How important are Rho GTPases in neurosecretion?

Journal of Neurochemistry

Volumn 117, Issue 4, 2011, Pages 623-631

  Momboisse, Fanny ^a   Houy, Sébastien ^a   Ory, Stéphane ^a   Calco, Valérie ^a   Bader, Marie France ^a   Gasman, Stéphane ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

calcium regulated exocytosis; chromaffin cells; neurons; neurotransmission; Rho GTPases

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR 6; PROTEIN CDC42; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

CHROMAFFIN CELL; HORMONE RELEASE; HUMAN; NERVE CELL PLASTICITY; NEUROSECRETION; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW;

ANIMALS; CHROMAFFIN SYSTEM; HUMANS; NEUROSECRETION; NEUROTRANSMITTER AGENTS; PC12 CELLS; RATS; RHO GTP-BINDING PROTEINS; SYNAPTIC TRANSMISSION;

EID: 79955005079     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2011.07241.x     Document Type: Review

References (100)

1. Albertinazzi C., Za L., Paris S., and, de Curtis I., (2003) ADP-ribosylation factor 6 and a functional PIX/p95-APP1 complex are required for Rac1B-mediated neurite outgrowth. Mol. Biol. Cell 14, 1295-1307. (Pubitemid 36547401)
2. Allen K. M., Gleeson J. G., Bagrodia S., Partington M. W., MacMillan J. C., Cerione R. A., Mulley J. C., and, Walsh C. A., (1998) PAK3 mutation in nonsyndromic X-linked mental retardation. Nat. Genet. 20, 25-30. (Pubitemid 28410338)
3. An S., and, Zenisek D., (2004) Regulation of exocytosis in neurons and neuroendocrine cells. Curr. Opin. Neurobiol. 14, 522-530. (Pubitemid 39349612)
4. Ashery U., Varoqueaux F., Voets T., Betz A., Thakur P., Koch H., Neher E., Brose N., and, Rettig J., (2000) Munc13-1 acts as a priming factor for large dense-core vesicles in bovine chromaffin cells. EMBO J. 19, 3586-3596. (Pubitemid 30462117)
5. Audebert S., Navarro C., Nourry C., et al. (2004) Mammalian scribble forms a tight complex with the betaPIX exchange factor. Curr. Biol. 14, 987-995. (Pubitemid 38722613)
6. Bader M. F., Holz R. W., Kumakura K., and, Vitale N., (2002) Exocytosis: the chromaffin cell as a model system. Ann. N Y Acad. Sci. 971, 178-183. (Pubitemid 35305291)
7. Bader M. F., Doussau F., Chasserot-Golaz S., Vitale N., and, Gasman S., (2004) Coupling actin and membrane dynamics during calcium-regulated exocytosis: a role for Rho and ARF GTPases. Biochim. Biophys. Acta 1742, 37-49. (Pubitemid 39601765)
8. Bagrodia S., Taylor S. J., Jordon K. A., Van Aelst L., and, Cerione R. A., (1998) A novel regulator of p21-activated kinases. J. Biol. Chem. 273, 23633-23636. (Pubitemid 28435688)
9. Begle A., Tryoen-Toth P., de Barry J., Bader M. F., and, Vitale N., (2009) ARF6 regulates the synthesis of fusogenic lipids for calcium-regulated exocytosis in neuroendocrine cells. J. Biol. Chem. 284, 4836-4845.
