Synaptobrevin N-terminally bound to syntaxin-SNAP-25 defines the primed vesicle state in regulated exocytosis

Journal of Cell Biology

Volumn 188, Issue 3, 2010, Pages 401-413

  Walter, Alexander M ^a   Wiederhold, Katrin ^a,d   Bruns, Dieter ^b   Fasshauer, Dirk ^a   Sørensen, Jakob B ^a,c  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b SAARLAND UNIVERSITY   (Germany)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

SNARE PROTEIN; SYNAPTOBREVIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNTAXIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FUSION; CELL VACUOLE; CHANNEL GATING; CHROMAFFIN CELL; CONTROLLED STUDY; EXOCYTOSIS; GENE MUTATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; TIME;

ANIMALS; CALCIUM; EXOCYTOSIS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; QA-SNARE PROTEINS; R-SNARE PROTEINS; RATS; SECRETORY VESICLES; SNARE PROTEINS; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25;

EID: 76349098018     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200907018     Document Type: Article

References (99)

1. An, S.J., and W. Almers. 2004. Tracking SNARE complex formation in live endocrine cells. Science. 306:1042-1046. doi:10.1126/science.1102559
2. Antonin, W., D. Fasshauer, S. Becker, R. Jahn, and T.R. Schneider. 2002. Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs. Nat. Struct. Biol. 9:107-111. doi:10.1038/nsb746
3. Ashery, U., A. Betz, T. Xu, N. Brose, and J. Rettig. 1999. An efficient method for infection of adrenal chromaffin cells using the Semliki Forest virus gene expression system. Eur. J. Cell Biol. 78:525-532.
4. Bai, J., C.T. Wang, D.A. Richards, M.B. Jackson, and E.R. Chapman. 2004. Fusion pore dynamics are regulated by synaptotagmin*t-SNARE inter-actions. Neuron. 41:929-942. doi:10.1016/S0896-6273(04)00117-5
5. Baumert, M., P.R. Maycox, F. Navone, P. De Camilli, and R. Jahn. 1989. Synaptobrevin: an integral membrane protein of 18,000 daltons present in small synaptic vesicles of rat brain. EMBO J. 8:379-384.
6. Bennett, M.K., N. Calakos, and R.H. Scheller. 1992. Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science. 257:255-259. doi:10.1126/science.1321498
7. Bhalla, A., M.C. Chicka, W.C. Tucker, and E.R. Chapman. 2006. Ca(2+)-synaptotagmin directly regulates t-SNARE function during reconstituted membrane fusion. Nat. Struct. Mol. Biol. 13:323-330. doi:10.1038/nsmb1076
8. Borisovska, M., Y. Zhao, Y. Tsytsyura, N. Glyvuk, S. Takamori, U. Matti, J. Rettig, T. Südhof, and D. Bruns. 2005. v-SNAREs control exocytosis of vesicles from priming to fusion. EMBO J. 24:2114-2126. doi:10.1038/sj.emboj.7600696
9. Broadie, K., A. Prokop, H.J. Bellen, C.J. O'Kane, K.L. Schulze, and S.T. Sweeney. 1995. Syntaxin and synaptobrevin function downstream of vesicle docking in Drosophila. Neuron. 15:663-673. doi:10.1016/0896-6273(95)90154-X
10. Cai, H., K. Reim, F. Varoqueaux, S. Tapechum, K. Hill, J.B. Sørensen, N. Brose, and R.H. Chow. 2008. Complexin II plays a positive role in Ca2+-triggered exocytosis by facilitating vesicle priming. Proc. Natl. Acad. Sci. USA. 105:19538-19543. doi:10.1073/pnas.0810232105
11. Chapman, E.R. 2008. How does synaptotagmin trigger neurotransmitter release? Annu. Rev. Biochem. 77:615-641. doi:10.1146/annurev.biochem.77. 062005.101135
12. Chen, X., D.R. Tomchick, E. Kovrigin, D. Araç, M. Machius, T.C. Südhof, and J. Rizo. 2002. Three-dimensional structure of the complexin/SNARE complex. Neuron. 33:397-409. doi:10.1016/S0896-6273(02) 00583-4
13. Chicka, M.C., E. Hui, H. Liu, and E.R. Chapman. 2008. Synaptotagmin arrests the SNARE complex before triggering fast, efficient membrane fusion in response to Ca2+. Nat. Struct. Mol. Biol. 15:827-835. doi:10.1038/nsmb.1463
14. Chow, R.H., L. von Rüden, and E. Neher. 1992. Delay in vesicle fusion revealed by electrochemical monitoring of single secretory events in adrenal chromaffin cells. Nature. 356:60-63. doi:10.1038/356060a0
15. Colliver, T.L., E.J. Hess, E.N. Pothos, D. Sulzer, and A.G. Ewing. 2000. Quantitative and statistical analysis of the shape of amperometric spikes recorded from two populations of cells. J. Neurochem. 74:1086-1097.
