Cell surface dynamics - how Rho GTPases orchestrate the interplay between the plasma membrane and the cortical cytoskeleton

Journal of Cell Science

Volumn 125, Issue 19, 2012, Pages 4435-4444

  de Curtis, Ivan ^a   Meldolesi, Jacopo ^a  

^a VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

Actin polymerization; Endocytosis; Exocytosis; Membrane dynamics; Small GTPase

Indexed keywords

ACTIN; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 1; ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; ARF PROTEIN; GUANOSINE TRIPHOSPHATASE; PROTEIN CDC42; RAB PROTEIN; RAC1 PROTEIN; RAS PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ARTICLE; CELL FUNCTION; CELL INTERACTION; CELL MEMBRANE; CELL SHAPE; CELL SURFACE; CELL VACUOLE; COMPLEX FORMATION; CYTOSKELETON; ENDOCYTOSIS; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME REGULATION; EXOCYTOSIS; INTERNALIZATION; MEMBRANE BIOLOGY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN TARGETING; REGULATORY MECHANISM; SURFACE PROPERTY;

ANIMALS; CELL MEMBRANE; CYTOSKELETON; ENDOCYTOSIS; EXOCYTOSIS; HUMANS; MODELS, BIOLOGICAL; RHO GTP-BINDING PROTEINS;

EID: 84872202588     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.108266     Document Type: Article

References (121)

1. Abdel-Latif, D., Steward, M. and Lacy, P. (2005). Neutrophil primary granule release and maximal superoxide generation depend on Rac2 in a common signalling pathway. Can. J. Physiol. Pharmacol. 83, 69-75.
2. Alberts, P., Rudge, R., Irinopoulou, T., Danglot, L., Gauthier-Rouvie're, C. and Galli, T. (2006). Cdc42 and actin control polarized expression of TI-VAMP vesicles to neuronal growth cones and their fusion with the plasma membrane. Mol. Biol. Cell 17, 1194-1203.
3. Arora, P. D., Marignani, P. A. and McCulloch, C. A. (2008). Collagen phagocytosis is regulated by the guanine nucleotide exchange factor Vav2. Am. J. Physiol. Cell Physiol. 295, C130-C137.
4. Asperti, C., Astro, V., Pettinato, E., Paris, S., Bachi, A. and de Curtis, I. (2011). Biochemical and functional characterization of the interaction between liprin-a1 and GIT1: implications for the regulation of cell motility. PLoS ONE 6, e20757.
5. Bretscher, M. S. (1996). Getting membrane flow and the cytoskeleton to cooperate in moving cells. Cell 87, 601-606.
6. Bröcker, C., Engelbrecht-Vandré, S. and Ungermann, C. (2010). Multisubunit tethering complexes and their role in membrane fusion. Curr. Biol. 20, R943-R952.
7. Brown, J. H., Del Re, D. P. and Sussman, M. A. (2006). The Rac and Rho hall of fame: a decade of hypertrophic signaling hits. Circ. Res. 98, 730-742.
8. Bu, W., Chou, A. M., Lim, K. B., Sudhaharan, T. and Ahmed, S. (2009). The Toca-1-N-WASP complex links filopodial formation to endocytosis. J. Biol. Chem. 284, 11622-11636.
9. Campellone, K. G. and Welch, M. D. (2010). A nucleator arms race: cellular control of actin assembly. Nat. Rev. Mol. Cell Biol. 11, 237-251.
10. Chen, X. W., Leto, D., Xiao, J., Goss, J., Wang, Q., Shavit, J. A., Xiong, T., Yu, G., Ginsburg, D., Toomre, D. et al. (2011). Exocyst function is regulated by effector phosphorylation. Nat. Cell Biol. 13, 580-588.
11. Chieregatti, E. and Meldolesi, J. (2005). Regulated exocytosis: new organelles for nonsecretory purposes. Nat. Rev. Mol. Cell Biol. 6, 181-187.
12. Citi, S., Spadaro, D., Schneider, Y., Stutz, J. and Pulimeno, P. (2011). Regulation of small GTPases at epithelial cell-cell junctions. Mol. Membr. Biol. 28, 427-444.
13. Clarke, M., Engel, U., Giorgione, J., Müller-Taubenberger, A., Prassler, J., Veltman, D. and Gerisch, G. (2010). Curvature recognition and force generation in phagocytosis. BMC Biol. 8, 154.
