Revisiting the role of SNAREs in exocytosis and membrane fusion

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1641, Issue 2-3, 2003, Pages 121-135

  Szule, Joseph A ^a   Coorssen, Jens R ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Clostridial toxin; Exocytosis; Fusion pore; Lipid; Molecular mechanism; Secretion

Indexed keywords

CLOSTRIDIUM TOXIN; HYBRID PROTEIN; SNARE PROTEIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25;

BILAYER MEMBRANE; ENDOCYTOSIS; EXOCYTOSIS; MEMBRANE FUSION; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REVIEW;

EID: 0043162015     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0167-4889(03)00095-8     Document Type: Review

References (209)

1. Rand R.P., Parsegian V.A. Hydration forces between phospholipid bilayers. Biochim. Biophys. Acta. 988:1989;351-376.
2. Rand R.P. The lipid-water interface: revelations by osmotic stress. Int. Rev. Cyt. 215:2002;33-48.
3. Kuzmin P.I., Zimmerberg J., Chizmadzhev Y.A., Cohen F.S. A quantitative model for membrane fusion based on low-energy intermediates. Proc. Natl. Acad. Sci. U. S. A. 98:2001;7235-7240.
4. Markin V.S., Albanes J.P. Membrane fusion: stalk model revisited. Biophys. J. 82:2002;693-712.
5. Kozlovsky Y., Kozlov M.M. Stalk model of membrane fusion: solution of energy crisis. Biophys. J. 82:2002;882-895.
6. Chavez R.A., Miller S.G., Moore H.P. A biosynthetic secretory pathway in constitutive secretory cells. J. Cell Biol. 133:1996;1177-1191.
7. 2+ triggers massive exocytosis in Chinese hamster ovary cells. EMBO J. 15:1996;3787-3791.
8. 2+ compound. J. Biol. Chem. 271:1996;17751-17754.
9. Dan Y., Poo M.M. Quantal transmitter secretion from myocytes loaded with acetylcholine. Nature. 359:1992;733-736.
10. Bugnard E., Taulier N., Bloc A., Correges P., Falk-Vairant J., Sors P., Loctin F., Dunant Y. Quantal transmitter release by glioma cells: quantification of intramembrane particle changes. Neuroscience. 113:2002;125-135.
11. Knight D.E., von Grafenstein H., Athayde C.M. Calcium-dependent and calcium-independent exocytosis. Trends Neurosci. 12:1989;451-458.
12. Vacquier V.D. The isolation of intact cortical granules from sea urchin eggs: calcium ions trigger granule discharge. Dev. Biol. 43:1975;62-74.
13. Baker P.F., Whitaker M.J. Influence of ATP and calcium on the cortical reaction in sea urchin eggs. Nature. 276:1978;513-515.
14. Vilmart-Seuwen J., Kersken H., Stürzl R., Plattner H. ATP keeps exocytosis sites in a primed state but is not required for membrane fusion: an analysis with Paramecium cells in vivo and in vitro. J. Cell Biol. 103:1986;1279-1288.
15. Holz R.W., Bittner M.A., Peppers S.C., Senter R.A., Eberhard D.A. MgATP-independent and MgATP-dependent exocytosis. J. Biol. Chem. 264:1989;5412-5419.
16. Hay J.C., Martin T.F. Resolution of regulated secretion into sequential MgATP-dependent and calcium-dependent stages mediated by distinct cytosolic proteins. J. Cell Biol. 119:1992;139-151.
17. 2+-activated secretion. Nature. 374:1995;173-177.
18. Parsons T., Coorssen J.R., Horstmann H., Almers W. Docked granules, the exocytotic burst, and the need for ATP hydrolysis in endocrine cells. Neuron. 15:1995;1085-1096.
19. Plattner H., Artalejo A.R., Neher E. Ultrastructural organization of bovine chromaffin cell cortex - analysis by cryofixation and morphometry of aspects pertinent to exocytosis. J. Cell Biol. 139:1997;1709-1717.