16. Criado, M., A. Gil, S. Viniegra, and L.M. Gutiérrez. 1999. A single amino acid near the C terminus of the synaptosomeassociated protein of 25 kDa (SNAP-25) is essential for exocytosis in chromaffin cells. Proc. Natl. Acad. Sci. USA. 96:7256-7261. doi:10.1073/pnas.96.13.7256
17. Dai, H., N. Shen, D. Araç, and J. Rizo. 2007. A quaternary SNARE-synaptotagmin-Ca2+-phospholipid complex in neurotransmitter release. J. Mol. Biol. 367:848-863. doi:10.1016/j.jmb.2007.01.040
18. de Wit, H., L.N. Cornelisse, R.F. Toonen, and M. Verhage. 2006. Docking of secretory vesicles is syntaxin dependent. PLoS One. 1:e126. doi:10.1371/journal.pone.0000126
19. de Wit, H., A.M. Walter, I. Milosevic, A. Gulyás-Kovács, D. Riedel, J.B. Sørensen, and M. Verhage. 2009. Synaptotagmin-1 docks secretory vesicles to syntaxin-1/SNAP-25 acceptor complexes. Cell. 138:935-946. doi:10.1016/j.cell.2009.07.027
20. Deák, F., Y. Xu, W.P. Chang, I. Dulubova, M. Khvotchev, X. Liu, T.C. Südhof, and J. Rizo. 2009. Munc18-1 binding to the neuronal SNARE complex controls synaptic vesicle priming. J. Cell Biol. 184:751-764. doi:10.1083/jcb.200812026
21. Dulubova, I., S. Sugita, S. Hill, M. Hosaka, I. Fernandez, T.C. Südhof, and J. Rizo. 1999. A conformational switch in syntaxin during exocytosis: role of munc18. EMBO J. 18:4372-4382. doi:10.1093/emboj/18. 16.4372
22. Elferink, L.A., W.S. Trimble, and R.H. Scheller. 1989. Two vesicle-associated membrane protein genes are differentially expressed in the rat central nervous system. J. Biol. Chem. 264:11061-11064.
