Coupling actin and membrane dynamics during calcium-regulated exocytosis: A role for Rho and ARF GTPases

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1742, Issue 1-3, 2004, Pages 37-49

  Bader, Marie France ^a   Doussau, Frédéric ^a   Chasserot Golaz, Sylvette ^a   Vitale, Nicolas ^a   Gasman, Stéphane ^a  

^a CNRS   (France)

Author keywords

Actin; ARF; Chromaffin cell; Exocytosis; Lipid; Neuron; Rho

Indexed keywords

ACTIN; ARF PROTEIN; GUANOSINE TRIPHOSPHATASE; HYBRID PROTEIN; PROTEIN DERIVATIVE; RHO FACTOR;

CALCIUM TRANSPORT; CELL MEMBRANE; CONFERENCE PAPER; CROSS COUPLING REACTION; EXOCYTOSIS; FLUORESCENCE ANALYSIS; LIPID MEMBRANE; MOLECULAR BIOLOGY; MOLECULAR INTERACTION; MOLECULAR MECHANICS; MUTATIONAL ANALYSIS; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS;

ACTINS; ADP-RIBOSYLATION FACTORS; ANIMALS; CALCIUM; EXOCYTOSIS; GTP PHOSPHOHYDROLASES; HUMANS; RHO FACTOR; SIGNAL TRANSDUCTION;

EUKARYOTA;

EID: 10044225690     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2004.09.028     Document Type: Conference Paper

References (131)