14. Corrotte, M., Chasserot-Golaz, S., Huang, P., Du, G., Ktistakis, N. T., Frohman, M. A., Vitale, N., Bader, M. F. and Grant, N. J. (2006). Dynamics and function of phospholipase D and phosphatidic acid during phagocytosis. Traffic 7, 365-377.
15. Côté, J. F. and Vuori, K. (2007). GEF what? Dock180 and related proteins help Rac to polarize cells in new ways. Trends Cell Biol. 17, 383-393.
16. Csépányi-Kömi, R., Sirokmány, G., Geiszt, M. and Ligeti, E. (2012). ARHGAP25, a novel Rac GTPase-activating protein, regulates phagocytosis in human neutrophilic granulocytes. Blood 119, 573-582.
17. D'Souza-Schorey, C. and Chavrier, P. (2006). ARF proteins: roles in membrane traffic and beyond. Nat. Rev. Mol. Cell Biol. 7, 347-358.
18. Danglot, L., Chaineau, M., Dahan, M., Gendron, M. C., Boggetto, N., Perez, F. and Galli, T. (2010). Role of TI-VAMP and CD82 in EGFR cell-surface dynamics and signaling. J. Cell Sci. 123, 723-735.
19. de Kreuk, B. J., Nethe, M., Fernandez-Borja, M., Anthony, E. C., Hensbergen, P. J., Deelder, A. M., Plomann, M. and Hordijk, P. L. (2011). The F-BAR domain protein PACSIN2 associates with Rac1 and regulates cell spreading and migration. J. Cell Sci. 124, 2375-2388.
20. Doherty, G. J. and Lundmark, R. (2009). GRAF1-dependent endocytosis. Biochem. Soc. Trans. 37, 1061-1065.
21. Doherty, G. J. and McMahon, H. T. (2009). Mechanisms of endocytosis. Annu. Rev. Biochem. 78, 857-902.
22. Donaldson, J. G. and Jackson, C. L. (2011). ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat. Rev. Mol. Cell Biol. 12, 362-375.
23. Dupraz, S., Grassi, D., Bernis, M. E., Sosa, L., Bisbal, M., Gastaldi, L., Jausoro, I., Cáceres, A., Pfenninger, K. H. and Quiroga, S. (2009). The TC10-Exo70 complex is essential for membrane expansion and axonal specification in developing neurons. J. Neurosci. 29, 13292-13301.
24. Echarri, A., Muriel, O., Pavón, D. M., Azegrouz, H., Escolar, F., Terrón, M. C., Sanchez-Cabo, F., Martínez, F., Montoya, M. C., Llorca, O. et al. (2012). Caveolar domain organization and trafficking is regulated by Abl kinases and mDia1. J. Cell Sci. 125, 3097-3113.
25. Falcone, S., Cocucci, E., Podini, P., Kirchhausen, T., Clementi, E. and Meldolesi, J. (2006). Macropinocytosis: regulated coordination of endocytic and exocytic membrane traffic events. J. Cell Sci. 119, 4758-4769.
26. Ferguson, S. M. and De Camilli, P. (2012). Dynamin, a membrane-remodelling GTPase. Nat. Rev. Mol. Cell Biol. 13, 75-88.
27. Flannagan, R. S., Jaumouillé, V. and Grinstein, S. (2012). The cell biology of phagocytosis. Annu. Rev. Pathol. 7, 61-98.
28. Frank, S. R. and Hansen, S. H. (2008). The PIX-GIT complex: a G protein signaling cassette in control of cell shape. Semin. Cell Dev. Biol. 19, 234-244.
29. Fütterer, K. and Machesky, L. M. (2007). "Wunder"F-BAR domains: going from pits to vesicles. Cell 129, 655-657.
30. Gauthier, N. C., Fardin, M. A., Roca-Cusachs, P. and Sheetz, M. P. (2011). Temporary increase in plasma membrane tension coordinates the activation of exocytosis and contraction during cell spreading. Proc. Natl. Acad. Sci. USA 108, 14467-14472.
31. Geissler, H., Ullmann, R. and Soldati, T. (2000). The tail domain of myosin M catalyses nucleotide exchange on Rac1 GTPases and can induce actin-driven surface protrusions. Traffic 1, 399-410.