20. 2+ channels accounts for first-phase insulin secretion in mouse β-cells. Diabetes. 51:2002;S74-S82.
21. Heidelberger R., Sterling P., Matthews G. Roles of ATP in depletion and replenishment of the releasable pool of synaptic vesicles. J. Neurophysiol. 88:2002;98-106.
22. Söllner T.H., Bennett M.K., Whitheart S.W., Scheller R.H., Rothman J.E. A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell. 75:1993;409-418.
23. Rothman J.E. Mechanisms of intracellular protein transport. Nature. 372:1994;55-63.
24. Gerber S.H., Südhof T.C. Molecular determinants of regulated exocytosis. Diabetes. 51:2002;S3-S11.
25. Storrie B., Desjardins M. The biogenesis of lysosomes: is it a kiss and run, continuous fusion and fission process? BioEssays. 18:1996;895-903.
26. Alés E., Tabares L., Poyato J.M., Valero V., Lindau M., Alvarez de Toledo G. High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism. Nat. Cell Biol. 1:1999;40-44.
27. Henkel A.W., Kang G., Kornhuber J. A common molecular machinery for exocytosis and the 'kiss-and-run' mechanism in chromaffin cells is controlled by phosphorylation. J. Cell Sci. 114:2001;4613-4620.
28. 2+-dependent step in exocytosis subsequent to vesicle fusion. FEBS Lett. 363:1995;217-220.
29. Fernández-Chacón R., Alvarez de Toledo G. Cytosolic calcium facilitates release of secretory products after exocytotic vesicle fusion. FEBS Lett. 363:1995;221-225.
30. 2+ and protein kinase C via distinct mechanisms. EMBO J. 17:1998;4340-4345.
31. Rahamimoff R., Fernandez J.M. Pre- and postfusion regulation of transmitter release. Neuron. 18:1997;17-27.
32. Murthy V.N., Sejnowski T.J., Stevens C.F. Heterogeneous release properties of visualized individual hippocampal synapses. Neuron. 18:1997;599-612.
33. Murthy V.N., Stevens C.F. Reversal of synaptic vesicle docking at central synapses. Nat. Neurosci. 2:1999;503-507.
34. Shorter J., Beard M.B., Seemann J., Dirac-Svejstrup A.B., Warren G. Sequential tethering of golgins and catalysis of SNAREpin assembly by the vesicle-tethering protein p115. J. Cell Biol. 157:2002;45-62.
35. Whyte J.R.C., Munro S. Vesicle tethering complexes in membrane traffic. J. Cell Sci. 115:2002;2627-2637.
36. 2+-triggered fusion steps of exocytosis: rationale and perspectives. Biochimie. 82:2000;303-314.
37. Bruns D., Jahn R. Molecular determinants of exocytosis. Pflugers Arch. 443:2002;333-338.
38. Leikin S.L., Kozlov M.M., Chernomordik L.V., Markin V.S., Chizmadzhev Y.A. Membrane fusion: overcoming of the hydration barrier and local restructuring. J. Theor. Biol. 129:1987;411-425.
39. Chernomordik L. Non-bilayer lipids and biological fusion intermediates. Chem. Phys. Lipids. 81:1996;203-213.
40. Kozlovsky Y., Chernomordik L.V., Kozlov M.M. Lipid intermediates in membrane fusion: formation, structure, and decay of hemifusion diaphragm. Biophys. J. 83:2002;2634-2651.
41. Schiavo G., Matteoli M., Montecucco C. Neurotoxins affecting neuroexocytosis. Physiol. Rev. 80:2000;717-766.
42. Schiavo G., Benfenati F., Poulain B., Rossetto O., Polverino de Laureto P., DasGupta B.R., Montecucco C. Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature. 359:1992;832-835.
43. Schiavo G., Shone C.C., Rossetto O., Alexander F.C.G., Montecucco C. Botulinum neurotoxin serotype F is a zinc endopeptidase specific for VAMP/synaptobrevin. J. Biol. Chem. 268:1993;11516-11519.
