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. 1996 Apr;16(4):1376–1390. doi: 10.1128/mcb.16.4.1376

The LIM domain-containing Dbm1 GTPase-activating protein is required for normal cellular morphogenesis in Saccharomyces cerevisiae.

G C Chen 1, L Zheng 1, C S Chan 1
PMCID: PMC231122  PMID: 8657111

Abstract

Normal cell growth in the yeast Saccharomyces cerevisiae involves the selection of genetically determined bud sites where most growth is localized. Previous studies have shown that BEM2, which encodes a GTPase-activating protein (GAP) that is specific for the Rho-type GTPase Rho1p in vitro, is required for proper bud site selection and bud emergence. We show here that DBM1, which encodes another putative Rho-type GAP with two tandemly arranged cysteine-rich LIM domains, also is needed for proper bud site selection, as haploid cells lacking Dbm1p bud predominantly in a bipolar, rather than the normal axial, manner. Furthermore, yeast cells lacking both Bem2p and Dbm1p are inviable. The nonaxial budding defect of dbm1 mutants can be rescued partially by overproduction of Bem3p and is exacerbated by its absence. Since Bem3p has previously been shown to function as a GAP for Cdc42p, and also less efficiently for Rho1p, our results suggest that Dbm1p, like Bem2p and Bem3p, may function in vivo as a GAP for Cdc42p and/or Rho1p. Both LIM domains of Dbm1p are essential for its normal function. Point mutations that alter single conserved cysteine residues within either LIM domain result in mutant forms of Dbm1p that can no longer function in bud site selection but instead are capable of rescuing the inviability of bem2 mutants at 35 degrees C.

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Selected References

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  1. Adames N., Blundell K., Ashby M. N., Boone C. Role of yeast insulin-degrading enzyme homologs in propheromone processing and bud site selection. Science. 1995 Oct 20;270(5235):464–467. doi: 10.1126/science.270.5235.464. [DOI] [PubMed] [Google Scholar]
  2. Adams A. E., Johnson D. I., Longnecker R. M., Sloat B. F., Pringle J. R. CDC42 and CDC43, two additional genes involved in budding and the establishment of cell polarity in the yeast Saccharomyces cerevisiae. J Cell Biol. 1990 Jul;111(1):131–142. doi: 10.1083/jcb.111.1.131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Adams A. E., Pringle J. R. Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutant Saccharomyces cerevisiae. J Cell Biol. 1984 Mar;98(3):934–945. doi: 10.1083/jcb.98.3.934. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Archer V. E., Breton J., Sanchez-Garcia I., Osada H., Forster A., Thomson A. J., Rabbitts T. H. Cysteine-rich LIM domains of LIM-homeodomain and LIM-only proteins contain zinc but not iron. Proc Natl Acad Sci U S A. 1994 Jan 4;91(1):316–320. doi: 10.1073/pnas.91.1.316. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bender A. 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 U S A. 1993 Nov 1;90(21):9926–9929. doi: 10.1073/pnas.90.21.9926. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bender A., Pringle J. R. 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 U S A. 1989 Dec;86(24):9976–9980. doi: 10.1073/pnas.86.24.9976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bender A., Pringle J. R. 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. 1991 Mar;11(3):1295–1305. doi: 10.1128/mcb.11.3.1295. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Benton B. K., Tinkelenberg A. H., Jean D., Plump S. D., Cross F. R. Genetic analysis of Cln/Cdc28 regulation of cell morphogenesis in budding yeast. EMBO J. 1993 Dec 15;12(13):5267–5275. doi: 10.1002/j.1460-2075.1993.tb06222.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bretscher A., Drees B., Harsay E., Schott D., Wang T. What are the basic functions of microfilaments? Insights from studies in budding yeast. J Cell Biol. 1994 Aug;126(4):821–825. doi: 10.1083/jcb.126.4.821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Brewster J. L., Gustin M. C. Positioning of cell growth and division after osmotic stress requires a MAP kinase pathway. Yeast. 1994 Apr;10(4):425–439. doi: 10.1002/yea.320100402. [DOI] [PubMed] [Google Scholar]