1. W.J. Strittmatter Molecular mechanisms of exocytosis: the adrenal chromaffin cell as a model system Cell. Mol. Neurobiol. 8 1988 19 25
2. R. Jahn, and T.C. Sudhof Synaptic vesicles and exocytosis Annu. Rev. Neurosci. 17 1994 219 246
3. R.D. Burgoyne, and A. Morgan Analysis of regulated exocytosis in adrenal chromaffin cells: insights into NSF/SNAP/SNARE function BioEssays 20 1998 328 335
4. T.F. Martin Prime movers of synaptic vesicle exocytosis Neuron 34 2002 9 12
5. 2+-triggered exocytosis Science 298 2002 781 785
6. V.N. Murthy, and P. De Camilli Cell biology of the presynaptic terminal Annu. Rev. Neurosci. 26 2003 701 728
7. D. Aunis, and M.F. Bader The cytoskeleton as a barrier to exocytosis in secretory cells J. Exp. Biol. 139 1988 253 266
8. M.L. Vitale, E.P. Seward, and J.M. Trifaro 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
9. J.M. Trifaro, M. Glavinovic, and S.D. Rose Secretory vesicle pools and rate and kinetics of single vesicle exocytosis in neurosecretory cells Neurochem. Res. 22 1997 831 841
10. J.A. Steyer, H. Horstmann, and W. Almers Transport, docking and exocytosis of single secretory granules in live chromaffin cells Nature 388 1997 474 478
11. T. Voets, E. Neher, and T. Moser Mechanisms underlying phasic and sustained secretion in chromaffin cells from mouse adrenal slices Neuron 23 1999 607 615
12. F. Doussau, and G.J. Augustine The actin cytoskeleton and neurotransmitter release: an overview Biochimie 82 2000 353 363
13. M.A. Bittner, and R.W. Holz Kinetic analysis of secretion from permeabilized adrenal chromaffin cells reveals distinct components J. Biol. Chem. 267 1992 16219 16225
14. V.A. Klenchin, and T.J.F. Martin Priming in exocytosis: attaining fusion-competence after vesicle docking Biochimie 82 2000 399 407
15. R.B. Sutton, D. Fasshauer, R. Jahn, and A.T. Brunger Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution Nature 395 1998 347 353
16. Y.A. Chen, and R.H. Scheller SNARE-mediated membrane fusion Nat. Rev., Mol. Cell Biol. 2 2001 98 106
17. U. Ashery, F. Varoqueaux, T. Voets, A. Betz, P. Thakur, H. Koch, E. Neher, N. Brose, and J. Rettig Munc13-1 acts as a priming factor for large dense-core vesicles in bovine chromaffin cells EMBO J. 19 2000 3586 3596
18. R.N. Grishanin, J.A. Kowalchyk, V.A. Klenchin, K. Ann, C.A. Earles, E.R. Chapman, R.R.L. Gerona, and T.F.J. Martin CAPS acts at a prefusion step in dense-core vesicle exocytosis as a PIP2 binding protein Neuron 43 2004 551 562
19. J.A. Szule, and J.R. Coorssen Revisiting the role of SNAREs in exocytosis and membrane fusion Biochim. Biophys. Acta 1641 2003 121 135
20. A. Mayer What drives membrane fusion in eukaryotes? Trends Biochim. Sci. 26 2001 717 723
21. J. Zimmerberg, and L.V. Chernomordik Membrane fusion Adv. Drug Deliv. Rev. 38 1999 197 205
22. D.P. Siegel The modified stalk mechanism of lamellar/inverted phase transitions and its implications for membrane fusion Biophys. J. 76 1999 291 313
23. L.V. Chernomordik, and M.M. Kozlov Protein-lipid interplay in fusion and fission of biological membranes Annu. Rev. Biochem. 72 2003 175 207
24. C. Salaün, D.J. James, and L.H. Chamberlain Lipid rafts and the regulation of exocytosis Traffic 5 2004 255 264
25. G. Eitzen Actin remodeling to facilitate membrane fusion Biochim. Biophys. Acta 1641 2003 175 181
26. L. Orci, K.H. Gabbay, and W.J. Malaisse Pancreatic beta-cell web: its possible role in insulin secretion Science 175 1972 1128 1130
27. P.H. Cooke, and A.M. Poisner The role of cytoskeleton in adreno-medullary secretion Methods Achiev. Exp. Pathol. 9 1979 137 146