10. Billuart P., Bienvenu T., Ronce N., et al. (1998) Oligophrenin-1 encodes a rhoGAP protein involved in X-linked mental retardation. Nature 392, 923-926. (Pubitemid 28232063)
11. Bishop A. L., and, Hall A., (2000) Rho GTPases and their effector proteins. Biochem. J. 348 (Pt 2), 241-255. (Pubitemid 30345195)
12. Boquet P., (1999) Bacterial toxins inhibiting or activating small GTP-binding proteins. Ann. N Y Acad. Sci. 886, 83-90. (Pubitemid 30042425)
13. Boureux A., Vignal E., Faure S., and, Fort P., (2007) Evolution of the Rho family of ras-like GTPases in eukaryotes. Mol. Biol. Evol. 24, 203-216. (Pubitemid 46026295)
14. Burgoyne R. D., and, Morgan A., (2003) Secretory granule exocytosis. Physiol. Rev. 83, 581-632. (Pubitemid 36378679)
15. Cherfils J., and, Chardin P., (1999) GEFs: structural basis for their activation of small GTP-binding proteins. Trends Biochem. Sci. 24, 306-311. (Pubitemid 29366804)
16. Colicos M. A., Collins B. E., Sailor M. J., and, Goda Y., (2001) Remodeling of synaptic actin induced by photoconductive stimulation. Cell 107, 605-616. (Pubitemid 34014862)
17. Cotton M., Boulay P. L., Houndolo T., Vitale N., Pitcher J. A., and, Claing A., (2007) Endogenous ARF6 interacts with Rac1 upon angiotensin II stimulation to regulate membrane ruffling and cell migration. Mol. Biol. Cell 18, 501-511. (Pubitemid 46213219)
18. Daniel S., Noda M., Cerione R. A., and, Sharp G. W., (2002) A link between Cdc42 and syntaxin is involved in mastoparan-stimulated insulin release. Biochemistry 41, 9663-9671. (Pubitemid 34810041)
19. DerMardirossian C., and, Bokoch G. M., (2005) GDIs: central regulatory molecules in Rho GTPase activation. Trends Cell Biol. 15, 356-363. (Pubitemid 40943524)
20. Di Cesare A., Paris S., Albertinazzi C., Dariozzi S., Andersen J., Mann M., Longhi R., and, de Curtis I., (2000) p95-APP1 links membrane transport to Rac-mediated reorganization of actin. Nat. Cell Biol. 2, 521-530.
21. Diana G., Valentini G., Travaglione S., Falzano L., Pieri M., Zona C., Meschini S., Fabbri A., and, Fiorentini C., (2007) Enhancement of learning and memory after activation of cerebral Rho GTPases. Proc. Natl Acad. Sci. USA 104, 636-641. (Pubitemid 46123077)
22. Doussau F., and, Augustine G. J., (2000) The actin cytoskeleton and neurotransmitter release: an overview. Biochimie 82, 353-363. (Pubitemid 30391913)
23. Doussau F., Gasman S., Humeau Y., Vitiello F., Popoff M., Boquet P., Bader M. F., and, Poulain B., (2000) A Rho-related GTPase is involved in Ca(2 +)-dependent neurotransmitter exocytosis. J. Biol. Chem. 275, 7764-7770. (Pubitemid 30159681)
24. Doussau F., Humeau Y., Benfenati F., and, Poulain B., (2010) A novel form of presynaptic plasticity based on the fast reactivation of release sites switched off during low-frequency depression. J. Neurosci. 30, 16679-16691.
25. Etienne-Manneville S., and, Hall A., (2002) Rho GTPases in cell biology. Nature 420, 629-635. (Pubitemid 36764489)
26. Feig L. A., (1999) Tools of the trade: use of dominant-inhibitory mutants of Ras-family GTPases. Nat. Cell Biol. 1, E25-E27.
27. Feng Q., Albeck J. G., Cerione R. A., and, Yang W., (2002) Regulation of the Cool/Pix proteins: key binding partners of the Cdc42/Rac targets, the p21-activated kinases. J. Biol. Chem. 277, 5644-5650. (Pubitemid 34968619)
28. Ferraro F., Ma X. M., Sobota J. A., Eipper B. A., and, Mains R. E., (2007) Kalirin/Trio Rho guanine nucleotide exchange factors regulate a novel step in secretory granule maturation. Mol. Biol. Cell 18, 4813-4825. (Pubitemid 350246684)
29. Frangiskakis J. M., Ewart A. K., Morris C. A., et al. (1996) LIM-kinase1 hemizygosity implicated in impaired visuospatial constructive cognition. Cell 86, 59-69. (Pubitemid 26256578)