23. Fang, Q., K. Berberian, L.W. Gong, I. Hafez, J.B. Sørensen, and M. Lindau. 2008. The role of the C terminus of the SNARE protein SNAP-25 in fusion pore opening and a model for fusion pore mechanics. Proc. Natl. Acad. Sci. USA. 105:15388-15392. doi:10.1073/pnas.0805377105
24. Fasshauer, D., and M. Margittai. 2004. A transient N-terminal interaction of SNAP-25 and syntaxin nucleates SNARE assembly. J. Biol. Chem. 279:7613-7621. doi:10.1074/jbc.M312064200
25. Fasshauer, D., H. Otto, W.K. Eliason, R. Jahn, and A.T. Brünger. 1997. Structural changes are associated with soluble N-ethylmaleimide-sensitive fusion protein attachment protein receptor complex formation. J. Biol. Chem. 272:28036-28041. doi:10.1074/jbc.272.44.28036
26. Fasshauer, D., R.B. Sutton, A.T. Brunger, and R. Jahn. 1998. Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc. Natl. Acad. Sci. USA. 95:15781-15786. doi:10.1073/pnas.95.26.15781
27. Fasshauer, D., W. Antonin, M. Margittai, S. Pabst, and R. Jahn. 1999. Mixed and non-cognate SNARE complexes. Characterization of assembly and biophysical properties. J. Biol. Chem. 274:15440-15446. doi:10.1074/jbc.274.22.15440
28. Fasshauer, D., W. Antonin, V. Subramaniam, and R. Jahn. 2002. SNARE assembly and disassembly exhibit a pronounced hysteresis. Nat. Struct. Biol. 9:144-151. doi:10.1038/nsb750
29. Gerber, S.H., J.C. Rah, S.W. Min, X. Liu, H. de Wit, I. Dulubova, A.C. Meyer, J. Rizo, M. Arancillo, R.E. Hammer, et al. 2008. Conformational switch of syntaxin-1 controls synaptic vesicle fusion. Science. 321:1507-1510. doi:10.1126/science.1163174
30. Gil, A., L.M. Gutiérrez, C. Carrasco-Serrano, M.T. Alonso, S. Viniegra, and M. Criado. 2002. Modifications in the C terminus of the synaptosome-associated protein of 25 kDa (SNAP-25) and in the complementary region of synaptobrevin affect the final steps of exocytosis. J. Biol. Chem. 277:9904-9910. doi:10.1074/jbc.M110182200
31. Giraudo, C.G., W.S. Eng, T.J. Melia, and J.E. Rothman. 2006. A clamping mechanism involved in SNARE-dependent exocytosis. Science. 313:676-680. doi:10.1126/science.1129450
32. Giraudo, C.G., A. Garcia-Diaz, W.S. Eng, Y. Chen, W.A. Hendrickson, T.J. Melia, and J.E. Rothman. 2009. Alternative zippering as an on-off switch for SNARE-mediated fusion. Science. 323:512-516. doi:10.1126/ science.1166500
33. Guan, R., H. Dai, and J. Rizo. 2008. Binding of the Munc13-1 MUN domain to membrane-anchored SNARE complexes. Biochemistry. 47:1474-1481. doi:10.1021/bi702345m
34. Gulyás-Kovács, A., H. de Wit, I. Milosevic, O. Kochubey, R. Toonen, J. Klingauf, M. Verhage, and J.B. Sørensen. 2007. Munc18-1: sequential interactions with the fusion machinery stimulate vesicle docking and priming. J. Neurosci. 27:8676-8686. doi:10.1523/JNEUROSCI.0658-07.2007
35. Halemani, N.D., I. Bethani, S.O. Rizzoli, and T. Lang. 2009. Structure and dynamics of a two-helix SNARE complex in live cells. Traffic doi:10.1111/j.1600-0854.2009.01020.x.
36. Hammarlund, M., M.T. Palfreyman, S. Watanabe, S. Olsen, and E.M. Jorgensen. 2007. Open syntaxin docks synaptic vesicles. PLoS Biol. 5:e198. doi:10.1371/journal.pbio.0050198
37. 2+-triggered exocytosis. J. Cell Biol. 172:281-293. doi:10.1083/jcb.200510012
38. Hanson, P.I., J.E. Heuser, and R. Jahn. 1997a. Neurotransmitter release - four years of SNARE complexes. Curr. Opin. Neurobiol. 7:310-315. doi:10.1016/S0959-4388(97)80057-8
39. Hanson, P.I., R. Roth, H. Morisaki, R. Jahn, and J.E. Heuser. 1997b. Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch electron microscopy. Cell. 90:523-535. doi:10.1016/S0092-8674(00)80512-7
40. Hayashi, T., H. McMahon, S. Yamasaki, T. Binz, Y. Hata, T.C. Südhof, and H. Niemann. 1994. Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly. EMBO J. 13:5051-5061.