28. E. Fifkova, and R.J. Delay Cytoplasmic actin in neuronal processes as a possible mediator of synaptic plasticity J. Cell Biol. 95 1982 345 350
29. A. Koffer, P.E.R. Tatham, and B.D. Gomperts Changes in the state of actin during the exocytotic reaction of permeabilized rat mast cells J. Cell Biol. 111 1990 919 927
30. T. Lang, I. Wacker, I. Wunderlich, A. Rohrbach, G. Giese, T. Soldati, and W. Almers Role of actin cortex in the subplasmalemmal transport of secretory granules in PC12 cells Biophys. J. 78 2000 2863 2877
31. S. Gasman, S. Chasserot-Golaz, M. Malacombe, M. Way, and M.F. Bader Regulated exocytosis in neuroendocrine cells: a role for subplasmalemmal Cdc42/N-WASP-induced actin filaments Mol. Biol. Cell 15 2004 520 531
32. M.G. Roth Snapshots of ARF1: implications for mechanisms of activation and inactivation Cell 97 1999 149 152
33. J. Donaldson Multiple roles for ARF6: sorting, structuring and signaling at the plasma membrane J. Biol. Chem. 278 2003 41546 41573
34. A. Hall Rho GTPases and the actin cytoskeleton Science 279 1998 509 514
35. J.R. Whyte, and S. Munro Vesicle tethering complexes in membrane traffic J. Cell. Sci. 115 2002 2627 2637
36. T. Dresbach, B. Qualmann, M.M. Kessels, C.C. Garner, and E.D. Gundelfinger The presynaptic cytomatrix of brain synapses Cell. Mol. Life Sci. 58 2001 94 116
37. E.D. Gundelfinger, M.M. Kessels, and B. Qualmann Temporal and spatial coordination of exocytosis and endocytosis Nat. Rev. 4 2003 127 139
38. M. Rupnik, G.J. Law, A.J. Northrop, W.T. Mason, and R. Zorec Brefeldin A and a synthetic peptide to ADP-ribosylation factor (ARF) inhibit regulated exocytosis in melanotrophs NeuroReport 6 1995 853 856
39. C.Z. Yang, and M. Mueckler ADP-ribosylation factor 6 (ARF6) defines two insulin-regulated secretory pathways in adipocytes J. Biol. Chem. 274 1999 25297 25300
40. J.L. Rosales, and J.D. Ernst GTP-dependent permeabilized neutrophil secretion requires a freely diffusible cytosolic protein J. Cell. Biochem. 80 2000 37 45
41. S. Cockcroft, G. Way, N. O'Luanaigh, R. Pardo, E. Sarri, and A. Fensome Signalling role for ARF and phospholipase D in mast cell exocytosis stimulated by cross-linking of the high affinity Fc epsilon R1 receptor Mol. Immunol. 38 2002 1277 1284
42. J. Matsukawa, K. Nakayama, T. Nagao, H. Ichijo, and T. Urushidani Role of ADP-ribosylation factor 6 (ARF6) in gastric acid secretion J. Biol. Chem. 278 2003 36470 36475
43. J.T.R. Lauwrence, and M.J. Birnbaum ADP-ribosylation factor 6 regulates insulin secretion through plasma membrane phosphatidylinositol 4,5-bisphosphate Proc. Natl. Acad. Sci. U. S. A. 100 2003 13320 13325
44. A.S. Caumont, M.C. Galas, N. Vitale, D. Aunis, and M.F. Bader Regulated exocytosis in chromaffin cells: translocation of ARF6 stimulates a plasma membrane-associated phospholipase D J. Biol. Chem. 273 1998 1373 1379
45. N. Vitale, S. Chasserot-Golaz, Y. Bailly, N. Morinaga, M.A. Frohman, and M.F. Bader Calcium-regulated exocytosis of dense core vesicles requires the activation of ARF6 by ARNO at the plasma membrane J. Cell Biol. 159 2002 79 89
46. A.S. Caumont, N. Vitale, M. Gensse, M.C. Galas, J.E. Casanova, and M.F. Bader Identification of a plasma membrane-associated guanine nucleotide exchange factor for ARF6 in chromaffin cells: possible role in the regulated exocytotic pathway J. Biol. Chem. 275 2000 15637 15644
47. D. Jones, C. Morgan, and S. Cockcroft Phospholipase D and membrane traffic. Potential roles in regulated exocytosis, membrane delivery and vesicle budding Biochim. Biophys. Acta 1439 1999 229 244
48. N. Vitale, A.S. Caumont, S. Chasserot-Golaz, G. Du, S. Wu, V.A. Sciorra, A.J. Morris, M.A. Frohman, and M.F. Bader Phospholipase D1: a key factor for the exocytotic machinery in neuroendocrine cells EMBO J. 20 2001 2424 2434