44. Humeau Y., Doussau F., Grant N.J., Poulain B. How botulinum and tetanus neurotoxins block neurotransmitter release. Biochimie. 82:2000;427-446.
45. Harvey A.M. The peripheral action of tetanus toxin. J. Physiol. 96:1939;348-365.
46. Burgen A.S.V., Dickens F., Zatman L.J. The action of botulinum toxin on the neuro-muscular junction. J. Physiol. 109:1949;10-24.
47. Boroff D.A., DelCastillo J., Evoy W.H., Steinhardt R.A. Observations on the actions of type A botulinum toxin on frog neuromuscular junctions. J. Physiol. 240:1974;227-253.
48. Hua S.Y., Charlton M.P. Activity-dependent changes in partial VAMP complexes during neurotransmitter release. Nat. Neurosci. 2:1999;1078-1083.
49. Brooks V.B. The action of botulinum toxin on motor-nerve filaments. J. Physiol. 123:1954;501-515.
50. Brooks V.B. An intracellular study of the action of repetitive nerve volleys and of botulinum toxin on miniature end-plate potentials. J. Physiol. 134:1956;264-277.
51. Thesleff S. Supersensitivity of skeletal muscle produced by botulinum toxin. J. Physiol. 151:1960;598-607.
52. Dreyer F., Schmitt A. Transmitter release in tetanus and botulinum A toxin-poisoned mammalian motor endplates and its dependence on nerve stimulation and temperature. Pflugers Arch. 399:1983;228-234.
53. Parsons R.L., Hofmann W.W., Feigen G.A. Mode of action of tetanus toxin on the neuromuscular junction. Am. J. Physiol. 210:1966;84-90.
54. Harris A.J., Miledi R. The effect of type D botulinum toxin on frog neuromuscular junctions. J. Physiol. 217:1971;497-515.
55. Duchen L.W., Tonge D.A. The effects of tetanus toxin on neuromuscular transmission and on the morphology of motor end-plates in slow and fast skeletal muscle of the mouse. J. Physiol. 228:1973;157-172.
56. Stewart B.A., Mohtashami M., Trimble W.S., Boulianne G.L. SNARE proteins contribute to calcium cooperativity of synaptic transmission. Proc. Natl. Acad. Sci. U. S. A. 97:2000;13955-13960.
57. Finley M.F., Patel S.M., Madison D.V., Scheller R.H. The core membrane fusion complex governs the probability of synaptic vesicle fusion but not transmitter release kinetics. J. Neurosci. 22:2002;1266-1272.
58. Mellanby J., Thompson P.A. The effect of tetanus toxin at the neuromuscular junction in the goldfish. J. Physiol. 224:1972;407-419.
59. Cull-Candy S.G., Lundh H., Thesleff S. Effects of botulinum toxin on neuromuscular transmission in the rat. J. Physiol. 260:1976;177-203.
60. Gansel M., Penner R., Dreyer F. Distinct sites of action of clostridial neurotoxins revealed by double-poisoning of mouse motor nerve terminals. Pflugers Arch. 409:1987;533-539.
61. Dreyer F., Rosenberg F., Becker C., Bigalke H., Penner R. Differential effects of various secretagogues on quantal transmitter release from mouse motor nerve terminals treated with botulinum A and tetanus toxin. Naunyn-Schmiedeberg's Arch. Pharmacol. 335:1987;1-7.
62. Ashton A.C., Dolly J.O. Microtubule-dissociating drugs and A23187 reveal differences in the inhibition of synaptosomal transmitter release by botulinum neurotoxins types A and B. J. Neurochem. 56:1991;827-835.
63. Lawrence G.W., Weller U., Dolly J.O. Botulinum A and the light chain of tetanus toxin inhibit distinct stages of MgATP-dependent catecholamine exocytosis from permeabilised chromaffin cells. Eur. J. Biochem. 222:1994;325-333.