41. Heinemann, C., R.H. Chow, E. Neher, and R.S. Zucker. 1994. Kinetics of the secretory response in bovine chromaffin cells following flash photolysis of caged Ca2+. Biophys. J. 67:2546-2557. doi:10.1016/S0006-3495(94)80744-1
42. Huntwork, S., and J.T. Littleton. 2007. A complexin fusion clamp regulates spontaneous neurotransmitter release and synaptic growth. Nat. Neurosci. 10:1235-1237. doi:10.1038/nn1980
43. Jahn, R., and R.H. Scheller. 2006. SNAREs-engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7:631-643. doi:10.1038/nrm2002
44. James, D.J., J. Kowalchyk, N. Daily, M. Petrie, and T.F. Martin. 2009. CAPS drives trans-SNARE complex formation and membrane fusion through syntaxin interactions. Proc. Natl. Acad. Sci. USA. 106:17308-17313. doi:10.1073/pnas.0900755106
45. Kesavan, J., M. Borisovska, and D. Bruns. 2007. v-SNARE actions during Ca(2+)-triggered exocytosis. Cell. 131:351-363. doi:10.1016/j.cell.2007. 09.025
46. Kloepper, T.H., C.N. Kienle, and D. Fasshauer. 2007. An elaborate classification of SNARE proteins sheds light on the conservation of the eukaryotic endomembrane system. Mol. Biol. Cell. 18:3463-3471. doi:10.1091/mbc.E07-03-0193
47. Kweon, D.H., C.S. Kim, and Y.K. Shin. 2003. Insertion of the membrane-proximal region of the neuronal SNARE coiled coil into the membrane. J. Biol. Chem. 278:12367-12373. doi:10.1074/jbc.M211123200
48. Li, C., B. Ullrich, J.Z. Zhang, R.G. Anderson, N. Brose, and T.C. Südhof. 1995. Ca(2+)-dependent and -independent activities of neural and non-neural synaptotagmins. Nature. 375:594-599. doi:10.1038/375594a0
49. Li, F., F. Pincet, E. Perez, W.S. Eng, T.J. Melia, J.E. Rothman, and D. Tareste. 2007. Energetics and dynamics of SNAREpin folding across lipid bilayers. Nat. Struct. Mol. Biol. 14:890-896. doi:10.1038/nsmb1310
50. Lindau, M., and E. Neher. 1988. Patch-clamp techniques for time-resolved capacitance measurements in single cells. Pflugers Arch. 411:137-146. doi:10.1007/BF00582306
51. Malsam, J., S. Kreye, and T.H. Söllner. 2008. Membrane fusion: SNAREs and regulation. Cell. Mol. Life Sci. 65:2814-2832. doi:10.1007/s00018-008-8352-3
52. Margittai, M., D. Fasshauer, R. Jahn, and R. Langen. 2003. The Habc domain and the SNARE core complex are connected by a highly flexible linker. Biochemistry. 42:4009-4014. doi:10.1021/bi027437z
53. Martens, S., M.M. Kozlov, and H.T. McMahon. 2007. How synaptotagmin promotes membrane fusion. Science. 316:1205-1208. doi:10.1126/science. 1142614
54. Maximov, A., J. Tang, X. Yang, Z.P. Pang, and T.C. Südhof. 2009. Complexin controls the force transfer from SNARE complexes to membranes in fusion. Science. 323:516-521. doi:10.1126/science.1166505
