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. 2003 Apr 15;371(Pt 2):233–241. doi: 10.1042/BJ20030139

Regulation of endocytic traffic by Rho GTPases.

Britta Qualmann 1, Harry Mellor 1
PMCID: PMC1223314  PMID: 12564953

Abstract

The members of the Rho subfamily of small GTPases are key regulators of the actin cytoskeleton. However, recent studies have provided evidence for multiple additional roles for these signalling proteins in controlling endocytic traffic. Here we review our current understanding of Rho GTPase action within the endocytic pathway and examine the potential points of convergence with the more established, actin-based functions of these signalling proteins.

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Selected References

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  1. Adamson P., Paterson H. F., Hall A. Intracellular localization of the P21rho proteins. J Cell Biol. 1992 Nov;119(3):617–627. doi: 10.1083/jcb.119.3.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Albert M. L., Kim J. I., Birge R. B. alphavbeta5 integrin recruits the CrkII-Dock180-rac1 complex for phagocytosis of apoptotic cells. Nat Cell Biol. 2000 Dec;2(12):899–905. doi: 10.1038/35046549. [DOI] [PubMed] [Google Scholar]
  3. Allen L. A., Aderem A. Molecular definition of distinct cytoskeletal structures involved in complement- and Fc receptor-mediated phagocytosis in macrophages. J Exp Med. 1996 Aug 1;184(2):627–637. doi: 10.1084/jem.184.2.627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Allen W. E., Zicha D., Ridley A. J., Jones G. E. A role for Cdc42 in macrophage chemotaxis. J Cell Biol. 1998 Jun 1;141(5):1147–1157. doi: 10.1083/jcb.141.5.1147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Amyere Mustapha, Mettlen Marcel, Van Der Smissen Patrick, Platek Anna, Payrastre Bernard, Veithen Alex, Courtoy Pierre J. Origin, originality, functions, subversions and molecular signalling of macropinocytosis. Int J Med Microbiol. 2002 Feb;291(6-7):487–494. doi: 10.1078/1438-4221-00157. [DOI] [PubMed] [Google Scholar]
  6. Apodaca G. Endocytic traffic in polarized epithelial cells: role of the actin and microtubule cytoskeleton. Traffic. 2001 Mar;2(3):149–159. doi: 10.1034/j.1600-0854.2001.020301.x. [DOI] [PubMed] [Google Scholar]
  7. Bagrodia S., Cerione R. A. Pak to the future. Trends Cell Biol. 1999 Sep;9(9):350–355. doi: 10.1016/s0962-8924(99)01618-9. [DOI] [PubMed] [Google Scholar]
  8. Barbieri M. A., Heath C. M., Peters E. M., Wells A., Davis J. N., Stahl P. D. Phosphatidylinositol-4-phosphate 5-kinase-1beta is essential for epidermal growth factor receptor-mediated endocytosis. J Biol Chem. 2001 Oct 1;276(50):47212–47216. doi: 10.1074/jbc.C100490200. [DOI] [PubMed] [Google Scholar]
  9. Barois N., Forquet F., Davoust J. Actin microfilaments control the MHC class II antigen presentation pathway in B cells. J Cell Sci. 1998 Jul;111(Pt 13):1791–1800. doi: 10.1242/jcs.111.13.1791. [DOI] [PubMed] [Google Scholar]
  10. Benesch Stefanie, Lommel Silvia, Steffen Anika, Stradal Theresia E. B., Scaplehorn Niki, Way Michael, Wehland Juergen, Rottner Klemens. Phosphatidylinositol 4,5-biphosphate (PIP2)-induced vesicle movement depends on N-WASP and involves Nck, WIP, and Grb2. J Biol Chem. 2002 Jul 29;277(40):37771–37776. doi: 10.1074/jbc.M204145200. [DOI] [PubMed] [Google Scholar]
  11. Bishop A. L., Hall A. Rho GTPases and their effector proteins. Biochem J. 2000 Jun 1;348(Pt 2):241–255. [PMC free article] [PubMed] [Google Scholar]