64. Lawrence G.W., Foran P., Dolly J.O. Distinct exocytotic responses of intact and permeabilized chromaffin cells after cleavage of the 25-kDa synaptosomal-associated protein (SNAP-25) or synaptobrevin by botulinum toxin A or B. Eur. J. Biochem. 236:1996;877-886.
65. Bittner M.A., Holz R.W. Protein kinase C and clostridial neurotoxins affect discrete and related steps in the secretory pathway. Cell. Mol. Neurobiol. 13:1993;649-664.
66. Ahnert-Hilger G., Weller U. Comparison of the intracellular effects of clostridial neurotoxins on exocytosis from streptolysin O-permeabilized rat pheochromocytoma (PC12) and bovine adrenal chromaffin cells. Neuroscience. 53:1993;547-552.
67. 2+-induced and GTP analogue-induced catecholamine release from permeabilised adrenal chromaffin cells. FEBS Lett. 386:1996;137-140.
68. 2+ partially rescues synaptic transmission in hippocampal cultures treated with botulinum toxin A and C, but not tetanus toxin. J. Neurosci. 17:1997;7190-7202.
69. Land J., Zhang H., Vaidyanathan V.V., Sadoul K., Niemann H., Wollheim C.B. Transient expression of botulinum neurotoxin C1 light chain differentially inhibits calcium and glucose induced insulin secretion in clonal beta-cells. FEBS Lett. 419:1997;13-17.
70. Xu T., Binz T., Niemann H., Neher E. Multiple kinetic components of exocytosis distinguished by neurotoxin sensitivity. Nat. Neurosci. 1:1998;192-200.
71. Hua S.Y., Raciborska D.A., Trimble W.S., Charlton M.P. Different VAMP/synaptobrevin complexes for spontaneous and evoked transmitter release at the crayfish neuromuscular junction. J. Neurophysiol. 80:1998;3233-3246.
72. 2+- but not for GTPgS-induced insulin secretion. EMBO J. 15:1995;2723-2730.
73. Fassio A., Sala R., Bonanno G., Marchi M., Raiteri M. Evidence for calcium-dependent vesicular transmitter release insensitive to tetanus and botulinum toxin type F. Neuroscience. 90:1999;893-902.
74. Vogel S.S., Zimmerberg J. Proteins on exocytotic vesicles mediate calcium-triggered fusion. Proc. Natl. Acad. Sci. U. S. A. 89:1992;4749-4753.
75. 2+ sensitivity. J. Cell Biol. 143:1998;1845-1857.
76. Tahara M., Coorssen J.R., Timmers K., Blank P.S., Whalley T., Scheller R.H., Zimmerberg J. Calcium can disrupt the SNARE protein complex on sea urchin egg secretory vesicles without irreversibly blocking fusion. J. Biol. Chem. 273:1998;33667-33673.
77. Coorssen J.R., Tahara M., Blank P., Zimmerberg J. Role of SNARE proteins in membrane fusion. Mol. Biol. Cell. 8:1997;296a.
78. Bi G.Q., Alderton J.M., Steinhardt R.A. Calcium-regulated exocytosis is required for cell membrane resealing. J. Cell Biol. 131:1995;1747-1758.
79. Ungermann C., Nichols B.J., Pelham H.R.B., Wickner W. A vacuolar v-t-SNARE complex, the predominant form in vivo and on isolated vacuoles, is disassembled and activated for docking and fusion. J. Cell Biol. 140:1998;61-69.
80. Ungermann C., Sato K., Wickner W. Defining the functions of trans-SNARE pairs. Nature. 396:1998;543-548.
81. Peters C., Bayer M.J., Buhler S., Andersen J.S., Mann M., Mayer A. Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion. Nature. 409:2001;567-568.
82. Müller O., Bayer M.J., Peters C., Andersen J.S., Mann M., Mayer A. The Vtc proteins in vacuolar fusion: coupling NSF activity to V(0) trans-complex formation. EMBO J. 21:2002;259-269.