49. W.S. Choi, Y.M. Kim, C. Combs, M.A. Frohman, and M.A. Beaven Phospholipases D1 and D2 regulate different phases of exocytosis in mast cells J. Immunol. 168 2002 5682 5689
50. A. Honda, M. Nagomi, T. Yokozeki, M. Yamasaki, H. Nakamura, H. Watanabe, K. Kawamoto, K. Nakayama, A.J. Morris, M.A. Frohman, and Y. Kanaho Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation Cell 99 1999 521 532
51. H.L. Yin, and P.A. Janmey Phosphoinositide regulation of the actin cytoskeleton Annu. Rev. Physiol. 65 2003 761 789
52. O. Cremona, and P. De Camilli Phosphoinositides in membrane traffic at the synapse J. Cell. Sci. 114 2001 1041 1052
53. S. Cockcroft, and M.A. De Matteis Inositol lipids as spatial regulators of membrane traffic J. Membr. Biol. 180 2001 187 194
54. J.C. Hay, P.L. Fisette, G.H. Jenkins, K. Fukami, T. Takenawa, R.A. Anderson, and T.F.J. Martin ATP-dependent inositide phosphorylation required for calcium-activated secretion Nature 374 1995 173 177
55. R.W. Holz, M.D. Hlubek, S.D. Sorensen, S.K. Fisher, T. Balla, S. Ozaki, G.D. Prestwich, E.L. Stuenkel, and M.A. Bittner A pleckstrin homology domain specific for phosphatidylinositol 4, 5-bisphosphate (PtdIns-4,5-P2) and fused to green fluorescent protein identifies plasma membrane PtdIns-4,5-P2 as being important in exocytosis J. Biol. Chem. 275 2000 17878 17885
56. Y. Aikawa, and T.J.F. Martin ARF6 regulates a plasma membrane pool of phosphatidyl(4,5)bisphosphate required for regulated exocytosis J. Cell Biol. 162 2003 647 659
57. F.D. Brown, A.L. Rozelle, H.L. Yin, T. Balla, and J.G. Donaldson Phosphatidylinositol 4,5-bisphosphate and Arf6-regulated membrane traffic J. Cell Biol. 154 2001 1007 1017
58. S. Gasman, S. Chasserot-Golaz, M.R. Popoff, D. Aunis, and M.F. Bader Involvement of Rho GTPases in calcium-regulated exocytosis from adrenal chromaffin cells J. Cell. Sci. 112 1999 4763 4771
59. 3 bound to the plasma membrane Eur. J. Neurosci. 8 1996 1275 1285
60. S. Gasman, S. Chasserot-Golaz, M.R. Popoff, D. Aunis, and M.F. Bader Trimeric G proteins control exocytosis in chromaffin cells: Go regulates the peripheral actin network and catecholamine secretion by a mechanism involving the small GTP-binding Rho J. Biol. Chem. 272 1997 20564 20571
61. S. Gasman, S. Chasserot-Golaz, M. Malacombe, M. Way, and M.F. Bader Regulated exocytosis in neuroendocrine cells: a role for subplasmalemmal Cdc42/N-WASP-induced actin filaments Mol. Biol. Cell 15 2004 520 531
62. K. Matter, F. Dreyer, and K. Aktories Actin involvement in exocytosis from PC12 cells: studies on the influence of botulinum C2 toxin on stimulated noradrenaline release J. Neurochem. 52 1989 370 376
63. G. Li, B.E. Rungger, I. Just, J.C. Jonas, K. Aktories, and C.B. Wollheim 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
64. S. Muallem, K. Kwiatkowska, X. Xu, and H.L. Yin Actin filament disassembly is a sufficient final trigger for exocytosis in nonexcitable cells J. Cell Biol. 128 1995 589 598
65. A. Pendleton, and A. Koffer Effects of latrunculin reveal requirements for the actin cytoskeleton during secretion from mast cells Cell Motil. Cytoskeleton 48 2001 37 51
66. J.C. Norman, L.S. Price, A.J. Ridley, A. Hall, and A. Koffer Actin filament organization in activated mast cells is regulated by heterotrimeric and small GTP-binding proteins J. Cell Biol. 126 1994 1005 1015
67. S. Gasman, S. Chasserot-Golaz, P. Hubert, D. Aunis, and M.F. Bader 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 1998 16913 16920
68. H.L. Yin, and P.A. Janmey Phosphoinositide regulation of the Actin cytoskeleton Annu. Rev. Physiol. 65 2002 761 789
