The actin cytoskeleton and neurotransmitter release: An overview

Biochimie

Volumn 82, Issue 4, 2000, Pages 353-363

  Doussau, Frédéric ^a   Augustine, George J ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; BINDING PROTEIN; GUANOSINE TRIPHOSPHATE; MYOSIN; NEUROTRANSMITTER; PROTEIN KINASE C; SPECTRIN; SYNAPSIN;

CYTOSKELETON; ENDOCYTOSIS; EXOCYTOSIS; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; REVIEW; SYNAPSE VESICLE;

EID: 0034045608     PISSN: 03009084     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0300-9084(00)00217-0     Document Type: Article

References (123)

1. Kabsch W., Vandekerckhove J. Structure and function of actin. Annu. Rev. Biophys. Biomol. Struct. 21:1992;49-76.
2. Schmidt A., Hall M.N. Signaling to the actin cytoskeleton. Annu. Rev. Cell. Dev. Biol. 14:1998;305-338.
3. Landis D.M., Hall A.K., Weinstein L.A., Reese T.S. The organization of cytoplasm at the presynaptic active zone of a central nervous system synapse. Neuron. 1:1988;201-209.
4. Hirokawa N., Sobue K., Kanda K., Harada A., Yorifuji H. The cytoskeletal architecture of the presynaptic terminal and molecular structure of synapsin 1. J. Cell. Biol. 108:1989;111-126.
5. Gotow T., Miyaguchi K., Hashimoto P.H. Cytoplasmic architecture of the axon terminal: filamentous strands specifically associated with synaptic vesicles. Neuroscience. 40:1991;587-598.
6. Gray E.G. Neurotransmitter release mechanisms and microtubules. Proc. R. Soc. Lond. B. Biol. Sci. 218:1983;253-258.
7. Walker J.H., Boustead C.M., Witzemann V., Shaw G., Weber K., Osborn M. Cytoskeletal proteins at the cholinergic synapse: distribution of desmin, actin, fodrin, neurofilaments, and tubulin in Torpedo electric organ. Eur. J. Cell Biol. 38:1985;123-133.
8. Drenckhahn D., Kaiser H.W. Evidence for the concentration of F-actin and myosin in synapses and in the plasmalemmal zone of axons. Eur. J. Cell Biol. 31:1983;235-240.
9. Bernstein B.W., Bamburg J.R. Cycling of actin assembly in synaptosomes and neurotransmitter release. Neuron. 3:1989;257-265.
10. Job C., Lagnado L. Calcium and protein kinase C regulate the actin cytoskeleton in the synaptic terminal of retinal bipolar cells. J. Cell Biol. 143:1998;1661-1672.
11. Bernstein B.W., Dewit M., Bamburg J.R. Actin disassembles reversibly during electrically induced recycling of synaptic vesicles in cultured neurons. Mol. Brain. Res. 53:1998;236-251.
12. Huttner W.B., Schiebler W., Greengard P., De Camilli P. Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J. Cell Biol. 96:1983;1374-1388.
13. Südhof T.C., Jahn R. Proteins of synaptic vesicles involved in exocytosis and membrane recycling. Neuron. 6:1991;665-677.
14. Takei Y., Harada A., Takeda S., Kobayashi K., Terada S., Noda T., Takahashi T., Hirokawa N. Synapsin I deficiency results in the structural change in the presynaptic terminals in the murine nervous system. J. Cell Biol. 131:1995;1789-1800.
15. Zagon I.S., Higbee R., Riederer B.M., Goodman S.R. Spectrin subtypes in mammalian brain: an immunoelectron microscopic study. J. Neurosci. 6:1986;2977-2986.
16. Goodman S.R., Zimmer W.E., Clark M.B., Zagon I.S., Barker J.E., Bloom M.L. Brain spectrin: of mice and men. Brain. Res. Bull. 36:1995;593-606.
17. Cases-Langhoff C., Voss B., Garner A.M., Appeltauer U., Takei K., Kindler S., Veh R.W., De Camilli P., Gundelfinger E.D., Garner C.C. Piccolo, a novel 420 kDa protein associated with the presynaptic cytomatrix. Eur. J. Cell Biol. 69:1996;214-223.
18. Fenster S.D., Chung W.J., Zhai R., Cases-Langhoff C., Voss B., Garner A.M., Kaempf U., Kindler S., Gundelfinger E.D., Garner C.C. Piccolo, a presynaptic zinc finger protein structurally related to Bassoon. Neuron. 23:2000;203-214.