83. Smolen J.E., Stoehr S.J., Boxer L.A. Human neutrophils permeabilized with digitonin respond with lysosomal enzyme release when exposed to micromolar levels of free calcium. Biochim. Biophys. Acta. 886:1986;1-17.
84. 2+-regulated exocytotic vesicles in fibroblasts and epithelial cells. J. Cell Biol. 137:1997;93-104.
85. Horrigan F.T., Bookman R.J. Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells. Neuron. 13:1994;1119-1129.
86. Kirischuk S., Grantyn R. A readily releasable pool of single inhibitory boutons in culture. NeuroReport. 11:2000;3709-3713.
87. Moser T., Neher E. Rapid exocytosis in single chromaffin cells recorded from mouse adrenal slices. J. Neurosci. 17:1997;2314-2323.
88. Sun J.Y., Wu L.G. Fast kinetics of exocytosis revealed by simultaneous measurements of presynaptic capacitance and postsynaptic currents at a central synapse. Neuron. 30:2001;171-182.
89. 2+-sensitive pool of vesicles is regulated by protein kinase C in adrenal chromaffin cells. Proc. Natl. Acad. Sci. U. S. A. 99:2002;17060-17065.
90. Steyer J.A., Horstmann H., Almers W. Transport, docking and exocytosis of single secretory granules in live chromaffin cells. Nature. 388:1997;474-478.
91. Coorssen J.R., Blank P.S., Albertorio F., Bezrukov L., Kolosova I., Backlund P.S., Zimmerberg J. Quantitative femto- to attomole immunodetection of regulated secretory vesicle proteins critical to exocytosis. Anal. Biochem. 307:2002;54-62.
92. Xu T., Rammner B., Margittai M., Artalejo A.R., Neher E., Jahn R. Inhibition of SNARE complex assembly differentially affects kinetic components of exocytosis. Cell. 99:1999;713-722.
93. Chen Y.A., Scales S.J., Jagath J.R., Scheller R.H. A discontinuous SNAP-25 C-terminal coil supports exocytosis. J. Biol. Chem. 276:2001;28503-28508.
94. 2+ and drives membrane fusion. Cell. 97:1999;165-174.
95. Ray P., Berman J.D., Middleton W., Brendle J. Botulinum toxin inhibits arachadonic acid release associated with acetylcholine release from PC12 cells. J. Biol. Chem. 268:1993;11057-11064.
96. Ray P., Millaed C.B., Petrali J.P., Berman J.D., Ray R. Acetylcholine exocytosis in PC12 cells deficient in SNAP-25. NeuroReport. 8:1997;2271-2274.
97. Presek P., Jessen S., Dreyer F., Jarvie P.E., Findik D., Dunkley P.R. Tetanus toxin inhibits depolarization-stimulated protein phosphorylation in rat cortical synaptosomes: effect on synapsin I phosphorylation and translocation. J. Neurochem. 59:1992;1336-1343.
98. Considine R.V., Handler C.M., Simpson L.L., Sherwin J.R. Tetanus toxin inhibits neurotensin-induced mobilization of cytosolic protein kinase C activity in NG-108 cells. Toxicon. 29:1991;1351-1357.
99. Najib A., Pelliccioni P., Gil C., Aguilera J. Clostridium neurotoxins influence serotonin uptake and release differently in rat brain synaptosomes. J. Neurochem. 72:1999;1991-1998.
100. Caohuy H., Pollard H.B. Annexin 7: a non-SNARE proteolytic substrate for botulinum toxin type C in secreting chromaffin cells. Ann. N.Y. Acad. Sci. 971:2002;287-290.
101. Schulze K.L., Broadie K., Perin M.S., Bellen H.J. Genetic and electrophysiological studies of Drosophila syntaxin-1A demonstrate its role in non-neuronal secretion and neurotransmission. Cell. 80:1995;311-320.