69. D. Raucher, T. Stauffer, W. Chen, K. Shen, S. Guo, J.D. York, M.P. Sheetz, and T. Meyer Phosphatidylinositol 4,5-bisphosphate functions as a second messenger that regulates cytoskeleton-plasma membrane adhesion Cell 100 2000 221 228
70. A.S. Sechi, and J. Wehland The actin cytoskeleton and plasma membrane connection: PtdIns(4,5)P(2) influences cytoskeletal protein activity at the plasma membrane J. Cell. Sci. 113 2000 3685 3695
71. L. Zhang, M.G. Marcu, K. Nau-Staudt, and J.M. Trifaro Recombinant scinderin enhances exocytosis, an effect blocked by two scinderin-derived actin-binding peptides and PIP2 Neuron 17 1996 287 296
72. S. Cotteret, and J. Chernoff The evolutionary history of effectors downstream of Cdc42 and Rac Genome Biol. 3 2002 1 8
73. R. Rohatgi, L. Ma, H. Miki, M. Lopez, T. Kirchhausen, T. Takenawa, and M.W. Kirschner The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly Cell 97 1999 221 231
74. H.N. Higgs, and T.D. Pollard Regulation of actin filament network formation through Arp2/3 complex: activation by diverse array of proteins Annu. Rev. Biochem. 70 2001 649 676
75. G. Eitzen, L. Wang, N. Thorngren, and W. Wickner Remodeling of organelle-bound actin is required for yeast vacuole fusion J. Cell Biol. 158 2002 669 679
76. A.M. Sokac, C. Co, J. Taunton, and W. Bement Cdc42-dependent actin polymerization during compensatory endocytosis in Xenopus eggs Nat. Cell Biol. 5 2003 727 732
77. A. Elhamdani, H.C. Palfrey, and C.R. Artalejo Quantal size is dependent on stimulation frequency and calcium entry in calf chromaffin cells Neuron 31 2001 819 830
78. J.W. Taraska, D. Perrais, M. Ohara-Imaizumi, M. Nagamatsu, and A. Almers Secretory granules are recaptured largely intact after stimulated exocytosis in cultured endocrine cells Proc. Natl. Acad. Sci. U. S. A. 100 2003 2070 2075
79. V.N. Murthy, and P. De Camilli Cell biology of the presynaptic terminal Annu. Rev. Neurosci. 26 2003 701 728
80. J.E. Richmond, and K.S. Broadie The synaptic vesicle cycle: exocytosis and endocytosis in Drosophila and C. elegans Curr. Opin. Neurobiol. 12 2002 499 507
81. M. Krauss, M. Kinuta, M.R. Wenk, P. De Camilli, K. Takei, and V. Haucke ARF6 stimulates clathrin/AP-2 recruitment to synaptic membranes by activating phosphatidylinositol phosphate kinase type Igamma J. Cell Biol. 162 2003 113 124
82. M.R. Wenk, L. Pellegrini, V.A. Klenchin, G. Di Paolo, S. Chang, L. Daniell, M. Arioka, T.F. Martin, and P. De Camilli PIP kinase Iγ is the major PI(4,5)P(2) synthesizing enzyme at the synapse Neuron 32 2001 79 88
83. O. Cremona, and P. De Camilli Phosphoinositides in membrane traffic at the synapse J. Cell. Sci. 114 2001 1041 1052
84. U. Ashery, H. Koch, V. Scheuss, N. Brose, and J. Rettig A presynaptic role for the ADP ribosylation factor (ARF)-specific GDP/GTP exchange factor msec7-1 Proc. Natl. Acad. Sci. U. S. A. 96 1999 1094 1099
85. C. Rosenmund, A. Sigler, I. Augustin, K. Reim, N. Brose, and J.S. Rhee Related differential control of vesicle priming and short-term plasticity by Munc13 isoforms Neuron 33 2002 411 424
86. 2+ sensor for neurotransmitter release Trends Neurosci. 26 2003 413 422
87. A. Toker, and L.C. Cantley Signalling through the lipid products of phosphoinositide-3-OH kinase Nature 387 1997 673 676
88. 2+-dependent neurotransmitter exocytosis J. Biol. Chem. 275 2000 7764 7770
89. C. Busch, and K. Aktories Microbial toxins and the glycosylation of rho family GTPases Curr. Opin. Struct. Biol. 10 2000 528 535