  11. Chan C. S., Botstein D. Isolation and characterization of chromosome-gain and increase-in-ploidy mutants in yeast. Genetics. 1993 Nov;135(3):677–691. doi: 10.1093/genetics/135.3.677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chant J. Cell polarity in yeast. Trends Genet. 1994 Sep;10(9):328–333. doi: 10.1016/0168-9525(94)90036-1. [DOI] [PubMed] [Google Scholar]
  13. Chant J., Corrado K., Pringle J. R., Herskowitz I. Yeast BUD5, encoding a putative GDP-GTP exchange factor, is necessary for bud site selection and interacts with bud formation gene BEM1. Cell. 1991 Jun 28;65(7):1213–1224. doi: 10.1016/0092-8674(91)90016-r. [DOI] [PubMed] [Google Scholar]
  14. Chant J., Herskowitz I. Genetic control of bud site selection in yeast by a set of gene products that constitute a morphogenetic pathway. Cell. 1991 Jun 28;65(7):1203–1212. doi: 10.1016/0092-8674(91)90015-q. [DOI] [PubMed] [Google Scholar]
  15. Chant J., Mischke M., Mitchell E., Herskowitz I., Pringle J. R. Role of Bud3p in producing the axial budding pattern of yeast. J Cell Biol. 1995 May;129(3):767–778. doi: 10.1083/jcb.129.3.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Chant J., Pringle J. R. Patterns of bud-site selection in the yeast Saccharomyces cerevisiae. J Cell Biol. 1995 May;129(3):751–765. doi: 10.1083/jcb.129.3.751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Chenevert J., Corrado K., Bender A., Pringle J., Herskowitz I. A yeast gene (BEM1) necessary for cell polarization whose product contains two SH3 domains. Nature. 1992 Mar 5;356(6364):77–79. doi: 10.1038/356077a0. [DOI] [PubMed] [Google Scholar]
  18. Diekmann D., Brill S., Garrett M. D., Totty N., Hsuan J., Monfries C., Hall C., Lim L., Hall A. Bcr encodes a GTPase-activating protein for p21rac. Nature. 1991 May 30;351(6325):400–402. doi: 10.1038/351400a0. [DOI] [PubMed] [Google Scholar]
  19. Doignon F., Biteau N., Crouzet M., Aigle M. The complete sequence of a 19,482 bp segment located on the right arm of chromosome II from Saccharomyces cerevisiae. Yeast. 1993 Feb;9(2):189–199. doi: 10.1002/yea.320090210. [DOI] [PubMed] [Google Scholar]
  20. FREIFELDER D. Bud position in Saccharomyces cerevisiae. J Bacteriol. 1960 Oct;80:567–568. doi: 10.1128/jb.80.4.567-568.1960. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Feuerstein R., Wang X., Song D., Cooke N. E., Liebhaber S. A. The LIM/double zinc-finger motif functions as a protein dimerization domain. Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10655–10659. doi: 10.1073/pnas.91.22.10655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Flescher E. G., Madden K., Snyder M. Components required for cytokinesis are important for bud site selection in yeast. J Cell Biol. 1993 Jul;122(2):373–386. doi: 10.1083/jcb.122.2.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ford S. K., Pringle J. R. Cellular morphogenesis in the Saccharomyces cerevisiae cell cycle: localization of the CDC11 gene product and the timing of events at the budding site. Dev Genet. 1991;12(4):281–292. doi: 10.1002/dvg.1020120405. [DOI] [PubMed] [Google Scholar]