30. Frantz C., Coppola T., and, Regazzi R., (2002) Involvement of Rho GTPases and their effectors in the secretory process of PC12 cells. Exp. Cell Res. 273, 119-126. (Pubitemid 34920662)
31. Gasman S., Chasserot-Golaz S., Hubert P., Aunis D., and, Bader M. F., (1998) Identification of a potential effector pathway for the trimeric Go protein associated with secretory granules. Go stimulates a granule-bound phosphatidylinositol 4-kinase by activating RhoA in chromaffin cells. J. Biol. Chem. 273, 16913-16920. (Pubitemid 28311722)
32. Gasman S., Chasserot-Golaz S., Popoff M. R., Aunis D., and, Bader M. F., (1999) Involvement of Rho GTPases in calcium-regulated exocytosis from adrenal chromaffin cells. J. Cell Sci. 112 (Pt 24), 4763-4771. (Pubitemid 30034823)
33. Gasman S., Chasserot-Golaz S., Malacombe M., Way M., and, Bader M. F., (2004) Regulated exocytosis in neuroendocrine cells: a role for subplasmalemmal Cdc42/N-WASP-induced actin filaments. Mol. Biol. Cell 15, 520-531. (Pubitemid 38146470)
34. Gladycheva S. E., Lam A. D., Liu J., D'Andrea-Merrins M., Yizhar O., Lentz S. I., Ashery U., Ernst S. A., and, Stuenkel E. L., (2007) Receptor-mediated regulation of tomosyn-syntaxin 1A interactions in bovine adrenal chromaffin cells. J. Biol. Chem. 282, 22887-22899. (Pubitemid 47267375)
35. Gong L. W., Di Paolo G., Diaz E., Cestra G., Diaz M. E., Lindau M., De Camilli P., and, Toomre D., (2005) Phosphatidylinositol phosphate kinase type I gamma regulates dynamics of large dense-core vesicle fusion. Proc. Natl Acad. Sci. USA 102, 5204-5209.
36. Haditsch U., Leone D. P., Farinelli M., Chrostek-Grashoff A., Brakebusch C., Mansuy I. M., McConnell S. K., and, Palmer T. D., (2009) A central role for the small GTPase Rac1 in hippocampal plasticity and spatial learning and memory. Mol. Cell. Neurosci. 41, 409-419.
37. Hall A., (2005) Rho GTPases and the control of cell behaviour. Biochem. Soc. Trans. 33, 891-895. (Pubitemid 41659073)
38. Hall A., and, Lalli G., (2010) Rho and Ras GTPases in axon growth, guidance, and branching. Cold Spring Harb. Perspect. Biol. 2, a001818.
39. Hancock J. F., (2003) Ras proteins: different signals from different locations. Nat. Rev. Mol. Cell Biol. 4, 373-384. (Pubitemid 36565569)
40. Harada A., Furuta B., Takeuchi K., Itakura M., Takahashi M., and, Umeda M., (2000) Nadrin, a novel neuron-specific GTPase-activating protein involved in regulated exocytosis. J. Biol. Chem. 275, 36885-36891. (Pubitemid 32002101)
41. Harris B. Z., and, Lim W. A., (2001) Mechanism and role of PDZ domains in signaling complex assembly. J. Cell Sci. 114, 3219-3231. (Pubitemid 32998900)
42. Hata Y., Nakanishi H., and, Takai Y., (1998) Synaptic PDZ domain-containing proteins. Neurosci. Res. 32, 1-7. (Pubitemid 28495575)
43. 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.
44. Humeau Y., Vitale N., Chasserot-Golaz S., Dupont J. L., Du G., Frohman M. A., Bader M. F., and, Poulain B., (2001) A role for phospholipase D1 in neurotransmitter release. Proc. Natl Acad. Sci. USA 98, 15300-15305. (Pubitemid 34014009)
45. Humeau Y., Popoff M. R., Kojima H., Doussau F., and, Poulain B., (2002) Rac GTPase plays an essential role in exocytosis by controlling the fusion competence of release sites. J. Neurosci. 22, 7968-7981. (Pubitemid 35379102)
46. Jackson C., Welch H. C., and, Bellamy T. C., (2010) Control of cerebellar long-term potentiation by P-Rex-family guanine-nucleotide exchange factors and phosphoinositide 3-kinase. PLoS ONE 5, e11962.
47. Jayaram B., Syed I., Kyathanahalli C. N., Rhodes C. J., and, Kowluru A., (2011) Arf nucleotide binding site opener [ARNO] promotes sequential activation of Arf6, Cdc42 and Rac1 and insulin secretion in INS 832/13 beta-cells and rat islets. Biochem. Pharmacol. 81, 1016-1027.