  12. Bogan J. S., Lodish H. F. Two compartments for insulin-stimulated exocytosis in 3T3-L1 adipocytes defined by endogenous ACRP30 and GLUT4. J Cell Biol. 1999 Aug 9;146(3):609–620. doi: 10.1083/jcb.146.3.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Botelho R. J., Teruel M., Dierckman R., Anderson R., Wells A., York J. D., Meyer T., Grinstein S. Localized biphasic changes in phosphatidylinositol-4,5-bisphosphate at sites of phagocytosis. J Cell Biol. 2000 Dec 25;151(7):1353–1368. doi: 10.1083/jcb.151.7.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Bretscher M. S., Aguado-Velasco C. Membrane traffic during cell locomotion. Curr Opin Cell Biol. 1998 Aug;10(4):537–541. doi: 10.1016/s0955-0674(98)80070-7. [DOI] [PubMed] [Google Scholar]
  15. Brodsky F. M., Chen C. Y., Knuehl C., Towler M. C., Wakeham D. E. Biological basket weaving: formation and function of clathrin-coated vesicles. Annu Rev Cell Dev Biol. 2001;17:517–568. doi: 10.1146/annurev.cellbio.17.1.517. [DOI] [PubMed] [Google Scholar]
  16. Bryant Nia J., Govers Roland, James David E. Regulated transport of the glucose transporter GLUT4. Nat Rev Mol Cell Biol. 2002 Apr;3(4):267–277. doi: 10.1038/nrm782. [DOI] [PubMed] [Google Scholar]
  17. Caron E., Hall A. Identification of two distinct mechanisms of phagocytosis controlled by different Rho GTPases. Science. 1998 Nov 27;282(5394):1717–1721. doi: 10.1126/science.282.5394.1717. [DOI] [PubMed] [Google Scholar]
  18. Caron Emmanuelle. Regulation of Wiskott-Aldrich syndrome protein and related molecules. Curr Opin Cell Biol. 2002 Feb;14(1):82–87. doi: 10.1016/s0955-0674(01)00298-8. [DOI] [PubMed] [Google Scholar]
  19. Castellano F., Montcourrier P., Chavrier P. Membrane recruitment of Rac1 triggers phagocytosis. J Cell Sci. 2000 Sep;113(Pt 17):2955–2961. doi: 10.1242/jcs.113.17.2955. [DOI] [PubMed] [Google Scholar]
  20. Castellano F., Montcourrier P., Guillemot J. C., Gouin E., Machesky L., Cossart P., Chavrier P. Inducible recruitment of Cdc42 or WASP to a cell-surface receptor triggers actin polymerization and filopodium formation. Curr Biol. 1999 Apr 8;9(7):351–360. doi: 10.1016/s0960-9822(99)80161-4. [DOI] [PubMed] [Google Scholar]
  21. Chang Fred, Peter Matthias. Cell biology. Formins set the record straight. Science. 2002 Jul 26;297(5581):531–532. doi: 10.1126/science.1074649. [DOI] [PubMed] [Google Scholar]
  22. Chiang S. H., Baumann C. A., Kanzaki M., Thurmond D. C., Watson R. T., Neudauer C. L., Macara I. G., Pessin J. E., Saltiel A. R. Insulin-stimulated GLUT4 translocation requires the CAP-dependent activation of TC10. Nature. 2001 Apr 19;410(6831):944–948. doi: 10.1038/35073608. [DOI] [PubMed] [Google Scholar]
  23. Chimini G., Chavrier P. Function of Rho family proteins in actin dynamics during phagocytosis and engulfment. Nat Cell Biol. 2000 Oct;2(10):E191–E196. doi: 10.1038/35036454. [DOI] [PubMed] [Google Scholar]
  24. Clague Michael J. Membrane transport: a coat for ubiquitin. Curr Biol. 2002 Aug 6;12(15):R529–R531. doi: 10.1016/s0960-9822(02)01030-8. [DOI] [PubMed] [Google Scholar]
  25. Cook T. A., Nagasaki T., Gundersen G. G. Rho guanosine triphosphatase mediates the selective stabilization of microtubules induced by lysophosphatidic acid. J Cell Biol. 1998 Apr 6;141(1):175–185. doi: 10.1083/jcb.141.1.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Cremona O., De Camilli P. Phosphoinositides in membrane traffic at the synapse. J Cell Sci. 2001 Mar;114(Pt 6):1041–1052. doi: 10.1242/jcs.114.6.1041. [DOI] [PubMed] [Google Scholar]
  27. Daub H., Gevaert K., Vandekerckhove J., Sobel A., Hall A. Rac/Cdc42 and p65PAK regulate the microtubule-destabilizing protein stathmin through phosphorylation at serine 16. J Biol Chem. 2000 Oct 31;276(3):1677–1680. doi: 10.1074/jbc.C000635200. [DOI] [PubMed] [Google Scholar]