55. McNew, J.A., T. Weber, D.M. Engelman, T.H. Söllner, and J.E. Rothman. 1999. The length of the flexible SNAREpin juxtamembrane region is a critical determinant of SNARE-dependent fusion. Mol. Cell. 4:415-421. doi:10.1016/S1097-2765(00)80343-3
56. Melia, T.J., T. Weber, J.A. McNew, L.E. Fisher, R.J. Johnston, F. Parlati, L.K. Mahal, T.H. Sollner, and J.E. Rothman. 2002. Regulation of membrane fusion by the membrane-proximal coil of the t-SNARE during zippering of SNAREpins. J. Cell Biol. 158:929-940. doi:10.1083/jcb.200112081
57. Nagy, G., J.H. Kim, Z.P. Pang, U. Matti, J. Rettig, T.C. Südhof, and J.B. Sørensen. 2006. Different effects on fast exocytosis induced by synaptotagmin 1 and 2 isoforms and abundance but not by phosphorylation. J. Neurosci. 26:632-643. doi:10.1523/JNEUROSCI.2589-05.2006
58. Nagy, G., I. Milosevic, R. Mohrmann, K. Wiederhold, A.M. Walter, and J.B. Sørensen. 2008. The SNAP-25 linker as an adaptation toward fast exocytosis. Mol. Biol. Cell. 19:3769-3781. doi:10.1091/mbc.E07-12-1218
59. Neher, E. 2006. A comparison between exocytic control mechanisms in adrenal chromaffin cells and a glutamatergic synapse. Pflugers Arch. 453:261-268. doi:10.1007/s00424-006-0143-9
60. Neher, E., and T. Sakaba. 2008. Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron. 59:861-872. doi:10.1016/j.neuron.2008.08.019
61. Nonet, M.L., O. Saifee, H. Zhao, J.B. Rand, and L. Wei. 1998. Synaptic transmission deficits in Caenorhabditis elegans synaptobrevin mutants. J. Neurosci. 18:70-80.
62. Oyler, G.A., G.A. Higgins, R.A. Hart, E. Battenberg, M. Billingsley, F.E. Bloom, and M.C. Wilson. 1989. The identification of a novel synaptosomal-associated protein, SNAP-25, differentially expressed by neuronal subpopulations. J. Cell Biol. 109:3039-3052. doi:10.1083/jcb.109.6.3039
63. Pobbati, A.V., A. Stein, and D. Fasshauer. 2006. N- to C-terminal SNARE complex assembly promotes rapid membrane fusion. Science. 313:673-676. doi:10.1126/science.1129486
64. Rickman, C., and B. Davletov. 2003. Mechanism of calcium-independent synaptotagmin binding to target SNAREs. J. Biol. Chem. 278:5501-5504. doi:10.1074/jbc.C200692200
65. Rickman, C., F.A. Meunier, T. Binz, and B. Davletov. 2004. High affinity interaction of syntaxin and SNAP-25 on the plasma membrane is abolished by botulinum toxin E. J. Biol. Chem. 279:644-651. doi:10.1074/jbc.M310879200
66. Rizo, J., and C. Rosenmund. 2008. Synaptic vesicle fusion. Nat. Struct. Mol. Biol. 15:665-674. doi:10.1038/nsmb.1450
67. Saifee, O., L. Wei, and M.L. Nonet. 1998. The Caenorhabditis elegans unc-64 locus encodes a syntaxin that interacts genetically with synaptobrevin. Mol. Biol. Cell. 9:1235-1252.