  24. Fujita A., Oka C., Arikawa Y., Katagai T., Tonouchi A., Kuhara S., Misumi Y. A yeast gene necessary for bud-site selection encodes a protein similar to insulin-degrading enzymes. Nature. 1994 Dec 8;372(6506):567–570. doi: 10.1038/372567a0. [DOI] [PubMed] [Google Scholar]
  25. Gimeno C. J., Ljungdahl P. O., Styles C. A., Fink G. R. Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell. 1992 Mar 20;68(6):1077–1090. doi: 10.1016/0092-8674(92)90079-r. [DOI] [PubMed] [Google Scholar]
  26. Haarer B. K., Pringle J. R. 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. 1987 Oct;7(10):3678–3687. doi: 10.1128/mcb.7.10.3678. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hall A. Small GTP-binding proteins and the regulation of the actin cytoskeleton. Annu Rev Cell Biol. 1994;10:31–54. doi: 10.1146/annurev.cb.10.110194.000335. [DOI] [PubMed] [Google Scholar]
  28. Hempe J. M., Cousins R. J. Cysteine-rich intestinal protein binds zinc during transmucosal zinc transport. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9671–9674. doi: 10.1073/pnas.88.21.9671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Johnson D. I., Pringle J. R. Molecular characterization of CDC42, a Saccharomyces cerevisiae gene involved in the development of cell polarity. J Cell Biol. 1990 Jul;111(1):143–152. doi: 10.1083/jcb.111.1.143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Jones J. S., Prakash L. Yeast Saccharomyces cerevisiae selectable markers in pUC18 polylinkers. Yeast. 1990 Sep-Oct;6(5):363–366. doi: 10.1002/yea.320060502. [DOI] [PubMed] [Google Scholar]
  31. Kim H. B., Haarer B. K., Pringle J. R. Cellular morphogenesis in the Saccharomyces cerevisiae cell cycle: localization of the CDC3 gene product and the timing of events at the budding site. J Cell Biol. 1991 Feb;112(4):535–544. doi: 10.1083/jcb.112.4.535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kim Y. J., Francisco L., Chen G. C., Marcotte E., Chan C. S. Control of cellular morphogenesis by the Ip12/Bem2 GTPase-activating protein: possible role of protein phosphorylation. J Cell Biol. 1994 Dec;127(5):1381–1394. doi: 10.1083/jcb.127.5.1381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Koerner T. J., Hill J. E., Myers A. M., Tzagoloff A. High-expression vectors with multiple cloning sites for construction of trpE fusion genes: pATH vectors. Methods Enzymol. 1991;194:477–490. doi: 10.1016/0076-6879(91)94036-c. [DOI] [PubMed] [Google Scholar]
  34. Kosa J. L., Michelsen J. W., Louis H. A., Olsen J. I., Davis D. R., Beckerle M. C., Winge D. R. Common metal ion coordination in LIM domain proteins. Biochemistry. 1994 Jan 18;33(2):468–477. doi: 10.1021/bi00168a011. [DOI] [PubMed] [Google Scholar]
  35. Kunkel T. A., Roberts J. D., Zakour R. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 1987;154:367–382. doi: 10.1016/0076-6879(87)54085-x. [DOI] [PubMed] [Google Scholar]
  36. Lamarche N., Hall A. GAPs for rho-related GTPases. Trends Genet. 1994 Dec;10(12):436–440. doi: 10.1016/0168-9525(94)90114-7. [DOI] [PubMed] [Google Scholar]
  37. Li P. M., Reichert J., Freyd G., Horvitz H. R., Walsh C. T. The LIM region of a presumptive Caenorhabditis elegans transcription factor is an iron-sulfur- and zinc-containing metallodomain. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9210–9213. doi: 10.1073/pnas.88.20.9210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Li R., Zheng Y., Drubin D. G. Regulation of cortical actin cytoskeleton assembly during polarized cell growth in budding yeast. J Cell Biol. 1995 Feb;128(4):599–615. doi: 10.1083/jcb.128.4.599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Madaule P., Axel R., Myers A. M. Characterization of two members of the rho gene family from the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1987 Feb;84(3):779–783. doi: 10.1073/pnas.84.3.779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Madden K., Costigan C., Snyder M. Cell polarity and morphogenesis in Saccharomyces cerevisiae. Trends Cell Biol. 1992 Jan;2(1):22–29. doi: 10.1016/0962-8924(92)90140-i. [DOI] [PubMed] [Google Scholar]