90. M.R. Popoff, E. Chaves-Olarte, E. Lemichez, C. von Eichel-Streiber, M. Thelestam, P. Chardin, D. Cussac, B. Antonny, P. Chavrier, G. Flatau, M. Giry, J. de Gunzburg, and P. Boquet Ras, Rap, and Rac small GTP-binding proteins are targets for Clostridium sordellii lethal toxin glucosylation J. Biol. Chem. 271 1996 10217 10224
91. B. Poulain, A. De Paiva, F. Deloye, F. Doussau, L. Tauc, U. Weller, and J.O. Dolly Differences in the multiple step process of inhibition of neurotransmitter release induced by tetanus toxin and botulinum neurotoxins type A and B at Aplysia synapses Neuroscience 70 1996 567 576
92. Y. Humeau, M.R. Popoff, H. Kojima, F. Doussau, and B. Poulain Rac GTPase plays an essential role in exocytosis by controlling the fusion competence of release site J. Neurosci. 22 2002 7968 7981
93. C.F. Stevens, and T. Tsujimoto Estimates for the pool size of releasable quanta at a single central synapse and for the time required to refill the pool Proc. Natl. Acad. Sci. U. S. A. 92 1995 846 849
94. J. Klingauf, E.T. Kavalali, and R.W. Tsien Kinetics and regulation of fast endocytosis at hippocampal synapses Nature 394 1998 581 585
95. V.N. Murthy, and C.F. Stevens Reversal of synaptic vesicle docking at central synapses Nat. Neurosci. 2 1999 503 507
96. D.M. Quastel The binomial model in fluctuation analysis of quantal neurotransmitter release Biophys. J. 72 1997 728 753
97. J.D. Clements, and R.A. Silver Unveiling synaptic plasticity: a new graphical and analytical approach Trends Neurosci. 23 2000 105 113
98. V. Scheuss, and E. Neher Estimating synaptic parameters from mean, variance, and covariance in trains of synaptic responses Biophys. J. 81 2001 1970 1989
99. Y. Humeau, N. Vitale, S. Chassserot-Golaz, J.L. Dupont, G. Du, M.A. Frohman, M.F. Bader, and B. Poulain A role for phospholipase D1 in neurotransmitter release Proc. Natl. Acad. Sci. U. S. A. 98 2001 15300 15305
100. M.A. Frohman, T.C. Sung, and A.J. Morris Mammalian phospholipase D structure and regulation Biochim. Biophys. Acta 1439 1999 175 186
101. J.H. Exton Regulation of phospholipase D FEBS Lett. 531 2002 58 61
102. C. Job, and L. Lagnado Calcium and protein kinase C regulate the actin cytoskeleton in the synaptic terminal of retinal bipolar cells J. Cell Biol. 143 1998 1661 1672
103. B.W. Bernstein, M. DeWit, and J.R. Bamburg Actin disassembles reversibly during electrically induced recycling of synaptic vesicles in cultured neurons Brain Res. Mol. Brain Res. 53 1998 236 251
104. X.H. Wang, J.Q. Zheng, and M.M. Poo Effect of cytochalasin treatment in short-term synaptic plasticity at developing neuromuscular junctions in frogs J. Physiol. 491 1996 187 195
105. M. Morales, M.A. Colicos, and Y. Goda Actin-dependent regulation of neurotransmitter release at central synapses Neuron 27 2000 539 550
106. J.C. Cole, B.R. Villa, and R.S. Wilkinson Disruption of actin impedes transmitter release in snake motor terminals J. Physiol. 525 2000 579 586
107. S. Sankaranarayanan, P.P. Atluri, and T.A. Ryan Actin has a molecular scaffolding, not propulsive, role in presynaptic function Nat. Neurosci. 6 2003 127 134
108. T. Sakaba, and E. Neher Involvement of actin polymerization in vesicle recruitment at the calyx of Held synapse J. Neurosci. 23 2003 837 846
109. O. Shupliakov, O. Bloom, J.S. Gustafsson, O. Kjaerulff, P. Löw, N. Tomilin, V.A. Pieribone, P. Greengard, and L. Brodin Impaired recycling of synaptic vesicles after acute perturbation of the presynaptic actin cytoskeleton Proc. Natl. Acad. Sci. U. S. A. 99 2002 14476 14481
110. M.M. Kessels, and B. Qualmann Syndapins integrate N-WASP in receptor-mediated endocytosis EMBO J. 21 2002 6083 6094
111. J.Y. Wang, D.J. Wigston, H.D. Rees, A.I. Levey, and D.L. Falls LIM kinase 1 accumulates in presynaptic terminals during synapse maturation J. Comp. Neurol. 416 2000 319 334