  28. Dharmawardhane S., Brownson D., Lennartz M., Bokoch G. M. Localization of p21-activated kinase 1 (PAK1) to pseudopodia, membrane ruffles, and phagocytic cups in activated human neutrophils. J Leukoc Biol. 1999 Sep;66(3):521–527. doi: 10.1002/jlb.66.3.521. [DOI] [PubMed] [Google Scholar]
  29. Dharmawardhane S., Sanders L. C., Martin S. S., Daniels R. H., Bokoch G. M. Localization of p21-activated kinase 1 (PAK1) to pinocytic vesicles and cortical actin structures in stimulated cells. J Cell Biol. 1997 Sep 22;138(6):1265–1278. doi: 10.1083/jcb.138.6.1265. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Dharmawardhane S., Schürmann A., Sells M. A., Chernoff J., Schmid S. L., Bokoch G. M. Regulation of macropinocytosis by p21-activated kinase-1. Mol Biol Cell. 2000 Oct;11(10):3341–3352. doi: 10.1091/mbc.11.10.3341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Diakonova Maria, Bokoch Gary, Swanson Joel A. Dynamics of cytoskeletal proteins during Fcgamma receptor-mediated phagocytosis in macrophages. Mol Biol Cell. 2002 Feb;13(2):402–411. doi: 10.1091/mbc.01-05-0273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Eitzen G., Thorngren N., Wickner W. Rho1p and Cdc42p act after Ypt7p to regulate vacuole docking. EMBO J. 2001 Oct 15;20(20):5650–5656. doi: 10.1093/emboj/20.20.5650. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Eitzen Gary, Wang Li, Thorngren Naomi, Wickner William. Remodeling of organelle-bound actin is required for yeast vacuole fusion. J Cell Biol. 2002 Aug 12;158(4):669–679. doi: 10.1083/jcb.200204089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Etienne-Manneville S., Hall A. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell. 2001 Aug 24;106(4):489–498. doi: 10.1016/s0092-8674(01)00471-8. [DOI] [PubMed] [Google Scholar]
  35. Fujimoto L. M., Roth R., Heuser J. E., Schmid S. L. Actin assembly plays a variable, but not obligatory role in receptor-mediated endocytosis in mammalian cells. Traffic. 2000 Feb;1(2):161–171. doi: 10.1034/j.1600-0854.2000.010208.x. [DOI] [PubMed] [Google Scholar]
  36. Fukata Masaki, Watanabe Takashi, Noritake Jun, Nakagawa Masato, Yamaga Masaki, Kuroda Shinya, Matsuura Yoshiharu, Iwamatsu Akihiro, Perez Franck, Kaibuchi Kozo. Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell. 2002 Jun 28;109(7):873–885. doi: 10.1016/s0092-8674(02)00800-0. [DOI] [PubMed] [Google Scholar]
  37. Gampel A., Parker P. J., Mellor H. Regulation of epidermal growth factor receptor traffic by the small GTPase rhoB. Curr Biol. 1999 Sep 9;9(17):955–958. doi: 10.1016/s0960-9822(99)80422-9. [DOI] [PubMed] [Google Scholar]
  38. Gampel Alexandra, Mellor Harry. Small interfering RNAs as a tool to assign Rho GTPase exchange-factor function in vivo. Biochem J. 2002 Sep 1;366(Pt 2):393–398. doi: 10.1042/BJ20020844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Garrett W. S., Chen L. M., Kroschewski R., Ebersold M., Turley S., Trombetta S., Galán J. E., Mellman I. Developmental control of endocytosis in dendritic cells by Cdc42. Cell. 2000 Aug 4;102(3):325–334. doi: 10.1016/s0092-8674(00)00038-6. [DOI] [PubMed] [Google Scholar]
  40. Gorvel J. P., Méresse S. Maturation steps of the Salmonella-containing vacuole. Microbes Infect. 2001 Nov-Dec;3(14-15):1299–1303. doi: 10.1016/s1286-4579(01)01490-3. [DOI] [PubMed] [Google Scholar]
  41. Gulli M. P., Peter M. Temporal and spatial regulation of Rho-type guanine-nucleotide exchange factors: the yeast perspective. Genes Dev. 2001 Feb 15;15(4):365–379. doi: 10.1101/gad.876901. [DOI] [PubMed] [Google Scholar]