19. Tom Dieck S., Sanmarti-Vila L., Langnaese K., Richter K., Kindler S., Soyke A., Wex H., Smalla K.H., Kampf U., Franzer J.T., Stumm M., Garner C.C., Gundelfinger E.D. Bassoon, a novel zinc-finger CAG/glutamine-repeat protein selectively localized at the active zone of presynaptic nerve terminals. J. Cell Biol. 142:1998;499-509.
20. Wang X., Kibschull M., Laue M.M., Lichte B., Petrasch-Parwez E., Kilimann M.W. Aczonin, a 550-kD putative scaffolding protein of presynaptic active zones, shares homology regions with rim and bassoon and binds profilin. J. Cell Biol. 147:1999;151-162.
21. Richter K., Langnaese K., Kreutz M.R., Olias G., Zhai R., Scheich H., Garner C.C., Gundelfinger E.D. Presynaptic cytomatrix protein bassoon is localized at both excitatory and inhibitory synapses of rat brain. J. Comp. Neurol. 408:1999;437-448.
22. Aunis D., Bader M.F. The cytoskeleton as a barrier to exocytosis in secretory cells. J. Exp. Biol. 139:1988;253-266.
23. Sontag J.M., Aunis D., Bader M.F. Peripheral actin filaments control calcium-mediated catecholamine release from streptolysin-O-permeabilized chromaffin cells. Eur. J. Cell Biol. 46:1988;316-326.
24. Trifaró J.M., Vitale M.L. Cytoskeleton dynamics during neurotransmitter release. Trends Neurosci. 16:1993;466-472.
25. Vitale M.L., Seward E.P., Trifaró J.M. Chromaffin cell cortical actin network dynamics control the size of the release-ready vesicle pool and the initial rate of exocytosis. Neuron. 14:1995;353-363.
26. Li G., Rungger-Brandle E., Just I., Jonas J.C., Aktories K., Wollheim C.B. Effect of disruption of actin filaments by Clostridium botulinum C2 toxin on insulin secretion in HIT-T15 cells and pancreatic islets. Mol. Biol. Cell. 5:1994;1199-1213.
27. Couteaux R., Pecot-Dechavassine M. Synaptic vesicles and pouches at the level of 'active zones' of the neuromuscular junction. C.R. Acad. Sci. (Paris). 271:1970;2346-2349.
28. Heuser J.E., Reese T.S., Dennis M.J., Jan Y., Jan L., Evans L. Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J. Cell Biol. 81:1979;275-300.
29. Wang X.H., Zheng J.Q., Poo M.M. Effects of cytochalasin treatment on short-term synaptic plasticity at developing neuromuscular junctions in frogs. J. Physiol. (Lond.). 491:1996;187-195.
30. Kuromi H., Kidokoro Y. Two distinct pools of synaptic vesicles in single presynaptic boutons in a temperature-sensitive Drosophila mutant, shibire. Neuron. 20:1998;917-925.
31. Almers W., Tse F.W. Transmitter release from synapses: does a preassembled fusion pore initiate exocytosis? Neuron. 4:1990;813-818.
32. Katz B., Miledi R. Suppression of transmitter release at the neuromuscular junction. Proc. R. Soc. Lond. B. Biol. Sci. 196:1977;465-469.
33. Schweizer F.E., Betz H., Augustine G.J. From vesicle docking to endocytosis: intermediate reactions of exocytosis. Neuron. 14:1995;689-696.
34. Bajjalieh S.M. Synaptic vesicle docking and fusion. Curr. Opin. Neurobiol. 9:1999;321-328.
35. Betz W.J. Depression of transmitter release at the neuromuscular junction of the frog. J. Physiol. (Lond.). 206:1970;629-644.
36. Kübler E., Riezman H. Actin and fimbrin are required for the internalization step of endocytosis in yeast. EMBO J. 12:1993;2855-2862.
37. Munn A.L., Stevenson B.J., Geli M.I., Riezman H. end5, end6, and end7: mutations that cause actin delocalization and block the internalization step of endocytosis in Saccharomyces cerevisiae. Mol. Biol. Cell. 6:1995;1721-1742.
38. Goodson H.V., Anderson B.L., Warrick H.M., Pon L.A., Spudich J.A. Synthetic lethality screen identifies a novel yeast myosin I gene (MYO5): myosin I proteins are required for polarization of the actin cytoskeleton. J. Cell Biol. 133:1996;1277-1291.