48. Khelfaoui M., Denis C., van Galen E., et al. (2007) Loss of X-linked mental retardation gene oligophrenin1 in mice impairs spatial memory and leads to ventricular enlargement and dendritic spine immaturity. J. Neurosci. 27, 9439-9450. (Pubitemid 47358207)
49. Khelfaoui M., Pavlowsky A., Powell A. D., Valnegri P., Cheong K. W., Blandin Y., Passafaro M., Jefferys J. G., Chelly J., and, Billuart P., (2009) Inhibition of RhoA pathway rescues the endocytosis defects in Oligophrenin1 mouse model of mental retardation. Hum. Mol. Genet. 18, 2575-2583.
50. Koh C. G., (2006) Rho GTPases and their regulators in neuronal functions and development. Neurosignals 15, 228-237.
51. Kutsche K., Yntema H., Brandt A., et al. (2000) Mutations in ARHGEF6, encoding a guanine nucleotide exchange factor for Rho GTPases, in patients with X-linked mental retardation. Nat. Genet. 26, 247-250.
52. Lackner M. R., Nurrish S. J., and, Kaplan J. M., (1999) Facilitation of synaptic transmission by EGL-30 Gqalpha and EGL-8 PLCbeta: DAG binding to UNC-13 is required to stimulate acetylcholine release. Neuron 24, 335-346. (Pubitemid 29508408)
53. Lam A. D., Tryoen-Toth P., Tsai B., Vitale N., and, Stuenkel E. L., (2008) SNARE-catalyzed fusion events are regulated by Syntaxin1A-lipid interactions. Mol. Biol. Cell 19, 485-497. (Pubitemid 351272138)
54. Li Q., Ho C. S., Marinescu V., Bhatti H., Bokoch G. M., Ernst S. A., Holz R. W., and, Stuenkel E. L., (2003) Facilitation of Ca(2+)-dependent exocytosis by Rac1-GTPase in bovine chromaffin cells. J. Physiol. 550, 431-445. (Pubitemid 36889304)
55. Liu L., Liao H., Castle A., Zhang J., Casanova J., Szabo G., and, Castle D., (2005) SCAMP2 interacts with Arf6 and phospholipase D1 and links their function to exocytotic fusion pore formation in PC12 cells. Mol. Biol. Cell 16, 4463-4472. (Pubitemid 41416433)
56. Lonart G., Schoch S., Kaeser P. S., Larkin C. J., Sudhof T. C., and, Linden D. J., (2003) Phosphorylation of RIM1alpha by PKA triggers presynaptic long-term potentiation at cerebellar parallel fiber synapses. Cell 115, 49-60. (Pubitemid 37255317)
57. Mains R. E., Alam M. R., Johnson R. C., Darlington D. N., Back N., Hand T. A., and, Eipper B. A., (1999) Kalirin, a multifunctional PAM COOH-terminal domain interactor protein, affects cytoskeletal organization and ACTH secretion from AtT-20 cells. J. Biol. Chem. 274, 2929-2937. (Pubitemid 29075380)
58. Malacombe M., Bader M. F., and, Gasman S., (2006a) Exocytosis in neuroendocrine cells: new tasks for actin. Biochim. Biophys. Acta 1763, 1175-1183. (Pubitemid 44779865)
59. Malacombe M., Ceridono M., Calco V., Chasserot-Golaz S., McPherson P. S., Bader M. F., and, Gasman S., (2006b) Intersectin-1L nucleotide exchange factor regulates secretory granule exocytosis by activating Cdc42. EMBO J. 25, 3494-3503. (Pubitemid 44264860)
60. Manser E., Loo T. H., Koh C. G., Zhao Z. S., Chen X. Q., Tan L., Tan I., Leung T., and, Lim L., (1998) PAK kinases are directly coupled to the PIX family of nucleotide exchange factors. Mol. Cell 1, 183-192. (Pubitemid 128378659)
61. McMullan R., Hiley E., Morrison P., and, Nurrish S. J., (2006) Rho is a presynaptic activator of neurotransmitter release at pre-existing synapses in C. elegans. Genes Dev. 20, 65-76. (Pubitemid 43042668)
62. Meng Y., Zhang Y., Tregoubov V., et al. (2002) Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice. Neuron 35, 121-133. (Pubitemid 34804327)
63. Meng J., Meng Y., Hanna A., Janus C., and, Jia Z., (2005) Abnormal long-lasting synaptic plasticity and cognition in mice lacking the mental retardation gene Pak3. J. Neurosci. 25, 6641-6650. (Pubitemid 40995296)
64. Meyer M. Z., Deliot N., Chasserot-Golaz S., Premont R. T., Bader M. F., and, Vitale N., (2006) Regulation of neuroendocrine exocytosis by the ARF6 GTPase-activating protein GIT1. J. Biol. Chem. 281, 7919-7926. (Pubitemid 43847408)
65. Milosevic I., Sorensen J. B., Lang T., Krauss M., Nagy G., Haucke V., Jahn R., and, Neher E., (2005) Plasmalemmal phosphatidylinositol-4, 5-bisphosphate level regulates the releasable vesicle pool size in chromaffin cells. J. Neurosci. 25, 2557-2565. (Pubitemid 40365167)
66. 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.