  42. Gundersen G. G., Bulinski J. C. Selective stabilization of microtubules oriented toward the direction of cell migration. Proc Natl Acad Sci U S A. 1988 Aug;85(16):5946–5950. doi: 10.1073/pnas.85.16.5946. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Hall A. Rho GTPases and the actin cytoskeleton. Science. 1998 Jan 23;279(5350):509–514. doi: 10.1126/science.279.5350.509. [DOI] [PubMed] [Google Scholar]
  44. Hardt W. D., Chen L. M., Schuebel K. E., Bustelo X. R., Galán J. E. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell. 1998 May 29;93(5):815–826. doi: 10.1016/s0092-8674(00)81442-7. [DOI] [PubMed] [Google Scholar]
  45. Hoffmann P. R., deCathelineau A. M., Ogden C. A., Leverrier Y., Bratton D. L., Daleke D. L., Ridley A. J., Fadok V. A., Henson P. M. Phosphatidylserine (PS) induces PS receptor-mediated macropinocytosis and promotes clearance of apoptotic cells. J Cell Biol. 2001 Nov 12;155(4):649–659. doi: 10.1083/jcb.200108080. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Hussain N. K., Jenna S., Glogauer M., Quinn C. C., Wasiak S., Guipponi M., Antonarakis S. E., Kay B. K., Stossel T. P., Lamarche-Vane N. Endocytic protein intersectin-l regulates actin assembly via Cdc42 and N-WASP. Nat Cell Biol. 2001 Oct;3(10):927–932. doi: 10.1038/ncb1001-927. [DOI] [PubMed] [Google Scholar]
  47. Jiang Zhen Y., Chawla Anil, Bose Avirup, Way Michael, Czech Michael P. A phosphatidylinositol 3-kinase-independent insulin signaling pathway to N-WASP/Arp2/3/F-actin required for GLUT4 glucose transporter recycling. J Biol Chem. 2001 Nov 1;277(1):509–515. doi: 10.1074/jbc.M108280200. [DOI] [PubMed] [Google Scholar]
  48. Kanzaki Makoto, Watson Robert T., Hou June Chunqiu, Stamnes Mark, Saltiel Alan R., Pessin Jeffrey E. Small GTP-binding protein TC10 differentially regulates two distinct populations of filamentous actin in 3T3L1 adipocytes. Mol Biol Cell. 2002 Jul;13(7):2334–2346. doi: 10.1091/mbc.01-10-0490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Kessels Michael M., Qualmann Britta. Syndapins integrate N-WASP in receptor-mediated endocytosis. EMBO J. 2002 Nov 15;21(22):6083–6094. doi: 10.1093/emboj/cdf604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Kroschewski R., Hall A., Mellman I. Cdc42 controls secretory and endocytic transport to the basolateral plasma membrane of MDCK cells. Nat Cell Biol. 1999 May;1(1):8–13. doi: 10.1038/8977. [DOI] [PubMed] [Google Scholar]
  51. Lamaze C., Chuang T. H., Terlecky L. J., Bokoch G. M., Schmid S. L. Regulation of receptor-mediated endocytosis by Rho and Rac. Nature. 1996 Jul 11;382(6587):177–179. doi: 10.1038/382177a0. [DOI] [PubMed] [Google Scholar]
  52. Lamaze C., Dujeancourt A., Baba T., Lo C. G., Benmerah A., Dautry-Varsat A. Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. Mol Cell. 2001 Mar;7(3):661–671. doi: 10.1016/s1097-2765(01)00212-x. [DOI] [PubMed] [Google Scholar]
  53. Leverrier Y., Lorenzi R., Blundell M. P., Brickell P., Kinnon C., Ridley A. J., Thrasher A. J. Cutting edge: the Wiskott-Aldrich syndrome protein is required for efficient phagocytosis of apoptotic cells. J Immunol. 2001 Apr 15;166(8):4831–4834. doi: 10.4049/jimmunol.166.8.4831. [DOI] [PubMed] [Google Scholar]
  54. Li E., Stupack D., Bokoch G. M., Nemerow G. R. Adenovirus endocytosis requires actin cytoskeleton reorganization mediated by Rho family GTPases. J Virol. 1998 Nov;72(11):8806–8812. doi: 10.1128/jvi.72.11.8806-8812.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Li G., D'Souza-Schorey C., Barbieri M. A., Cooper J. A., Stahl P. D. Uncoupling of membrane ruffling and pinocytosis during Ras signal transduction. J Biol Chem. 1997 Apr 18;272(16):10337–10340. [PubMed] [Google Scholar]