  41. Madden K., Snyder M. Specification of sites for polarized growth in Saccharomyces cerevisiae and the influence of external factors on site selection. Mol Biol Cell. 1992 Sep;3(9):1025–1035. doi: 10.1091/mbc.3.9.1025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Matsui Y., Toh-E A. 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. 1992 Dec;12(12):5690–5699. doi: 10.1128/mcb.12.12.5690. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Michelsen J. W., Schmeichel K. L., Beckerle M. C., Winge D. R. The LIM motif defines a specific zinc-binding protein domain. Proc Natl Acad Sci U S A. 1993 May 15;90(10):4404–4408. doi: 10.1073/pnas.90.10.4404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Michelsen J. W., Sewell A. K., Louis H. A., Olsen J. I., Davis D. R., Winge D. R., Beckerle M. C. Mutational analysis of the metal sites in an LIM domain. J Biol Chem. 1994 Apr 15;269(15):11108–11113. [PubMed] [Google Scholar]
  45. Molero G., Yuste-Rojas M., Montesi A., Vázquez A., Nombela C., Sanchez M. A cdc-like autolytic Saccharomyces cerevisiae mutant altered in budding site selection is complemented by SPO12, a sporulation gene. J Bacteriol. 1993 Oct;175(20):6562–6570. doi: 10.1128/jb.175.20.6562-6570.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Mulholland J., Preuss D., Moon A., Wong A., Drubin D., Botstein D. Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane. J Cell Biol. 1994 Apr;125(2):381–391. doi: 10.1083/jcb.125.2.381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Müller L., Xu G., Wells R., Hollenberg C. P., Piepersberg W. LRG1 is expressed during sporulation in Saccharomyces cerevisiae and contains motifs similar to LIM and rho/racGAP domains. Nucleic Acids Res. 1994 Aug 11;22(15):3151–3154. doi: 10.1093/nar/22.15.3151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Nakajima H., Hirata A., Ogawa Y., Yonehara T., Yoda K., Yamasaki M. A cytoskeleton-related gene, uso1, is required for intracellular protein transport in Saccharomyces cerevisiae. J Cell Biol. 1991 Apr;113(2):245–260. doi: 10.1083/jcb.113.2.245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Ohya Y., Miyamoto S., Ohsumi Y., Anraku Y. Calcium-sensitive cls4 mutant of Saccharomyces cerevisiae with a defect in bud formation. J Bacteriol. 1986 Jan;165(1):28–33. doi: 10.1128/jb.165.1.28-33.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Ohya Y., Ohsumi Y., Anraku Y. Genetic study of the role of calcium ions in the cell division cycle of Saccharomyces cerevisiae: a calcium-dependent mutant and its trifluoperazine-dependent pseudorevertants. Mol Gen Genet. 1984;193(3):389–394. doi: 10.1007/BF00382073. [DOI] [PubMed] [Google Scholar]
  51. Ohya Y., Qadota H., Anraku Y., Pringle J. R., Botstein D. Suppression of yeast geranylgeranyl transferase I defect by alternative prenylation of two target GTPases, Rho1p and Cdc42p. Mol Biol Cell. 1993 Oct;4(10):1017–1025. doi: 10.1091/mbc.4.10.1017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Park H. O., Chant J., Herskowitz I. BUD2 encodes a GTPase-activating protein for Bud1/Rsr1 necessary for proper bud-site selection in yeast. Nature. 1993 Sep 16;365(6443):269–274. doi: 10.1038/365269a0. [DOI] [PubMed] [Google Scholar]
