–630 [DOI] [PubMed] [Google Scholar]

[bib456] Zigmond S. H., Evangelista M., Boone C., Yang C., Dar A. C., et al. , 2003. Formin leaky cap allows elongation in the presence of tight capping proteins. Curr. Biol. 13: 1820–1823 [DOI] [PubMed] [Google Scholar]

[bib457] Ziman M., O’Brien J. M., Ouellette L. A., Church W. R., Johnson D. I., 1991. Mutational analysis of CDC42Sc, a Saccharomyces cerevisiae gene that encodes a putative GTP-binding protein involved in the control of cell polarity. Mol. Cell. Biol. 11: 3537–3544 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib458] Ziman M., Preuss D., Mulholland J., O’Brien J. M., Botstein D., et al. , 1993. Subcellular localization of Cdc42p, a Saccharomyces cerevisiae GTP-binding protein involved in the control of cell polarity. Mol. Biol. Cell 4: 1307–1316 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib459] Ziman M., Chuang J. S., Schekman R. W., 1996. Chs1p and Chs3p, two proteins involved in chitin synthesis, populate a compartment of the Saccharomyces cerevisiae endocytic pathway. Mol. Biol. Cell 7: 1909–1919 [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib460] Ziman M., Chuang J. S., Tsung M., Hamamoto S., Schekman R., 1998. Chs6p-dependent anterograde transport of Chs3p from the chitosome to the plasma membrane in Saccharomyces cerevisiae. Mol. Biol. Cell 9: 1565–1576 [DOI] [PMC free article] [PubMed] [Google Scholar]

PERMALINK

Cell Polarization and Cytokinesis in Budding Yeast

Erfei Bi

Hay-Oak Park

Abstract

Establishment and maintenance of polarized cell growth

Polarization of growth and the cytoskeleton during the cell cycle

Figure 1.

Cdc42: the center of cell polarization

Table 1. Proteins involved in polarized cell growth.

Cdc42 GTPase module:

Figure 2.

Singularity in budding and Cdc42 polarization

Figure 3.

Key questions in Cdc42 polarization:

Cdc42-controlled actin and septin organization

Actin organization, dynamics, and functions:

Actin cables and exocytosis:

Figure 4.

Role of Cdc42 in actin cable-mediated exocytosis: the “polarisome” platform:

Role of Cdc42 in actin cable-independent exocytosis:

Actin patches and endocytosis:

Role of Cdc42 in actin patch polarization:

Septin organization and dynamics:

Plasticity in septin complex and filament assembly:

Septin dynamics and regulation during the cell cycle:

Role of Cdc42 in polarized septin ring assembly:

An integrated model for Cdc42-controlled actin cable and septin ring assembly:

Key questions in Cdc42-controlled actin and septin organization:

Rho1 in polarized growth

Rho1 GTPase module:

Figure 5.

Rho1 in cell wall remodeling:

Rho1 in actin organization:

Rho1 in exocytosis:

Key questions on the roles of Rho1 in cell polarization:

Mechanism of Cytokinesis

Figure 6.

Table 2. Proteins involved in cytokinesis.

Actomyosin ring assembly and disassembly

AMR assembly:

A model and key questions on AMR assembly:

AMR disassembly:

Targeted membrane deposition and primary septum formation

Polarized exocytosis and membrane addition at the division site:

Figure 7.

Regulation of Chs2 and primary septum formation:

Coordination of the actomyosin ring and primary septum formation

Figure 8.

Key questions on cytokinesis

Spatial Control of Polarized Cell Growth and Division

Patterns of bud-site selection

Figure 9.

Figure 10.

Table 3. Proteins involved in bud-site selection.

The Rsr1 GTPase module: the center of spatial regulation

The Rsr1 GTPase module:

Localization of Rsr1, Bud2, and Bud5:

Polarization of the Rsr1 GTPase module:

Selection of a bud site in the axial pattern

Molecular nature of the axial-budding–specific proteins:

Localization of Bud3, Bud4, Axl1, and Axl2:

Choosing a nonoverlapping bud site:

Selection of a bud site in the bipolar pattern

Molecular nature of the bipolar-budding–specific proteins:

Localization of Bud8, Bud9, Rax1, and Rax2:

Other players in bipolar budding:

Mechanisms of the cell-type–specific budding patterns

Coupling of spatial landmarks to the Rsr1 GTPase module:

Regulation by cell type:

Directing polarity establishment by coupling of the Rsr1 and Cdc42 GTPase modules

Figure 11.

Acknowledgments

Footnotes

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