  56. Lin Qiong, Lo Charles G., Cerione Richard A., Yang Wannian. The Cdc42 target ACK2 interacts with sorting nexin 9 (SH3PX1) to regulate epidermal growth factor receptor degradation. J Biol Chem. 2002 Jan 17;277(12):10134–10138. doi: 10.1074/jbc.M110329200. [DOI] [PubMed] [Google Scholar]
  57. Locker J. K., Kuehn A., Schleich S., Rutter G., Hohenberg H., Wepf R., Griffiths G. Entry of the two infectious forms of vaccinia virus at the plasma membane is signaling-dependent for the IMV but not the EEV. Mol Biol Cell. 2000 Jul;11(7):2497–2511. doi: 10.1091/mbc.11.7.2497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Lorenzi R., Brickell P. M., Katz D. R., Kinnon C., Thrasher A. J. Wiskott-Aldrich syndrome protein is necessary for efficient IgG-mediated phagocytosis. Blood. 2000 May 1;95(9):2943–2946. [PubMed] [Google Scholar]
  59. Luzio J. P., Mullock B. M., Pryor P. R., Lindsay M. R., James D. E., Piper R. C. Relationship between endosomes and lysosomes. Biochem Soc Trans. 2001 Aug;29(Pt 4):476–480. doi: 10.1042/bst0290476. [DOI] [PubMed] [Google Scholar]
  60. Ma L., Cantley L. C., Janmey P. A., Kirschner M. W. Corequirement of specific phosphoinositides and small GTP-binding protein Cdc42 in inducing actin assembly in Xenopus egg extracts. J Cell Biol. 1998 Mar 9;140(5):1125–1136. doi: 10.1083/jcb.140.5.1125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Malecz N., McCabe P. C., Spaargaren C., Qiu R., Chuang Y., Symons M. Synaptojanin 2, a novel Rac1 effector that regulates clathrin-mediated endocytosis. Curr Biol. 2000 Nov 2;10(21):1383–1386. doi: 10.1016/s0960-9822(00)00778-8. [DOI] [PubMed] [Google Scholar]
  62. Manser E., Leung T., Salihuddin H., Tan L., Lim L. A non-receptor tyrosine kinase that inhibits the GTPase activity of p21cdc42. Nature. 1993 May 27;363(6427):364–367. doi: 10.1038/363364a0. [DOI] [PubMed] [Google Scholar]
  63. Martin T. F. PI(4,5)P(2) regulation of surface membrane traffic. Curr Opin Cell Biol. 2001 Aug;13(4):493–499. doi: 10.1016/s0955-0674(00)00241-6. [DOI] [PubMed] [Google Scholar]
  64. Massol P., Montcourrier P., Guillemot J. C., Chavrier P. Fc receptor-mediated phagocytosis requires CDC42 and Rac1. EMBO J. 1998 Nov 2;17(21):6219–6229. doi: 10.1093/emboj/17.21.6219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. May R. C., Caron E., Hall A., Machesky L. M. Involvement of the Arp2/3 complex in phagocytosis mediated by FcgammaR or CR3. Nat Cell Biol. 2000 Apr;2(4):246–248. doi: 10.1038/35008673. [DOI] [PubMed] [Google Scholar]
  66. May R. C., Machesky L. M. Phagocytosis and the actin cytoskeleton. J Cell Sci. 2001 Mar;114(Pt 6):1061–1077. doi: 10.1242/jcs.114.6.1061. [DOI] [PubMed] [Google Scholar]
  67. McGavin M. K., Badour K., Hardy L. A., Kubiseski T. J., Zhang J., Siminovitch K. A. The intersectin 2 adaptor links Wiskott Aldrich Syndrome protein (WASp)-mediated actin polymerization to T cell antigen receptor endocytosis. J Exp Med. 2001 Dec 17;194(12):1777–1787. doi: 10.1084/jem.194.12.1777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Mellman I., Steinman R. M. Dendritic cells: specialized and regulated antigen processing machines. Cell. 2001 Aug 10;106(3):255–258. doi: 10.1016/s0092-8674(01)00449-4. [DOI] [PubMed] [Google Scholar]
  69. Merrifield Christien J., Feldman Morris E., Wan Lei, Almers Wolfhard. Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol. 2002 Sep;4(9):691–698. doi: 10.1038/ncb837. [DOI] [PubMed] [Google Scholar]
  70. Murphy C., Saffrich R., Grummt M., Gournier H., Rybin V., Rubino M., Auvinen P., Lütcke A., Parton R. G., Zerial M. Endosome dynamics regulated by a Rho protein. Nature. 1996 Dec 5;384(6608):427–432. doi: 10.1038/384427a0. [DOI] [PubMed] [Google Scholar]