32. Goldfinger, L. E. (2008). Choose your own path: specificity in Ras GTPase signaling. Mol. Biosyst. 4, 293-299.
33. Graham, T. R. and Kozlov, M. M. (2010). Interplay of proteins and lipids in generating membrane curvature. Curr. Opin. Cell Biol. 22, 430-436.
34. Guilluy, C., Garcia-Mata, R. and Burridge, K. (2011). Rho protein crosstalk: another social network? Trends Cell Biol. 21, 718-726.
35. Hall, A. and Lalli, G. (2010). Rho and Ras GTPases in axon growth, guidance, and branching. Cold Spring Harb. Perspect. Biol. 2, a001818.
36. Hansen, C. G. and Nichols, B. J. (2009). Molecular mechanisms of clathrinindependent endocytosis. J. Cell Sci. 122, 1713-1721.
37. Hansen, C. G., Bright, N. A., Howard, G. and Nichols, B. J. (2009). SDPR induces membrane curvature and functions in the formation of caveolae. Nat. Cell Biol. 11, 807-814.
38. He, B. and Guo, W. (2009). The exocyst complex in polarized exocytosis. Curr. Opin. Cell Biol. 21, 537-542.
39. Heasman, S. J. and Ridley, A. J. (2008). Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 9, 690-701.
40. Heo, W. D., Inoue, T., Park, W. S., Kim, M. L., Park, B. O., Wandless, T. J. and Meyer, T. (2006). PI(3,4,5)P3 and PI(4,5)P2 lipids target proteins with polybasic clusters to the plasma membrane. Science 314, 1458-1461.
41. Hill, M. M., Bastiani, M., Luetterforst, R., Kirkham, M., Kirkham, A., Nixon, S. J., Walser, P., Abankwa, D., Oorschot, V. M., Martin, S. et al. (2008). PTRF-Cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell 132, 113-124.
42. Hong, W. (2005). SNAREs and traffic. Biochim. Biophys. Acta 1744, 493-517.
43. Horgan, C. P. and McCaffrey, M. W. (2011). Rab GTPases and microtubule motors. Biochem. Soc. Trans. 39, 1202-1206.
44. Hutagalung, A. H. and Novick, P. J. (2011). Role of Rab GTPases in membrane traffic and cell physiology. Physiol. Rev. 91, 119-149.
45. Jahn, R. and Scheller, R. H. (2006). SNAREs-engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7, 631-643.
46. Jeon, C. Y., Kim, H. J., Lee, J. Y., Kim, J. B., Kim, S. C. and Park, J. B. (2010). p190RhoGAP and Rap-dependent RhoGAP (ARAP3) inactivate RhoA in response to nerve growth factor leading to neurite outgrowth from PC12 cells. Exp. Mol. Med. 42, 335-344.
47. Jeon, C. Y., Moon, M. Y., Kim, J. H., Kim, H. J., Kim, J. G., Li, Y., Jin, J. K., Kim, P. H., Kim, H. C., Meier, K. E. et al. (2012). Control of neurite outgrowth by RhoA inactivation. J. Neurochem. 120, 684-698.
48. Johnson, D. S. and Chen, Y. H. (2012). Ras family of small GTPases in immunity and inflammation. Curr. Opin. Pharmacol. 12, 458-463.
49. Johnson, J. L., Monfregola, J., Napolitano, G., Kiosses, W. B. and Catz, S. D. (2012). Vesicular trafficking through cortical actin during exocytosis is regulated by the Rab27a effector JFC1/Slp1 and the RhoA-GTPase-activating protein Gem-interacting protein. Mol. Biol. Cell 23, 1902-1916.
50. Kawase, K., Nakamura, T., Takaya, A., Aoki, K., Namikawa, K., Kiyama, H., Inagaki, S., Takemoto, H., Saltiel, A. R. and Matsuda, M. (2006). GTP hydrolysis by the Rho family GTPase TC10 promotes exocytic vesicle fusion. Dev. Cell 11, 411-421.
51. Klein, I. K., Predescu, D. N., Sharma, T., Knezevic, I., Malik, A. B. and Predescu, S. (2009). Intersectin-2L regulates caveola endocytosis secondary to Cdc42-mediated actin polymerization. J. Biol. Chem. 284, 25953-25961.