  53. Peterson J., Zheng Y., Bender L., Myers A., Cerione R., Bender A. Interactions between the bud emergence proteins Bem1p and Bem2p and Rho-type GTPases in yeast. J Cell Biol. 1994 Dec;127(5):1395–1406. doi: 10.1083/jcb.127.5.1395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Powers S., Gonzales E., Christensen T., Cubert J., Broek D. Functional cloning of BUD5, a CDC25-related gene from S. cerevisiae that can suppress a dominant-negative RAS2 mutant. Cell. 1991 Jun 28;65(7):1225–1231. doi: 10.1016/0092-8674(91)90017-s. [DOI] [PubMed] [Google Scholar]
  55. Pringle J. R., Preston R. A., Adams A. E., Stearns T., Drubin D. G., Haarer B. K., Jones E. W. Fluorescence microscopy methods for yeast. Methods Cell Biol. 1989;31:357–435. doi: 10.1016/s0091-679x(08)61620-9. [DOI] [PubMed] [Google Scholar]
  56. Ramer S. W., Elledge S. J., Davis R. W. Dominant genetics using a yeast genomic library under the control of a strong inducible promoter. Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11589–11593. doi: 10.1073/pnas.89.23.11589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Ridley A. J., Self A. J., Kasmi F., Paterson H. F., Hall A., Marshall C. J., Ellis C. rho family GTPase activating proteins p190, bcr and rhoGAP show distinct specificities in vitro and in vivo. EMBO J. 1993 Dec 15;12(13):5151–5160. doi: 10.1002/j.1460-2075.1993.tb06210.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Rine J., Herskowitz I. Four genes responsible for a position effect on expression from HML and HMR in Saccharomyces cerevisiae. Genetics. 1987 May;116(1):9–22. doi: 10.1093/genetics/116.1.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Roberts R. L., Fink G. R. Elements of a single MAP kinase cascade in Saccharomyces cerevisiae mediate two developmental programs in the same cell type: mating and invasive growth. Genes Dev. 1994 Dec 15;8(24):2974–2985. doi: 10.1101/gad.8.24.2974. [DOI] [PubMed] [Google Scholar]
  60. Rose M. D., Novick P., Thomas J. H., Botstein D., Fink G. R. A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene. 1987;60(2-3):237–243. doi: 10.1016/0378-1119(87)90232-0. [DOI] [PubMed] [Google Scholar]
  61. Rothstein R. J. One-step gene disruption in yeast. Methods Enzymol. 1983;101:202–211. doi: 10.1016/0076-6879(83)01015-0. [DOI] [PubMed] [Google Scholar]
  62. Sadler I., Crawford A. W., Michelsen J. W., Beckerle M. C. Zyxin and cCRP: two interactive LIM domain proteins associated with the cytoskeleton. J Cell Biol. 1992 Dec;119(6):1573–1587. doi: 10.1083/jcb.119.6.1573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Schmeichel K. L., Beckerle M. C. The LIM domain is a modular protein-binding interface. Cell. 1994 Oct 21;79(2):211–219. doi: 10.1016/0092-8674(94)90191-0. [DOI] [PubMed] [Google Scholar]
  64. Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Sloat B. F., Adams A., Pringle J. R. Roles of the CDC24 gene product in cellular morphogenesis during the Saccharomyces cerevisiae cell cycle. J Cell Biol. 1981 Jun;89(3):395–405. doi: 10.1083/jcb.89.3.395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Sloat B. F., Pringle J. R. A mutant of yeast defective in cellular morphogenesis. Science. 1978 Jun 9;200(4346):1171–1173. doi: 10.1126/science.349694. [DOI] [PubMed] [Google Scholar]
  67. Snyder M., Gehrung S., Page B. D. Studies concerning the temporal and genetic control of cell polarity in Saccharomyces cerevisiae. J Cell Biol. 1991 Aug;114(3):515–532. doi: 10.1083/jcb.114.3.515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Snyder M. The SPA2 protein of yeast localizes to sites of cell growth. J Cell Biol. 1989 Apr;108(4):1419–1429. doi: 10.1083/jcb.108.4.1419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Stevenson B. J., Ferguson B., De Virgilio C., Bi E., Pringle J. R., Ammerer G., Sprague G. F., Jr 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. 1995 Dec 1;9(23):2949–2963. doi: 10.1101/gad.9.23.2949. [DOI] [PubMed] [Google Scholar]