112. S. Arber, F.A. Barbayannis, H. Hanser, C. Schneider, C.A. Stanyon, O. Bernard, and P. Caroni Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase Nature 393 1998 805 809
113. N. Yang, O. Higuchi, K. Ohashi, K. Nagata, A. Wada, K. Kangawa, E. Nishida, and K. Mizuno Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization Nature 393 1998 809 812
114. Y. Fukazawa, Y. Saitoh, F. Ozawa, Y. Ohta, K. Mizuno, and K. Inokuchi Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo Neuron 38 2003 447 460
115. Y. Meng, Y. Zhang, V. Tregoubov, C. Janus, L. Cruz, M. Jackson, W.Y. Lu, J.F. MacDonald, J.Y. Wang, D.L. Falls, and Z. Jia Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice Neuron 35 2002 121 133
116. H.J. Murray, and J.J. O'Connor A role for monomeric G-proteins in synaptic plasticity in the rat dentate gyrus in vitro Brain Res. 1000 2004 85 91
117. J.R. Whyte, and S. Munro Vesicle tethering complexes in membrane traffic J. Cell. Sci. 115 2002 2627 2637
118. C.C. Garner, S. Kindler, and E.D. Gundelfinger Molecular determinants of presynaptic active zones Curr. Opin. Neurobiol. 10 2000 321 327
119. D. Bilder, M. Li, and N. Perrimon Cooperative regulation of cell polarity and growth by Drosophila tumor suppressors Science 289 2000 113 116
120. C. Rongo Disparate cell types use a shared complex of PDZ proteins for polarized protein localization Cytokines Growth Factors Rev. 12 2001 349 359
121. Z.H. Baruch, and W.A. Lim Mechanism and role of PDZ domains in signalling complex assembly J. Cell. Sci. 114 2001 3219 3231
122. Y. Hata, H. Nakanishi, and Y. Takai Synaptic PDZ domain-containing proteins Neurosci. Res. 32 1998 1 7
123. J.P. Roche, M.C. Packard, S. Moeckel-Cole, and V. Budnik Regulation of synaptic plasticity and synaptic vesicle dynamics by the PDZ protein Scribble J. Neurosci. 22 2002 6471 6479
124. S. Audebert, C. Navarro, C. Nourry, S. Chasserot-Golaz, P. Lécine, Y. Bellaiche, J.L. Dupont, J.M. Strub, A. Van Dorsselaer, N. Vitale, and J.P. Borg Mammalian Scribble recruits the βPIX exchange factor to regulate exocytosis Curr. Biol. 14 2004 987 995
125. X. Wang, M. Kibschull, M.M. Laue, B. Lichte, E. Petrasch-Parwez, and M.W. Kilimann 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
126. S.D. Fenster, W.J. Chung, R. Zhai, C. Cases-Langhoff, B. Voss, A.M. Garner, U. Kaempf, S. Kindler, E.D. Gundelfinger, and C.C. Garner Piccolo, a presynaptic zinc finger protein structurally related to Bassoon Neuron 25 2000 203 214
127. Y. Wang, M. Okamoto, F. Schmitz, K. Hofmann, and T.C. Südhof Rim is a putative Rab3 effector in regulating synaptic vesicle fusion Nature 388 1997 593 598
128. N. Brose, C. Rosenmond, and J. Rettig Regulation of transmitter release by Unc-13 and its homologues Curr. Opin. Neurobiol. 10 2000 303 311
129. E. Takao-Rikitsu, S. Mochida, E. Inoue, M. Deguchi-Tawarada, M. Inoue, T. Ohtsuka, and Y. Takai Physical and functional interaction of the active zone proteins, CAST, RIM1, and Bassoon, in neurotransmitter release J. Cell Biol. 164 2004 301 311
130. K. Fujimoto, T. Shibasaki, N. Yokoi, Y. Kashima, M. Matsumoto, T. Sasaki, N. Tajima, T. Iwanaga, and S. Seino Piccolo, A calcium sensor in pancreatic β cells. Involvement of camp-GEFII•Rim2•Piccolo complex in cAMP-dependent exocytosis J. Biol. Chem. 277 2002 50497 50502
131. S. Kim, J. Ko, H. Shin, J.R. Lee, C. Lim, J.H. Han, W.D. Altrock, C.C. Garner, E.D. Gundelfinger, R.T. Premont, B.K. Kaang, and E. Kim The GIT family of proteins forms multimers and associates with the presynaptic cytomatrix protein Piccolo J. Biol. Chem. 278 2003 6291 6300