52. Koronakis, V., Hume, P. J., Humphreys, D., Liu, T., Hørning, O., Jensen, O. N. and McGhie, E. J. (2011). WAVE regulatory complex activation by cooperating GTPases Arf and Rac1. Proc. Natl. Acad. Sci. USA 108, 14449-14454.
53. Kozma, R., Sarner, S., Ahmed, S. and Lim, L. (1997). Rho family GTPases and neuronal growth cone remodelling: relationship between increased complexity induced by Cdc42Hs, Rac1, and acetylcholine and collapse induced by RhoA and lysophosphatidic acid. Mol. Cell. Biol. 17, 1201-1211.
54. Kumari, S. and Mayor, S. (2008). ARF1 is directly involved in dynamin-independent endocytosis. Nat. Cell Biol. 10, 30-41.
55. Lajoie, P. and Nabi, I. R. (2010). Lipid rafts, caveolae, and their endocytosis. Int. Rev. Cell Mol. Biol. 282, 135-163.
56. Lee, K., Gallop, J. L., Rambani, K. and Kirschner, M. W. (2010). Self-assembly of filopodia-like structures on supported lipid bilayers. Science 329, 1341-1345.
57. Lee, S. H. and Dominguez, R. (2010). Regulation of actin cytoskeleton dynamics in cells. Mol. Cells 29, 311-325.
58. Letinic, K., Sebastian, R., Toomre, D. and Rakic, P. (2009). Exocyst is involved in polarized cell migration and cerebral cortical development. Proc. Natl. Acad. Sci. USA 106, 11342-11347.
59. Lim, J. P. and Gleeson, P. A. (2011). Macropinocytosis: an endocytic pathway for internalising large gulps. Immunol. Cell Biol. 89, 836-843.
60. Liu, J., Sun, Y., Drubin, D. G. and Oster, G. F. (2009). The mechanochemistry of endocytosis. PLoS Biol. 7, e1000204.
61. Ludwig, A., Otto, G. P., Riento, K., Hams, E., Fallon, P. G. and Nichols, B. J. (2010). Flotillin microdomains interact with the cortical cytoskeleton to control uropod formation and neutrophil recruitment. J. Cell Biol. 191, 771-781.
62. Maekawa, M., Ishizaki, T., Boku, S., Watanabe, N., Fujita, A., Iwamatsu, A., Obinata, T., Ohashi, K., Mizuno, K. and Narumiya, S. (1999). Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 285, 895-898.
63. Malsam, J., Kreye, S. and Söllner, T. H. (2008). Membrane fusion: SNAREs and regulation. Cell. Mol. Life Sci. 65, 2814-2832.
64. Martin, T. F. (2012). Role of PI(4,5)P2 in vesicle exocytosis and membrane fusion. Subcell. Biochem. 59, 111-130.
65. Martinez-Arca, S., Coco, S., Mainguy, G., Schenk, U., Alberts, P., Bouillé, P., Mezzina, M., Prochiantz, A., Matteoli, M., Louvard, D. et al. (2001). A common exocytotic mechanism mediates axonal and dendritic outgrowth. J. Neurosci. 21, 3830-3838.
66. McConnell, R. E. and Tyska, M. J. (2010). Leveraging the membrane - cytoskeleton interface with myosin-1. Trends Cell Biol. 20, 418-426.
67. McMahon, H. T. and Boucrot, E. (2011). Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 12, 517-533.
68. Mellman, I. and Nelson, W. J. (2008). Coordinated protein sorting, targeting and distribution in polarized cells. Nat. Rev. Mol. Cell Biol. 9, 833-845.
69. Momboisse, F., Lonchamp, E., Calco, V., Ceridono, M., Vitale, N., Bader, M. F. and Gasman, S. (2009). betaPIX-activated Rac1 stimulates the activation of phospholipase D, which is associated with exocytosis in neuroendocrine cells. J. Cell Sci. 122, 798-806.
70. Momboisse, F., Ory, S., Ceridono, M., Calco, V., Vitale, N., Bader, M. F. and Gasman, S. (2010). The Rho guanine nucleotide exchange factors Intersectin 1L and b-Pix control calcium-regulated exocytosis in neuroendocrine PC12 cells. Cell. Mol. Neurobiol. 30, 1327-1333.
71. Moskalenko, S., Henry, D. O., Rosse, C., Mirey, G., Camonis, J. H. and White, M. A. (2002). The exocyst is a Ral effector complex. Nat. Cell Biol. 4, 66-72.