68. Schaub, J.R., X. Lu, B. Doneske, Y.K. Shin, and J.A. McNew. 2006. Hemifusion arrest by complexin is relieved by Ca2+-synaptotagmin I. Nat. Struct. Mol. Biol. 13:748-750. doi:10.1038/nsmb1124
69. Schiavo, G., G. Stenbeck, J.E. Rothman, and T.H. Söllner. 1997. Binding of the synaptic vesicle v-SNARE, synaptotagmin, to the plasma membrane t-SNARE, SNAP-25, can explain docked vesicles at neurotoxintreated synapses. Proc. Natl. Acad. Sci. USA. 94:997-1001. doi:10.1073/pnas.94.3.997
70. Schoch, S., F. Deák, A. Königstorfer, M. Mozhayeva, Y. Sara, T.C. Südhof, and E.T. Kavalali. 2001. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science. 294:1117-1122. doi:10.1126/science.1064335
71. Schuette, C.G., K. Hatsuzawa, M. Margittai, A. Stein, D. Riedel, P. Küster, M. König, C. Seidel, and R. Jahn. 2004. Determinants of liposome fusion mediated by synaptic SNARE proteins. Proc. Natl. Acad. Sci. USA. 101:2858-2863. doi:10.1073/pnas.0400044101
72. Schulte, A., and R.H. Chow. 1996. A simple method for insulating carbon-fiber microelectrodes using anodic electrophoretic deposition of paint. Anal. Chem. 68:3054-3058. doi:10.1021/ac960210n
73. Siddiqui, T.J., O. Vites, A. Stein, R. Heintzmann, R. Jahn, and D. Fasshauer. 2007. Determinants of synaptobrevin regulation in membranes. Mol. Biol. Cell. 18:2037-2046. doi:10.1091/mbc.E07-01-0049
74. Söllner, T., M.K. Bennett, S.W. Whiteheart, R.H. Scheller, and J.E. Rothman. 1993. A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell. 75:409-418. doi:10.1016/0092-8674(93)90376-2
75. Sørensen, J.B., G. Nagy, F. Varoqueaux, R.B. Nehring, N. Brose, M.C. Wilson, and E. Neher. 2003. Differential control of the releasable vesicle pools by SNAP-25 splice variants and SNAP-23. Cell. 114:75-86. doi:10.1016/S0092-8674(03)00477-X
76. Sørensen, J.B., K. Wiederhold, E.M. Müller, I. Milosevic, G. Nagy, B.L. de Groot, H. Grubmüller, and D. Fasshauer. 2006. Sequential N- to C-terminal SNARE complex assembly drives priming and fusion of secretory vesicles. EMBO J. 25:955-966. doi:10.1038/sj.emboj.7601003
77. Stein, A., A. Radhakrishnan, D. Riedel, D. Fasshauer, and R. Jahn. 2007. Synaptotagmin activates membrane fusion through a Ca2+-dependent trans interaction with phospholipids. Nat. Struct. Mol. Biol. 14:904-911. doi:10.1038/nsmb1305
78. Südhof, T.C. 2004. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27:509-547. doi:10.1146/annurev.neuro.26.041002.131412
79. Südhof, T.C., and J.E. Rothman. 2009. Membrane fusion: grappling with SNARE and SM proteins. Science. 323:474-477. doi:10.1126/science. 1161748
80. Sutton, R.B., D. Fasshauer, R. Jahn, and A.T. Brunger. 1998. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature. 395:347-353. doi:10.1038/26412
81. Tang, J., A. Maximov, O.H. Shin, H. Dai, J. Rizo, and T.C. Südhof. 2006. A complexin/synaptotagmin 1 switch controls fast synaptic vesicle exocytosis. Cell. 126:1175-1187. doi:10.1016/j.cell.2006.08.030
82. Verhage, M., and J.B. Sørensen. 2008. Vesicle docking in regulated exocytosis. Traffic. 9:1414-1424. doi:10.1111/j.1600-0854.2008.00759.x
83. Voets, T. 2000. Dissection of three Ca2+-dependent steps leading to secretion in chromaffin cells from mouse adrenal slices. Neuron. 28:537-545. doi:10.1016/S0896-6273(00)00131-8
84. Voets, T., E. Neher, and T. Moser. 1999. Mechanisms underlying phasic and sustained secretion in chromaffin cells from mouse adrenal slices. Neuron. 23:607-615. doi:10.1016/S0896-6273(00)80812-0
85. Voets, T., T. Moser, P.E. Lund, R.H. Chow, M. Geppert, T.C. Südhof, and E. Neher. 2001a. Intracellular calcium dependence of large dense-core vesicle exocytosis in the absence of synaptotagmin I. Proc. Natl. Acad. Sci. USA. 98:11680-11685. doi:10.1073/pnas.201398798
86. Voets, T., R.F. Toonen, E.C. Brian, H. de Wit, T. Moser, J. Rettig, T.C. Südhof, E. Neher, and M. Verhage. 2001b. Munc18-1 promotes large dense-core vesicle docking. Neuron. 31:581-591. doi:10.1016/S0896-6273(01)00391-9
87. Wang, C.T., R. Grishanin, C.A. Earles, P.Y. Chang, T.F. Martin, E.R. Chapman, and M.B. Jackson. 2001. Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense-core vesicles. Science. 294:1111-1115. doi:10.1126/science.1064002
88. Wang, C.T., J. Bai, P.Y. Chang, E.R. Chapman, and M.B. Jackson. 2006. Synaptotagmin-Ca2+ triggers two sequential steps in regulated exocytosis in rat PC12 cells: fusion pore opening and fusion pore dilation. J. Physiol. 570:295-307.