  71. Murphy C., Saffrich R., Olivo-Marin J. C., Giner A., Ansorge W., Fotsis T., Zerial M. Dual function of rhoD in vesicular movement and cell motility. Eur J Cell Biol. 2001 Jun;80(6):391–398. doi: 10.1078/0171-9335-00173. [DOI] [PubMed] [Google Scholar]
  72. Müller O., Johnson D. I., Mayer A. Cdc42p functions at the docking stage of yeast vacuole membrane fusion. EMBO J. 2001 Oct 15;20(20):5657–5665. doi: 10.1093/emboj/20.20.5657. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Nichols B. J., Lippincott-Schwartz J. Endocytosis without clathrin coats. Trends Cell Biol. 2001 Oct;11(10):406–412. doi: 10.1016/s0962-8924(01)02107-9. [DOI] [PubMed] [Google Scholar]
  74. Nobes C. D., Hall A. Rho GTPases control polarity, protrusion, and adhesion during cell movement. J Cell Biol. 1999 Mar 22;144(6):1235–1244. doi: 10.1083/jcb.144.6.1235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Nobes C. D., Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell. 1995 Apr 7;81(1):53–62. doi: 10.1016/0092-8674(95)90370-4. [DOI] [PubMed] [Google Scholar]
  76. O'Bryan J. P., Mohney R. P., Oldham C. E. Mitogenesis and endocytosis: What's at the INTERSECTIoN? Oncogene. 2001 Oct 1;20(44):6300–6308. doi: 10.1038/sj.onc.1204773. [DOI] [PubMed] [Google Scholar]
  77. Ohno S. Intercellular junctions and cellular polarity: the PAR-aPKC complex, a conserved core cassette playing fundamental roles in cell polarity. Curr Opin Cell Biol. 2001 Oct;13(5):641–648. doi: 10.1016/s0955-0674(00)00264-7. [DOI] [PubMed] [Google Scholar]
  78. Olazabal Isabel M., Caron Emmanuelle, May Robin C., Schilling Kerstin, Knecht David A., Machesky Laura M. Rho-kinase and myosin-II control phagocytic cup formation during CR, but not FcgammaR, phagocytosis. Curr Biol. 2002 Aug 20;12(16):1413–1418. doi: 10.1016/s0960-9822(02)01069-2. [DOI] [PubMed] [Google Scholar]
  79. Palazzo A. F., Cook T. A., Alberts A. S., Gundersen G. G. mDia mediates Rho-regulated formation and orientation of stable microtubules. Nat Cell Biol. 2001 Aug;3(8):723–729. doi: 10.1038/35087035. [DOI] [PubMed] [Google Scholar]
  80. Palazzo A. F., Joseph H. L., Chen Y. J., Dujardin D. L., Alberts A. S., Pfister K. K., Vallee R. B., Gundersen G. G. Cdc42, dynein, and dynactin regulate MTOC reorientation independent of Rho-regulated microtubule stabilization. Curr Biol. 2001 Oct 2;11(19):1536–1541. doi: 10.1016/s0960-9822(01)00475-4. [DOI] [PubMed] [Google Scholar]
  81. Pollard Thomas D. Formins initiate new actin filaments. Nat Cell Biol. 2002 Aug;4(8):E191–E191. doi: 10.1038/ncb0802-e191a. [DOI] [PubMed] [Google Scholar]
  82. Qualmann B., Kessels M. M., Kelly R. B. Molecular links between endocytosis and the actin cytoskeleton. J Cell Biol. 2000 Sep 4;150(5):F111–F116. doi: 10.1083/jcb.150.5.f111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Qualmann Britta, Kessels Michael M. Endocytosis and the cytoskeleton. Int Rev Cytol. 2002;220:93–144. doi: 10.1016/s0074-7696(02)20004-2. [DOI] [PubMed] [Google Scholar]
  84. Raiborg Camilla, Bache Kristi G., Gillooly David J., Madshus Inger Helene, Stang Espen, Stenmark Harald. Hrs sorts ubiquitinated proteins into clathrin-coated microdomains of early endosomes. Nat Cell Biol. 2002 May;4(5):394–398. doi: 10.1038/ncb791. [DOI] [PubMed] [Google Scholar]
  85. Reddien P. W., Horvitz H. R. CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nat Cell Biol. 2000 Mar;2(3):131–136. doi: 10.1038/35004000. [DOI] [PubMed] [Google Scholar]
  86. Ridley A. J., Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell. 1992 Aug 7;70(3):389–399. doi: 10.1016/0092-8674(92)90163-7. [DOI] [PubMed] [Google Scholar]