72. Myers, K. R. and Casanova, J. E. (2008). Regulation of actin cytoskeleton dynamics by Arf-family GTPases. Trends Cell Biol. 18, 184-192.
73. Nambiar, R., McConnell, R. E. and Tyska, M. J. (2009). Control of cell membrane tension by myosin-I. Proc. Natl. Acad. Sci. USA 106, 11972-11977.
74. Neubrand, V. E., Thomas, C., Schmidt, S., Debant, A. and Schiavo, G. (2010). Kidins220/ARMS regulates Rac1-dependent neurite outgrowth by direct interaction with the RhoGEF Trio. J. Cell Sci. 123, 2111-2123.
75. Nichols, B. (2009). Endocytosis of lipid-anchored proteins: excluding GEECs from the crowd. J. Cell Biol. 186, 457-459.
76. Nightingale, T. D., Cutler, D. F. and Cramer, L. P. (2012). Actin coats and rings promote regulated exocytosis. Trends Cell Biol. 22, 329-337.
77. Nightingale, T. D., White, I. J., Doyle, E. L., Turmaine, M., Harrison-Lavoie, K. J., Webb, K. F., Cramer, L. P. and Cutler, D. F. (2011). Actomyosin II contractility expels von Willebrand factor from Weibel-Palade bodies during exocytosis. J. Cell Biol. 194, 613-629.
78. Ohta, Y., Hartwig, J. H. and Stossel, T. P. (2006). FilGAP, a Rho- and ROCKregulated GAP for Rac binds filamin A to control actin remodelling. Nat. Cell Biol. 8, 803-814.
79. Omerovic, J., Laude, A. J. and Prior, I. A. (2007). Ras proteins: paradigms for compartmentalised and isoform-specific signalling. Cell. Mol. Life Sci. 64, 2575-2589.
80. Ory, S. and Gasman, S. (2011). Rho GTPases and exocytosis: what are the molecular links? Semin. Cell Dev. Biol. 22, 27-32.
81. Osmani, N., Peglion, F., Chavrier, P. and Etienne-Manneville, S. (2010). Cdc42 localization and cell polarity depend on membrane traffic. J. Cell Biol. 191, 1261-1269.
82. Otto, G. P. and Nichols, B. J. (2011). The roles of flotillin microdomains-endocytosis and beyond. J. Cell Sci. 124, 3933-3940.
83. Parrini, M. C., Sadou-Dubourgnoux, A., Aoki, K., Kunida, K., Biondini, M., Hatzoglou, A., Poullet, P., Formstecher, E., Yeaman, C., Matsuda, M. et al. (2011). SH3BP1, an exocyst-associated RhoGAP, inactivates Rac1 at the front to drive cell motility. Mol. Cell 42, 650-661.
84. Parsons, J. T., Horwitz, A. R. and Schwartz, M. A. (2010). Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat. Rev. Mol. Cell Biol. 11, 633-643.
85. Premkumar, L., Bobkov, A. A., Patel, M., Jaroszewski, L., Bankston, L. A., Stec, B., Vuori, K., Côté, J. F. and Liddington, R. C. (2010). Structural basis of membrane targeting by the Dock180 family of Rho family guanine exchange factors (Rho-GEFs). J. Biol. Chem. 285, 13211-13222.
86. Racchetti, G., D'Alessandro, R. and Meldolesi, J. (2012). Astrocyte stellation, a process dependent on Rac1 is sustained by the regulated exocytosis of enlargeosomes. Glia 60, 465-475.
87. Racchetti, G., Lorusso, A., Schulte, C., Gavello, D., Carabelli, V., D'Alessandro, R. and Meldolesi, J. (2010). Rapid neurite outgrowth in neurosecretory cells and neurons is sustained by the exocytosis of a cytoplasmic organelle, the enlargeosome. J. Cell Sci. 123, 165-170.
88. Rittmeyer, E. N., Daniel, S., Hsu, S. C. and Osman, M. A. (2008). A dual role for IQGAP1 in regulating exocytosis. J. Cell Sci. 121, 391-403.
89. Roberts-Galbraith, R. H. and Gould, K. L. (2010). Setting the F-BAR: functions and regulation of the F-BAR protein family. Cell Cycle 9, 4091-4097.