39. Geli M.I., Riezman H. Role of type I myosins in receptor-mediated endocytosis in yeast. Science. 272:1996;533-535.
40. Geli M.I., Riezman H. Endocytic internalization in yeast and animal cells: similar and different. J. Cell Sci. 111:1998;1031-1037.
41. Lamaze C., Fujimoto L.M., Yin H.L., Schmid S.L. The actin cytoskeleton is required for receptor-mediated endocytosis in mammalian cells. J. Biol. Chem. 272:1997;20332-20335.
42. Gottlieb T.A., Ivanov I.E., Adesnik M., Sabatini D.D. Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J. Cell Biol. 120:1993;695-710.
43. Jackman M.R., Shurety W., Ellis J.A., Luzio J.P. Inhibition of apical but not basolateral endocytosis of ricin and folate in Caco-2 cells by cytochalasin D. J. Cell Sci. 107:1994;2547-2556.
44. Merrifield C.J., Moss S.E., Ballestrem C., Imhof B.A., Giese G., Wunderlich I., Almers W. Endocytic vesicles move at the tips of actin tails in cultured mast cells. Nat. Cell Biol. 1:1999;72-74.
45. Frischknecht F., Cudmore S., Moreau V., Reckmann I., Rottger S., Way M. Tyrosine phosphorylation is required for actin-based motility of vaccinia but not Listeria or Shigella. Curr. Biol. 9:1999;89-92.
46. Schiebler W., Jahn R., Doucet J.P., Rothlein J., Greengard P. Characterization of synapsin I binding to small synaptic vesicles. J. Biol. Chem. 261:1986;8383-8390.
47. Südhof T.C., Czernik A.J., Kao H.T., Takei K., Johnston P.A., Horiuchi A., Kanazir S.D., Wagner M.A., Perin M.S., De Camilli P., Greengard P. Synapsins: mosaics of shared and individual domains in a family of synaptic vesicle phosphoproteins. Science. 245:1989;1474-1480.
48. Kao H.T., Porton B., Czernik A.J., Feng J., Yiu G., Haring M., Benfenati F., Greengard P. A third member of the synapsin gene family. Proc. Natl. Acad. Sci. USA. 95:1998;4667-4672.
49. Benfenati F., Valtorta F., Chieregatti E., Greengard P. Interaction of free and synaptic vesicle-bound synapsin I with F-actin. Neuron. 8:1992;377-386.
50. Valtorta F., Greengard P., Fesce R., Chieregatti E., Benfenati F. Effects of the neuronal phosphoprotein synapsin I on actin polymerization. I. Evidence for a phosphorylation-dependent nucleating effect. J. Biol. Chem. 267:1992;11281-11288.
51. Bähler M., Greengard P. Synapsin I bundles F-actin in a phosphorylation-dependent manner. Nature. 326:1987;704-707.
52. Petrucci T.C., Morrow J.S. Synapsin I: an actin-bundling protein under phosphorylation control. J. Cell Biol. 105:1987;1355-1363.
53. Bähler M., Benfenati F., Valtorta F., Czernik A.J., Greengard P. Characterization of synapsin I fragments produced by cysteine-specific cleavage: a study of their interactions with F-actin. J. Cell Biol. 108:1989;1841-1849.
54. Chilcote T.J., Siow Y.L., Schaeffer E., Greengard P., Thiel G. Synapsin IIa bundles actin filaments. J. Neurochem. 63:1994;1568-1571.
55. Chieregatti E., Ceccaldi P.E., Benfenati F., Valtorta F. Effects of synaptic vesicles on actin polymerization. FEBS Lett. 398:1996;211-216.
56. Pieribone V.A., Shupliakov O., Brodin L., Hilfiker-Rothenfluh S., Czernik A.J., Greengard P. Distinct pools of synaptic vesicles in neurotransmitter release. Nature. 375:1995;493-497.
57. Hilfiker S., Schweizer F.E., Kao H.T., Czernik A.J., Greengard P., Augustine G.J. Two sites of action for synapsin domain E in regulating neurotransmitter release. Nat. Neurosci. 1:1998;29-35.
58. Li L., Chin L.S., Shupliakov O., Brodin L., Sihra T.S., Hvalby O., Jensen V., Zheng D., Mc Namara J.O., Greengard P., Andersen P. Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin I-deficient mice. Proc. Natl. Acad. Sci. USA. 92:1995;9235-9239.
59. Rosahl T.W., Spillane D., Missler M., Herz J., Selig D.K., Wolff J.R., Hammer R.E., Malenka R.C., Sudhof T.C. Essential functions of synapsins I and II in synaptic vesicle regulation. Nature. 375:1995;488-493.