67. 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 beta-Pix control calcium-regulated exocytosis in neuroendocrine PC12 cells. Cell. Mol. Neurobiol. 30, 1327-1333.
68. Nadif Kasri N., Nakano-Kobayashi A., Malinow R., Li B., and, Van Aelst L., (2009) The Rho-linked mental retardation protein oligophrenin-1 controls synapse maturation and plasticity by stabilizing AMPA receptors. Genes Dev. 23, 1289-1302.
69. Nakano-Kobayashi A., Kasri N. N., Newey S. E., and, Van Aelst L., (2009) The Rho-linked mental retardation protein OPHN1 controls synaptic vesicle endocytosis via endophilin A1. Curr. Biol. 19, 1133-1139.
70. Nevins A. K., and, Thurmond D. C., (2005) A direct interaction between Cdc42 and vesicle-associated membrane protein 2 regulates SNARE-dependent insulin exocytosis. J. Biol. Chem. 280, 1944-1952.
71. O'Kane E. M., Stone T. W., and, Morris B. J., (2004) Increased long-term potentiation in the CA1 region of rat hippocampus via modulation of GTPase signalling or inhibition of Rho kinase. Neuropharmacology 46, 879-887. (Pubitemid 38368920)
72. Palacios F., and, D'Souza-Schorey C., (2003) Modulation of Rac1 and ARF6 activation during epithelial cell scattering. J. Biol. Chem. 278, 17395-17400. (Pubitemid 36799625)
73. Pang Z. P., and, Sudhof T. C., (2010) Cell biology of Ca2 + -triggered exocytosis. Curr. Opin. Cell Biol. 22, 496-505.
74. Pasteris N. G., Cadle A., Logie L. J., Porteous M. E., Schwartz C. E., Stevenson R. E., Glover T. W., Wilroy R. S., and, Gorski J. L., (1994) Isolation and characterization of the faciogenital dysplasia (Aarskog-Scott syndrome) gene: a putative Rho/Rac guanine nucleotide exchange factor. Cell 79, 669-678.
75. Powell C. M., Schoch S., Monteggia L., Barrot M., Matos M. F., Feldmann N., Sudhof T. C., and, Nestler E. J., (2004) The presynaptic active zone protein RIM1alpha is critical for normal learning and memory. Neuron 42, 143-153. (Pubitemid 38456974)
76. Powner D. J., Hodgkin M. N., and, Wakelam M. J., (2002) Antigen-stimulated activation of phospholipase D1b by Rac1, ARF6, and PKCalpha in RBL-2H3 cells. Mol. Biol. Cell 13, 1252-1262. (Pubitemid 34309620)
77. Premont R. T., Perry S. J., Schmalzigaug R., Roseman J. T., Xing Y., and, Claing A., (2004) The GIT/PIX complex: an oligomeric assembly of GIT family ARF GTPase-activating proteins and PIX family Rac1/Cdc42 guanine nucleotide exchange factors. Cell. Signal. 16, 1001-1011. (Pubitemid 38798051)
78. Qualmann B., and, Mellor H., (2003) Regulation of endocytic traffic by Rho GTPases. Biochem. J. 371, 233-241. (Pubitemid 36547606)
79. Richnau N., and, Aspenstrom P., (2001) Rich, a rho GTPase-activating protein domain-containing protein involved in signaling by Cdc42 and Rac1. J. Biol. Chem. 276, 35060-35070.