90. Saarikangas, J., Zhao, H. and Lappalainen, P. (2010). Regulation of the actin cytoskeleton-plasma membrane interplay by phosphoinositides. Physiol. Rev. 90, 259-289.
91. Sakisaka, T., Baba, T., Tanaka, S., Izumi, G., Yasumi, M. and Takai, Y. (2004). Regulation of SNAREs by tomosyn and ROCK: implication in extension and retraction of neurites. J. Cell Biol. 166, 17-25.
92. Sakurai-Yageta, M., Recchi, C., Le Dez, G., Sibarita, J. B., Daviet, L., Camonis, J., D'Souza-Schorey, C. and Chavrier, P. (2008). The interaction of IQGAP1 with the exocyst complex is required for tumor cell invasion downstream of Cdc42 and RhoA. J. Cell Biol. 181, 985-998.
93. Sandvig, K., Pust, S., Skotland, T. and van Deurs, B. (2011). Clathrin-independent endocytosis: mechanisms and function. Curr. Opin. Cell Biol. 23, 413-420.
94. Schwenger, D. B. and Kuner, T. (2010). Acute genetic perturbation of exocyst function in the rat calyx of Held impedes structural maturation, but spares synaptic transmission. Eur. J. Neurosci. 32, 974-984.
95. Sheetz, M. P., Sable, J. E. and Döbereiner, H. G. (2006). Continuous membranecytoskeleton adhesion requires continuous accommodation to lipid and cytoskeleton dynamics. Annu. Rev. Biophys. Biomol. Struct. 35, 417-434.
96. Shim, J., Lee, S. M., Lee, M. S., Yoon, J., Kweon, H. S. and Kim, Y. J. (2010). Rab35 mediates transport of Cdc42 and Rac1 to the plasma membrane during phagocytosis. Mol. Cell. Biol. 30, 1421-1433.
97. Sigismund, S., Confalonieri, S., Ciliberto, A., Polo, S., Scita, G. and Di Fiore, P. P. (2012). Endocytosis and signaling: cell logistics shape the eukaryotic cell plan. Physiol. Rev. 92, 273-366.
98. Spiczka, K. S. and Yeaman, C. (2008). Ral-regulated interaction between Sec5 and paxillin targets Exocyst to focal complexes during cell migration. J. Cell Sci. 121, 2880-2891.
99. Stenmark, H. (2009). Rab GTPases as coordinators of vesicle traffic. Nat. Rev. Mol. Cell Biol. 10, 513-525.
100. Stöckli, J., Fazakerley, D. J. and James, D. E. (2011). GLUT4 exocytosis. J. Cell Sci. 124, 4147-4159.
101. Stoeber, M., Stoeck, I. K., Hänni, C., Bleck, C. K., Balistreri, G. and Helenius, A. (2012). Oligomers of the ATPase EHD2 confine caveolae to the plasma membrane through association with actin. EMBO J. 31, 2350-2364.
102. Stratmann, H., Schwan, C., Orth, J. H., Schmidt, G. and Aktories, K. (2010). Pleiotropic role of Rac in mast cell activation revealed by a cell permeable Bordetella dermonecrotic fusion toxin. Cell. Signal. 22, 1124-1131.
103. Suetsugu, S. and Gautreau, A. (2012). Synergistic BAR-NPF interactions in actindriven membrane remodeling. Trends Cell Biol. 22, 141-150.
104. Sztul, E. and Lupashin, V. (2006). Role of tethering factors in secretory membrane traffic. Am. J. Physiol. Cell Physiol. 290, C11-C26.
105. Takabayashi, T., Xie, M. J., Takeuchi, S., Kawasaki, M., Yagi, H., Okamoto, M., Tariqur, R. M., Malik, F., Kuroda, K., Kubota, C. et al. (2010). LL5b directs the translocation of filamin A and SHIP2 to sites of phosphatidylinositol 3,4,5-triphosphate (PtdIns(3,4,5)P3) accumulation, and PtdIns(3,4,5)P3 localization is mutually modified by co-recruited SHIP2. J. Biol. Chem. 285, 16155-16165.
106. Takefuji, M., Mori, K., Morita, Y., Arimura, N., Nishimura, T., Nakayama, M., Hoshino, M., Iwamatsu, A., Murohara, T., Kaibuchi, K. et al. (2007). Rho-kinase modulates the function of STEF, a Rac GEF, through its phosphorylation. Biochem. Biophys. Res. Commun. 355, 788-794.