89. Weber, T., B.V. Zemelman, J.A. McNew, B. Westermann, M. Gmachl, F. Parlati, T.H. Söllner, and J.E. Rothman. 1998. SNAREpins: minimal machinery for membrane fusion. Cell. 92:759-772. doi:10.1016/S0092-8674(00)81404-X
90. Wei, S., T. Xu, U. Ashery, A. Kollewe, U. Matti, W. Antonin, J. Rettig, and E. Neher. 2000. Exocytotic mechanism studied by truncated and zero layer mutants of the C-terminus of SNAP-25. EMBO J. 19:1279-1289. doi:10.1093/emboj/19.6.1279
91. Weimer, R.M., J.E. Richmond, W.S. Davis, G. Hadwiger, M.L. Nonet, and E.M. Jorgensen. 2003. Defects in synaptic vesicle docking in unc-18 mutants. Nat. Neurosci. 6:1023-1030. doi:10.1038/nn1118
92. Weninger, K., M.E. Bowen, U.B. Choi, S. Chu, and A.T. Brunger. 2008. Accessory proteins stabilize the acceptor complex for synaptobrevin, the 1:1 syntaxin/SNAP-25 complex. Structure. 16:308-320. doi:10.1016/j.str.2007. 12.010
93. Wiederhold, K., and D. Fasshauer. 2009. Is assembly of the SNARE complex enough to fuel membrane fusion? J. Biol. Chem. 284:13143-13152. doi:10.1074/jbc.M900703200
94. Wightman, R.M., J.A. Jankowski, R.T. Kennedy, K.T. Kawagoe, T.J. Schroeder, D.J. Leszczyszyn, J.A. Near, E.J. Diliberto Jr., and O.H. Viveros. 1991. Temporally resolved catecholamine spikes correspond to single vesicle release from individual chromaffin cells. Proc. Natl. Acad. Sci. USA. 88:10754-10758. doi:10.1073/pnas.88.23.10754
95. Wu, M.N., T. Fergestad, T.E. Lloyd, Y. He, K. Broadie, and H.J. Bellen. 1999. Syntaxin 1A interacts with multiple exocytic proteins to regulate neurotransmitter release in vivo. Neuron. 23:593-605. doi:10.1016/S0896-6273(00)80811-9
96. Xu, T., T. Binz, H. Niemann, and E. Neher. 1998. Multiple kinetic components of exocytosis distinguished by neurotoxin sensitivity. Nat. Neurosci. 1:192-200. doi:10.1038/642
97. Xue, M., K. Reim, X. Chen, H.T. Chao, H. Deng, J. Rizo, N. Brose, and C. Rosenmund. 2007. Distinct domains of complexin I differentially regulate neurotransmitter release. Nat. Struct. Mol. Biol. 14:949-958. doi:10.1038/nsmb1292
98. Yang, C., S. Mora, J.W. Ryder, K.J. Coker, P. Hansen, L.A. Allen, and J.E. Pessin. 2001. VAMP3 null mice display normal constitutive, insulin- and exercise-regulated vesicle trafficking. Mol. Cell. Biol. 21:1573-1580. doi:10.1128/MCB.21.5.1573-1580.2001
99. Zhang, X., M.J. Kim-Miller, M. Fukuda, J.A. Kowalchyk, and T.F. Martin. 2002. Ca2+-dependent synaptotagmin binding to SNAP-25 is essential for Ca2+-triggered exocytosis. Neuron. 34:599-611. doi:10.1016/S0896-6273(02) 00671-2