60. Benfenati F., Neyroz P., Bahler M., Masotti L., Greengard P. Time-resolved fluorescence study of the neuron-specific phosphoprotein synapsin I. Evidence for phosphorylation-dependent conformational changes. J. Biol. Chem. 265:1990;12584-12595.
61. Greengard P., Valtorta F., Czernik A.J., Benfenati F. Synaptic vesicle phosphoproteins and regulation of synaptic function. Science. 259:1993;780-785.
62. Llinas R., Mc Guinness T.L., Leonard C.S., Sugimori M., Greengard P. Intraterminal injection of synapsin I or calcium/calmodulin-dependent protein kinase II alters neurotransmitter release at the squid giant synapse. Proc. Natl. Acad. Sci. USA. 82:1985;3035-3039.
63. Esser L., Wang C.R., Hosaka M., Smagula C.S., Südhof T.C., Deisenhofer J. Synapsin I is structurally similar to ATP-utilizing enzymes. EMBO J. 17:1998;977-984.
64. 2+ regulation. J. Biol. Chem. 273:1998;1425-1429.
65. Schweizer F.E., Dresbach T., DeBello W.M., O'Connor V., Augustine G.J., Betz H. Regulation of neurotransmitter release kinetics by NSF. Science. 279:1998;1203-1206.
66. Mochida S., Kobayashi H., Matsuda Y., Yuda Y., Muramoto K., Nonomura Y. Myosin II is involved in transmitter release at synapses formed between rat sympathetic neurons in culture. Neuron. 13:1994;1131-1142.
67. 2+-dependent interaction with the synaptobrevin-synaptophysin complex. J. Cell Biol. 137:1997;1589-1601.
68. Ryan T.A. Inhibitors of myosin light chain kinase block synaptic vesicle pool mobilization during action potential firing. J. Neurosci. 19:1999;1317-1323.
69. Hasson T., Mooseker M.S. The growing family of myosin motors and their role in neurons and sensory cells. Curr. Opin. Neurobiol. 7:1997;615-623.
70. Mercer J.A., Seperack P.K., Strobel M.C., Copeland N.G., Jenkins N.A. Novel myosin heavy chain encoded by murine dilute coat colour locus. Nature. 349:1991;709-713.
71. Espreafico E.M., Cheney R.E., Matteoli M., Nascimento A.A., De Camilli P.V., Larson R.E., Mooseker M.S. Primary structure and cellular localization of chicken brain myosin-V (p190), an unconventional myosin with calmodulin light chains. J. Cell Biol. 1992;1541-1557.
72. Evans L.L., Lee A.J., Bridgman P.C., Mooseker M.S. Vesicle-associated brain myosin-V can be activated to catalyze actin-based transport. J. Cell. Sci. 111:1998;2055-2066.
73. Langford G.M., Molyneaux B.J. Myosin V in the brain: mutations lead to neurological defects. Brain Res. Rev. 28:1998;1-8.
74. Mehta A.D., Rock R.S., Rief M., Spudich J.A., Mooseker M.S., Cheney R.E. Myosin-V is a processive actin-based motor. Nature. 400:1999;590-593.
75. Kuznetsov S.A., Langford G.M., Weiss D.G. Actin-dependent organelle movement in squid axoplasm. Nature. 356:1992;722-725.
76. Tabb J.S., Molyneaux B.J., Cohen D.L., Kuznetsov S.A., Langford G.M. Transport of ER vesicles on actin filaments in neurons by myosin V. J. Cell. Sci. 111:1998;3221-3234.
77. rd.. Visualization of melanosome dynamics within wild-type and dilute melanocytes suggests a paradigm for myosin V function in vivo. J. Cell Biol. 143:1998;1899-1918.
78. Bridgman P.C. Myosin Va movements in normal and dilute-lethal axons provide support for a dual filament motor complex. J. Cell Biol. 146:1999;1045-1060.
79. Nascimento A.A.C., Cheney R.E., Tauhata S.B.F., Larson R.E., Mooseker M.S. Enzymatic characterization and functional domain mapping of brain myosin-V. J. Biol. Chem. 271:1996;17561-17569.
80. Costa M.C., Mani F., Santoro W. Jr., Espreafico E.M., Larson R.E. Brain myosin-V, a calmodulin-carrying myosin, binds to calmodulin-dependent protein kinase II and activates its kinase activity. J. Biol. Chem. 274:1999;15811-15819.