  87. Ridley A. J., Paterson H. F., Johnston C. L., Diekmann D., Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell. 1992 Aug 7;70(3):401–410. doi: 10.1016/0092-8674(92)90164-8. [DOI] [PubMed] [Google Scholar]
  88. Ridley A. J. Rho GTPases and cell migration. J Cell Sci. 2001 Aug;114(Pt 15):2713–2722. doi: 10.1242/jcs.114.15.2713. [DOI] [PubMed] [Google Scholar]
  89. Ridley A. J. Rho proteins: linking signaling with membrane trafficking. Traffic. 2001 May;2(5):303–310. doi: 10.1034/j.1600-0854.2001.002005303.x. [DOI] [PubMed] [Google Scholar]
  90. Robertson D., Paterson H. F., Adamson P., Hall A., Monaghan P. Ultrastructural localization of ras-related proteins using epitope-tagged plasmids. J Histochem Cytochem. 1995 May;43(5):471–480. doi: 10.1177/43.5.7537292. [DOI] [PubMed] [Google Scholar]
  91. Rohatgi R., Ma L., Miki H., Lopez M., Kirchhausen T., Takenawa T., Kirschner M. W. The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell. 1999 Apr 16;97(2):221–231. doi: 10.1016/s0092-8674(00)80732-1. [DOI] [PubMed] [Google Scholar]
  92. Rojas R., Ruiz W. G., Leung S. M., Jou T. S., Apodaca G. Cdc42-dependent modulation of tight junctions and membrane protein traffic in polarized Madin-Darby canine kidney cells. Mol Biol Cell. 2001 Aug;12(8):2257–2274. doi: 10.1091/mbc.12.8.2257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Sabharanjak Shefali, Sharma Pranav, Parton Robert G., Mayor Satyajit. GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. Dev Cell. 2002 Apr;2(4):411–423. doi: 10.1016/s1534-5807(02)00145-4. [DOI] [PubMed] [Google Scholar]
  94. Sachse Martin, Urbé Sylvie, Oorschot Viola, Strous Ger J., Klumperman Judith. Bilayered clathrin coats on endosomal vacuoles are involved in protein sorting toward lysosomes. Mol Biol Cell. 2002 Apr;13(4):1313–1328. doi: 10.1091/mbc.01-10-0525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Sansonetti P. Host-pathogen interactions: the seduction of molecular cross talk. Gut. 2002 May;50 (Suppl 3):III2–III8. doi: 10.1136/gut.50.suppl_3.iii2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Schafer Dorothy A. Coupling actin dynamics and membrane dynamics during endocytosis. Curr Opin Cell Biol. 2002 Feb;14(1):76–81. doi: 10.1016/s0955-0674(01)00297-6. [DOI] [PubMed] [Google Scholar]
  97. Settleman J. Rac 'n Rho: the music that shapes a developing embryo. Dev Cell. 2001 Sep;1(3):321–331. doi: 10.1016/s1534-5807(01)00053-3. [DOI] [PubMed] [Google Scholar]
  98. Takenawa T., Miki H. WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J Cell Sci. 2001 May;114(Pt 10):1801–1809. doi: 10.1242/jcs.114.10.1801. [DOI] [PubMed] [Google Scholar]
  99. Taunton J., Rowning B. A., Coughlin M. L., Wu M., Moon R. T., Mitchison T. J., Larabell C. A. Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP. J Cell Biol. 2000 Feb 7;148(3):519–530. doi: 10.1083/jcb.148.3.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. Teo M., Tan L., Lim L., Manser E. The tyrosine kinase ACK1 associates with clathrin-coated vesicles through a binding motif shared by arrestin and other adaptors. J Biol Chem. 2001 Feb 27;276(21):18392–18398. doi: 10.1074/jbc.M008795200. [DOI] [PubMed] [Google Scholar]
  101. Tolias K. F., Cantley L. C., Carpenter C. L. Rho family GTPases bind to phosphoinositide kinases. J Biol Chem. 1995 Jul 28;270(30):17656–17659. doi: 10.1074/jbc.270.30.17656. [DOI] [PubMed] [Google Scholar]
  102. Tolias K. F., Hartwig J. H., Ishihara H., Shibasaki Y., Cantley L. C., Carpenter C. L. Type Ialpha phosphatidylinositol-4-phosphate 5-kinase mediates Rac-dependent actin assembly. Curr Biol. 2000 Feb 10;10(3):153–156. doi: 10.1016/s0960-9822(00)00315-8. [DOI] [PubMed] [Google Scholar]