107. Tolias, K. F., Duman, J. G. and Um, K. (2011). Control of synapse development and plasticity by Rho GTPase regulatory proteins. Prog. Neurobiol. 94, 133-148.
108. Tsuji, T., Ishizaki, T., Okamoto, M., Higashida, C., Kimura, K., Furuyashiki, T., Arakawa, Y., Birge, R. B., Nakamoto, T., Hirai, H. et al. (2002). ROCK and mDia1 antagonize in Rho-dependent Rac activation in Swiss 3T3 fibroblasts. J. Cell Biol. 157, 819-830.
109. Verma, P., Ostermeyer-Fay, A. G. and Brown, D. A. (2010). Caveolin-1 induces formation of membrane tubules that sense actomyosin tension and are inhibited by polymerase I and transcript release factor/cavin-1. Mol. Biol. Cell 21, 2226-2240.
110. Vidal-Quadras, M., Gelabert-Baldrich, M., Soriano-Castell, D., Lladó, A., Rentero, C., Calvo, M., Pol, A., Enrich, C. and Tebar, F. (2011). Rac1 and calmodulin interactions modulate dynamics of ARF6-dependent endocytosis. Traffic 12, 1879-1896.
111. Villanueva, J., Torregrosa-Hetland, C. J., García-Martínez, V., Del Mar Francés, M., Viniegra, S. and Gutiérrez, L. M. (2012). The F-actin cortex in chromaffin granule dynamics and fusion: a minireview. J. Mol. Neurosci. 48, 323-327.
112. Vogel, V. and Sheetz, M. P. (2009). Cell fate regulation by coupling mechanical cycles to biochemical signaling pathways. Curr. Opin. Cell Biol. 21, 38-46.
113. Wang, C. C., Shi, H., Guo, K., Ng, C. P., Li, J., Gan, B. Q., Chien Liew, H., Leinonen, J., Rajaniemi, H., Zhou, Z. H. et al. (2007). VAMP8/endobrevin as a general vesicular SNARE for regulated exocytosis of the exocrine system. Mol. Biol. Cell 18, 1056-1063.
114. Wang, J. T., Kerr, M. C., Karunaratne, S., Jeanes, A., Yap, A. S. and Teasdale, R. D. (2010). The SNX-PX-BAR family in macropinocytosis: the regulation of macropinosome formation by SNX-PX-BAR proteins. PLoS ONE 5, e13763.
115. Wang, Z. and Thurmond, D. C. (2009). Mechanisms of biphasic insulin-granule exocytosis - roles of the cytoskeleton, small GTPases and SNARE proteins. J. Cell Sci. 122, 893-903.
116. White, D. T., McShea, K. M., Attar, M. A. and Santy, L. C. (2010). GRASP and IPCEF promote ARF-to-Rac signaling and cell migration by coordinating the association of ARNO/cytohesin 2 with Dock180. Mol. Biol. Cell 21, 562-571.
117. Wu, C., Agrawal, S., Vasanji, A., Drazba, J., Sarkaria, S., Xie, J., Welch, C.M., Liu, M., Anand-Apte, B. and Horowitz, A. (2011). Rab13-dependent trafficking of RhoA is required for directional migration and angiogenesis. J. Biol. Chem. 286, 23511-23520.
118. Wu, H., Rossi, G. and Brennwald, P. (2008). The ghost in the machine: small GTPases as spatial regulators of exocytosis. Trends Cell Biol. 18, 397-404.
119. Yamaguchi, Y., Katoh, H., Yasui, H., Mori, K. and Negishi, M. (2001). RhoA inhibits the nerve growth factor-induced Rac1 activation through Rho-associated kinasedependent pathway. J. Biol. Chem. 276, 18977-18983.
120. Yoshida, S., Hoppe, A. D., Araki, N. and Swanson, J. A. (2009). Sequential signaling in plasma-membrane domains during macropinosome formation in macrophages. J. Cell Sci. 122, 3250-3261.
121. Zuo, X., Zhang, J., Zhang, Y., Hsu, S. C., Zhou, D. and Guo, W. (2006). Exo70 interacts with the Arp2/3 complex and regulates cell migration. Nat. Cell Biol. 8, 1383-1388.