81. Sikorski A.F., Terlecki G., Zagon I.S., Goodman S.R. Synapsin I-mediated interaction of brain spectrin with synaptic vesicles. J. Cell Biol. 114:1991;313-318.
82. Perrin D., Langley O.K., Aunis D. Anti-alpha-fodrin inhibits secretion from permeabilized chromaffin cells. Nature. 326:1987;498-501.
83. Weber T., Zemelman B.V., Mc New J.A., Westermann B., Gmachl M., Parlati F., Sollner T.H., Rothman J.E. SNAREpins: minimal machinery for membrane fusion. Cell. 92:1998;759-772.
84. Prekeris R., Mayhew M.W., Cooper J.B., Terrian D.M. Identification and localization of an actin-binding motif that is unique to the epsilon isoform of protein kinase C and participates in the regulation of synaptic function. J. Cell Biol. 132:1996;77-90.
85. Vaughan P.F., Walker J.H., Peers C. The regulation of neurotransmitter secretion by protein kinase C. Mol. Neurobiol. 18:1998;125-155.
86. Hilfiker S., Augustine G.J. Regulation of synaptic vesicle fusion by protein kinase C. J. Physiol. (Lond.). 515:1999;1.
87. Betz A., Ashery U., Rickmann M., Augustin I., Neher E., Südhof T.C., Rettig J., Brose N. Munc is a presynaptic phorbol ester receptor that enhances neurotransmitter release. Neuron. 21:1998;123-136.
88. Gillis K.D., Mossner R., Neher E. Protein kinase C enhances exocytosis from chromaffin cells by increasing the size of the readily releasable pool of secretory granules. Neuron. 16:1996;1209-1220.
89. Stevens C.F., Sullivan J.M. Regulation of the readily releasable vesicle pool by protein kinase C. Neuron. 21:1998;885-893.
90. Yawo H. Protein kinase C potentiates transmitter release from the chick ciliary presynaptic terminal by increasing the exocytotic fusion probability. J. Physiol. (Lond.). 515:1999;169-180.
91. Novick P., Zerial M. The diversity of Rab proteins in vesicle transport. Curr. Opin. Cell. Biol. 9:1997;496-504.
92. Chavrier P., Goud B. The role of ARF and Rab GTPases in membrane transport. Curr. Opin. Cell. Biol. 11:1999;466-475.
93. Peranen J., Auvinen P., Virta H., Wepf R., Simons K. Rab8 promotes polarized membrane transport through reorganization of actin and microtubules in fibroblasts. J. Cell Biol. 135:1996;153-167.
94. Valentijn J.A., Lacivita D.Q., Gumkowski F.D., Jamieson J.D. Rab4 associates with the actin terminal web in developing rat pancreatic acinar cells. Eur. J. Cell Biol. 72:1997;1-8.
95. Echard A., Jollivet F., Martinez O., Lacapere J.J., Rousselet A., Janoueix-Lerosey I., Goud B. Interaction of a Golgi-associated kinesin-like protein with Rab6. Science. 279:1998;580-585.
96. Imamura H., Takaishi K., Nakano K., Kodama A., Oishi H., Shiozaki H., Monden M., Sasaki T., Takai Y. Rho and Rab small G proteins coordinately reorganize stress fibers and focal adhesions in MDCK cells. Mol. Biol. Cell. 9:1998;2561-2575.
97. Fischer Von Mollard G., Südhof T.C., Jahn R. A small GTP-binding protein dissociates from synaptic vesicles during exocytosis. Nature. 349:1991;79-81.
98. Burton J.L., Burns M.E., Gatti E., Augustine G.J., De Camilli P. Specific interactions of Mss4 with members of the Rab GTPase subfamily. EMBO J. 13:1994;5547-5558.
99. Johannes L., Doussau F., Clabecq A., Henry J.P., Darchen F., Poulain B. Evidence for a functional link between Rab3 and the SNARE complex. J. Cell. Sci. 109:1996;2875-2884.
100. Geppert M., Goda Y., Stevens C.F., Südhof T.C. The small GTP-binding protein Rab3A regulates a late step in synaptic vesicle fusion. Nature. 387:1997;810-814.
101. Doussau F., Clabecq A., Henry J.P., Darchen F., Poulain B. Calcium-dependent regulation of Rab3 in short-term plasticity. J. Neurosci. 18:1998;3147-3157.