  103. Tominaga T., Sahai E., Chardin P., McCormick F., Courtneidge S. A., Alberts A. S. Diaphanous-related formins bridge Rho GTPase and Src tyrosine kinase signaling. Mol Cell. 2000 Jan;5(1):13–25. doi: 10.1016/s1097-2765(00)80399-8. [DOI] [PubMed] [Google Scholar]
  104. Valster A. H., Hepler P. K., Chernoff J. Plant GTPases: the Rhos in bloom. Trends Cell Biol. 2000 Apr;10(4):141–146. doi: 10.1016/s0962-8924(00)01728-1. [DOI] [PubMed] [Google Scholar]
  105. Watson R. T., Shigematsu S., Chiang S. H., Mora S., Kanzaki M., Macara I. G., Saltiel A. R., Pessin J. E. Lipid raft microdomain compartmentalization of TC10 is required for insulin signaling and GLUT4 translocation. J Cell Biol. 2001 Aug 13;154(4):829–840. doi: 10.1083/jcb.200102078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  106. Welch Heidi C. E., Coadwell W. John, Ellson Christian D., Ferguson G. John, Andrews Simon R., Erdjument-Bromage Hediye, Tempst Paul, Hawkins Phillip T., Stephens Len R. P-Rex1, a PtdIns(3,4,5)P3- and Gbetagamma-regulated guanine-nucleotide exchange factor for Rac. Cell. 2002 Mar 22;108(6):809–821. doi: 10.1016/s0092-8674(02)00663-3. [DOI] [PubMed] [Google Scholar]
  107. Welch M. D. The world according to Arp: regulation of actin nucleation by the Arp2/3 complex. Trends Cell Biol. 1999 Nov;9(11):423–427. doi: 10.1016/s0962-8924(99)01651-7. [DOI] [PubMed] [Google Scholar]
  108. West M. A., Prescott A. R., Eskelinen E. L., Ridley A. J., Watts C. Rac is required for constitutive macropinocytosis by dendritic cells but does not control its downregulation. Curr Biol. 2000 Jul 13;10(14):839–848. doi: 10.1016/s0960-9822(00)00595-9. [DOI] [PubMed] [Google Scholar]
  109. Wherlock Matthew, Mellor Harry. The Rho GTPase family: a Racs to Wrchs story. J Cell Sci. 2002 Jan 15;115(Pt 2):239–240. doi: 10.1242/jcs.115.2.239. [DOI] [PubMed] [Google Scholar]
  110. Wiedemann A., Linder S., Grassl G., Albert M., Autenrieth I., Aepfelbacher M. Yersinia enterocolitica invasin triggers phagocytosis via beta1 integrins, CDC42Hs and WASp in macrophages. Cell Microbiol. 2001 Oct;3(10):693–702. doi: 10.1046/j.1462-5822.2001.00149.x. [DOI] [PubMed] [Google Scholar]
  111. Wilkins A., Insall R. H. Small GTPases in Dictyostelium: lessons from a social amoeba. Trends Genet. 2001 Jan;17(1):41–48. doi: 10.1016/s0168-9525(00)02181-8. [DOI] [PubMed] [Google Scholar]
  112. Wright S. D., Weitz J. I., Huang A. J., Levin S. M., Silverstein S. C., Loike J. D. Complement receptor type three (CD11b/CD18) of human polymorphonuclear leukocytes recognizes fibrinogen. Proc Natl Acad Sci U S A. 1988 Oct;85(20):7734–7738. doi: 10.1073/pnas.85.20.7734. [DOI] [PMC free article] [PubMed] [Google Scholar]
  113. Yang W., Lo C. G., Dispenza T., Cerione R. A. The Cdc42 target ACK2 directly interacts with clathrin and influences clathrin assembly. J Biol Chem. 2001 Feb 15;276(20):17468–17473. doi: 10.1074/jbc.M010893200. [DOI] [PubMed] [Google Scholar]
  114. Zhang J., Shehabeldin A., da Cruz L. A., Butler J., Somani A. K., McGavin M., Kozieradzki I., dos Santos A. O., Nagy A., Grinstein S. Antigen receptor-induced activation and cytoskeletal rearrangement are impaired in Wiskott-Aldrich syndrome protein-deficient lymphocytes. J Exp Med. 1999 Nov 1;190(9):1329–1342. doi: 10.1084/jem.190.9.1329. [DOI] [PMC free article] [PubMed] [Google Scholar]
  115. van Deurs B., Holm P. K., Kayser L., Sandvig K. Delivery to lysosomes in the human carcinoma cell line HEp-2 involves an actin filament-facilitated fusion between mature endosomes and preexisting lysosomes. Eur J Cell Biol. 1995 Apr;66(4):309–323. [PubMed] [Google Scholar]

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