80. Ridley A. J., (2001) Rho family proteins: coordinating cell responses. Trends Cell Biol. 11, 471-477. (Pubitemid 33079138)
81. Ridley A. J., (2006) Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol. 16, 522-529. (Pubitemid 44444995)
82. Ridley A. J., and, Hall A., (1992a) Distinct patterns of actin organization regulated by the small GTP-binding proteins Rac and Rho. Cold Spring Harb. Symp. Quant. Biol. 57, 661-671.
83. Ridley A. J., and, Hall A., (1992b) The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399.
84. Ridley A. J., Paterson H. F., Johnston C. L., Diekmann D., and, Hall A., (1992) The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70, 401-410.
85. Roberts P. J., Mitin N., Keller P. J., Chenette E. J., Madigan J. P., Currin R. O., Cox A. D., Wilson O., Kirschmeier P., and, Der C. J., (2008) Rho Family GTPase modification and dependence on CAAX motif-signaled posttranslational modification. J. Biol. Chem. 283, 25150-25163.
86. Rohatgi R., Ma L., Miki H., Lopez M., Kirchhausen T., Takenawa T., and, Kirschner M. W., (1999) The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97, 221-231.
87. 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. (Pubitemid 38931913)
88. Sankaranarayanan S., Atluri P. P., and, Ryan T. A., (2003) Actin has a molecular scaffolding, not propulsive, role in presynaptic function. Nat. Neurosci. 6, 127-135. (Pubitemid 36182781)
89. Santy L. C., and, Casanova J. E., (2001) Activation of ARF6 by ARNO stimulates epithelial cell migration through downstream activation of both Rac1 and phospholipase D. J. Cell Biol. 154, 599-610. (Pubitemid 34286164)
90. Soderling S. H., Langeberg L. K., Soderling J. A., Davee S. M., Simerly R., Raber J., and, Scott J. D., (2003) Loss of WAVE-1 causes sensorimotor retardation and reduced learning and memory in mice. Proc. Natl Acad. Sci. USA 100, 1723-1728. (Pubitemid 36254515)
91. Sorokina E. M., and, Chernoff J., (2005) Rho-GTPases: new members, new pathways. J. Cell. Biochem. 94, 225-231. (Pubitemid 41420300)
92. Symons M., and, Rusk N., (2003) Control of vesicular trafficking by Rho GTPases. Curr. Biol. 13, R409-R418. (Pubitemid 36573246)
93. Tudor E. L., Perkinton M. S., Schmidt A., et al. (2005) ALS2/Alsin regulates Rac-PAK signaling and neurite outgrowth. J. Biol. Chem. 280, 34735-34740. (Pubitemid 41504606)
94. Udo H., Jin I., Kim J. H., Li H. L., Youn T., Hawkins R. D., Kandel E. R., and, Bailey C. H., (2005) Serotonin-induced regulation of the actin network for learning-related synaptic growth requires Cdc42, N-WASP, and PAK in Aplysia sensory neurons. Neuron 45, 887-901. (Pubitemid 40395267)
95. Vitale N., Chasserot-Golaz S., and, Bader M. F., (2002) Regulated secretion in chromaffin cells: an essential role for ARF6-regulated phospholipase D in the late stages of exocytosis. Ann. N Y Acad. Sci. 971, 193-200. (Pubitemid 35305293)
96. Westerink R. H., and, Ewing A. G., (2008) The PC12 cell as model for neurosecretion. Acta Physiol. (Oxf) 192, 273-285. (Pubitemid 351160990)
97. Xin X., Ferraro F., Back N., Eipper B. A., and, Mains R. E., (2004) Cdk5 and Trio modulate endocrine cell exocytosis. J. Cell Sci. 117, 4739-4748. (Pubitemid 39433440)
98. Yin H. L., and, Janmey P. A., (2003) Phosphoinositide regulation of the actin cytoskeleton. Annu. Rev. Physiol. 65, 761-789. (Pubitemid 38249176)
99. Zhang Y., and, Kubiseski T. J., (2010) Caenorhabditis elegans wsp-1 regulation of synaptic function at the neuromuscular junction. J. Biol. Chem. 285, 23040-23046.
100. Zhao Z. S., Manser E., Loo T. H., and, Lim L., (2000) Coupling of PAK-interacting exchange factor PIX to GIT1 promotes focal complex disassembly. Mol. Cell. Biol. 20, 6354-6363. (Pubitemid 30650222)