  70. Sánchez-García I., Osada H., Forster A., Rabbitts T. H. The cysteine-rich LIM domains inhibit DNA binding by the associated homeodomain in Isl-1. EMBO J. 1993 Nov;12(11):4243–4250. doi: 10.1002/j.1460-2075.1993.tb06108.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Sánchez-García I., Rabbitts T. H. The LIM domain: a new structural motif found in zinc-finger-like proteins. Trends Genet. 1994 Sep;10(9):315–320. doi: 10.1016/0168-9525(94)90034-5. [DOI] [PubMed] [Google Scholar]
  72. Takai Y., Sasaki T., Tanaka K., Nakanishi H. Rho as a regulator of the cytoskeleton. Trends Biochem Sci. 1995 Jun;20(6):227–231. doi: 10.1016/s0968-0004(00)89022-2. [DOI] [PubMed] [Google Scholar]
  73. Trueblood C. E., Ohya Y., Rine J. Genetic evidence for in vivo cross-specificity of the CaaX-box protein prenyltransferases farnesyltransferase and geranylgeranyltransferase-I in Saccharomyces cerevisiae. Mol Cell Biol. 1993 Jul;13(7):4260–4275. doi: 10.1128/mcb.13.7.4260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Wang T., Bretscher A. The rho-GAP encoded by BEM2 regulates cytoskeletal structure in budding yeast. Mol Biol Cell. 1995 Aug;6(8):1011–1024. doi: 10.1091/mbc.6.8.1011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Welch M. D., Holtzman D. A., Drubin D. G. The yeast actin cytoskeleton. Curr Opin Cell Biol. 1994 Feb;6(1):110–119. doi: 10.1016/0955-0674(94)90124-4. [DOI] [PubMed] [Google Scholar]
  76. Winey M., Hoyt M. A., Chan C., Goetsch L., Botstein D., Byers B. NDC1: a nuclear periphery component required for yeast spindle pole body duplication. J Cell Biol. 1993 Aug;122(4):743–751. doi: 10.1083/jcb.122.4.743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Xue D., Tu Y., Chalfie M. Cooperative interactions between the Caenorhabditis elegans homeoproteins UNC-86 and MEC-3. Science. 1993 Sep 3;261(5126):1324–1328. doi: 10.1126/science.8103239. [DOI] [PubMed] [Google Scholar]
  78. Yamochi W., Tanaka K., Nonaka H., Maeda A., Musha T., Takai Y. Growth site localization of Rho1 small GTP-binding protein and its involvement in bud formation in Saccharomyces cerevisiae. J Cell Biol. 1994 Jun;125(5):1077–1093. doi: 10.1083/jcb.125.5.1077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Zheng Y., Bender A., Cerione R. A. Interactions among proteins involved in bud-site selection and bud-site assembly in Saccharomyces cerevisiae. J Biol Chem. 1995 Jan 13;270(2):626–630. doi: 10.1074/jbc.270.2.626. [DOI] [PubMed] [Google Scholar]
  80. Zheng Y., Cerione R., Bender A. 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. 1994 Jan 28;269(4):2369–2372. [PubMed] [Google Scholar]
  81. Zheng Y., Hart M. J., Shinjo K., Evans T., Bender A., Cerione R. A. Biochemical comparisons of the Saccharomyces cerevisiae Bem2 and Bem3 proteins. Delineation of a limit Cdc42 GTPase-activating protein domain. J Biol Chem. 1993 Nov 25;268(33):24629–24634. [PubMed] [Google Scholar]
  82. Ziman M., Johnson D. I. Genetic evidence for a functional interaction between Saccharomyces cerevisiae CDC24 and CDC42. Yeast. 1994 Apr;10(4):463–474. doi: 10.1002/yea.320100405. [DOI] [PubMed] [Google Scholar]
  83. Ziman M., O'Brien J. M., Ouellette L. A., Church W. R., Johnson D. I. 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. 1991 Jul;11(7):3537–3544. doi: 10.1128/mcb.11.7.3537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Ziman M., Preuss D., Mulholland J., O'Brien J. M., Botstein D., Johnson D. I. Subcellular localization of Cdc42p, a Saccharomyces cerevisiae GTP-binding protein involved in the control of cell polarity. Mol Biol Cell. 1993 Dec;4(12):1307–1316. doi: 10.1091/mbc.4.12.1307. [DOI] [PMC free article] [PubMed] [Google Scholar]

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