102. Castillo P.E., Janz R., Südhof T.C., Tzounopoulos T., Malenka R.C., Nicoll R.A. Rab3A is essential for mossy fibre long-term potentiation in the hippocampus. Nature. 388:1997;590-593.
103. Stahl B., Chou J.H., Li C., Südhof T.C., Jahn R. Rab3 reversibly recruits rabphilin to synaptic vesicles by a mechanism analogous to raf recruitment by ras. EMBO J. 15:1996;1799-1809.
104. Burns M.E., Sasaki T., Takai Y., Augustine G.J. Rabphilin-3A: a multifunctional regulator of synaptic vesicle traffic. J. Gen. Physiol. 111:1998;243-255.
105. Kato M., Sasaki T., Ohya T., Nakanishi H., Nishioka H., Imamura M., Takai Y. Physical and functional interaction of rabphilin-3A with alpha-actinin. J. Biol. Chem. 271:1996;31775-31778.
106. 2+ and phosphatidylserine. Biochem. Biophys. Res. Commun. 205:1994;460-466.
107. Joberty G., Stabila P.F., Coppola T., Macara I.G., Regazzi R. High affinity rab3 binding is dispensable for rabphilin-dependent potentiation of stimulated secretion. J. Cell. Sci. 112:1999;3579-3587.
108. Schlüter O.M., Schnell E., Verhage M., Tzonopoulos T., Nicoll R.A., Janz R., Malenka R.C., Geppert M., Südhof T.C. Rabphilin knock-out mice reveal that rabphilin is not required for rab3 function in regulating neurotransmitter release. J. Neurosci. 19:1999;5834-5846.
109. Coppola T., Perret-Menoud V., Luthi S., Farnsworth C.C., Glomset J.A., Regazzi R. Disruption of Rab3-calmodulin interaction, but not other effector interactions, prevents rab3 inhibition of exocytosis. EMBO J. 18:1999;5885-5891.
110. Hall A. Rho GTPases and the actin cytoskeleton. Science. 279:1998;509-514.
111. Kaibuchi K., Kuroda S., Amano M. Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu. Rev. Biochem. 68:1999;459-486.
112. Prepens U., Just I., Von Eichel-Streiber C., Aktories K. Inhibition of Fc epsilon-RI-mediated activation of rat basophilic leukemia cells by Clostridium difficile toxin B. J. Biol. Chem. 271:1996;7324-7329.
113. Kowluru A., Li G., Rabaglia M.E., Segu V.B., Hofmann F., Aktories K., Metz S.A. Evidence for differential roles of the Rho subfamily of GTP-binding proteins in glucose- and calcium-induced insulin secretion from pancreatic beta cells. Biochem. Pharmacol. 54:1997;1097-1108.
114. Brown A.M., O' Sullivan A.J., Gomperts B.D. Induction of exocytosis from permeabilized mast cells by the guanosine triphosphatases Rac and Cdc42. Mol. Biol. Cell. 9:1998;1053-1063.
115. Gasman S., Chasserot-Golaz S., Popoff M.R., Aunis D., Bader M.F. Involvement of Rho GTPases in calcium-regulated exocytosis from adrenal chromaffin cells. J. Cell. Sci. 112:1999;4763-4771.
116. 2+-dependent neurotransmitter exocytosis. J. Biol. Chem. 275:2000;7764-7770.
117. Aspenström P. Effectors for the Rho GTPases. Curr. Opin. Cell. Biol. 11:1999;95-102.
118. De Camilli P., Emr S.D., Mc Pherson P.S., Novick P. Phosphoinositides as regulators in membrane traffic. Science. 271:1996;1533-1539.
119. Ayscough K.R. In vivo functions of actin-binding proteins. Curr. Opin. Cell. Biol. 10:1998;102-111.
120. Zhang L., Marcu M.G., Nau-Staudt K., Trifaro J.M. Recombinant scinderin enhances exocytosis, an effect blocked by two scinderin-derived actin-binding peptides and PIP2. Neuron. 17:1996;287-296.
121. Wang J.Y., Wigston D.J., Rees H.D., Levey A.I., Falls D.L. LIM kinase 1 accumulates in presynaptic terminals during synapse maturation. J. Comp. Neurol. 416:2000;319-334.
122. Arber S., Barbayannis F.A., Hanser H., Schneider C., Stanyon C.A., Bernard O., Caroni P. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature. 393:1998;805-809.
123. Yang N., Higuchi O., Ohashi K., Nagata K., Wada A., Kangawa K., Nishida E., Mizuno K. Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature. 393:1998;809-812.