102. Nonet M.L., Grundahl K., Meyer B.J., Rand J.B. Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell. 73:1993;1291-1305.
103. Nonet M.L., Saifee O., Zhao H., Rand J.B., Wei L. Synaptic transmission deficits in Caenorhabditis elegans synaptobrevin mutants. J. Neurosci. 18:1998;70-80.
104. Deitcher D.L., Ueda A., Stewart B.A., Burgess R.W., Kidokoro Y., Schwarz T.L. Distinct requirements for evoked and spontaneous release of neurotransmitter are revealed by mutations in the Drosophila gene neuronal-synaptobrevin. J. Neurosci. 18:1998;2028-2039.
105. Rao S.S., Stewart B.A., Rivlin P.K., Vilinsky I., Watson B.O., Lang C., Boulianne G., Salpeter M.M., Deitcher D.L. Two distinct effects on neurotransmission in a temperature-sensitive SNAP-25 mutant. EMBO J. 20:2001;6761-6771.
106. Bittner M.A., Bennett M.K., Holz R.W. Evidence that syntaxin 1A is involved in storage in the secretory pathway. J. Biol. Chem. 271:1996;11214-11221.
107. Nagamatsu S., Fujiwara T., Nakamichi Y., Watanabe T., Katahira H., Sawa H., Akagawa K. Expression and functional role of syntaxin 1/HPC-1 in pancreatic beta cells. Syntaxin 1A, but not 1 B, plays a negative role in regulatory insulin release pathway. J. Biol. Chem. 271:1996;1160-1165.
108. Nagamatsu S., Nakamichi Y., Yamamura C., Matsushima S., Watanabe T., Ozawa S., Furukawa H., Ishida H. Decreased expression of t-SNARE, syntaxin 1, and SNAP-25 in pancreatic beta cells is involved in impaired insulin secretion from diabetic GK rat islets: restoration of decreased t-SNARE proteins improves impaired insulin secretion. Diabetes. 48:1999;2367-2373.
109. 2+-induced insulin exocytosis. EMBO J. 15:1996;6951-6959.
110. Washbourne P., Bortoletto N., Graham M.E., Wilson M.C., Burgoyne R.D., Montecucco C. Botulinum neurotoxin E-insensitive mutants of SNAP-25 fail to bind VAMP but support exocytosis. J. Neurochem. 73:1999;2424-2433.
111. Graham M.E., Washbourne P., Wilson M.C., Burgoyne R.D. SNAP-25 with mutations in the zero layer supports normal membrane fusion kinetics. J. Cell Sci. 114:2001;4397-4405.
112. Washbourne P., Thompson P.M., Carta M., Costa E.T., Mathews J.R., Lopez-Bendito G., Molnar Z., Becher M.W., Valenzuela C.F., Partridge L.D., Wilson M.C. Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat. Neurosci. 5:2001;19-26.
113. Schoch S., Deak F., Konigstorfer A., Mozhayeva M., Sara Y., Südhof T.C., Kavalali E.T. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science. 294:2001;1117-1122.
114. Scales S.J., Finley M.F.A., Scheller R.H. Fusion without SNAREs? Science. 294:2001;1015-1016.
115. Vilinsky I., Stewart B.A., Drummond J., Robinson I., Deitcher D.L. A drosophila SNAP-25 null mutant reveals context-dependent redundancy with SNAP-24 in neurotransmission. Genetics. 162:2002;259-271.
116. Liu T.T., Barlow C. Analysis of Sec22p in endoplasmic reticulum/golgi transport reveals cellular redundancy in SNARE protein function. Mol. Biol. Cell. 13:2002;3314-3324.
117. Sadoul K., Berger A., Niemann H., Weller U., Roche P.A., Klip A., Trimble W.S., Regazzi R., Catsicas S., Halban P.A. SNAP-23 is not cleaved by botulinum neurotoxin E and can replace SNAP-25 in the process of insulin secretion. J. Biol. Chem. 272:1997;33023-33027.
118. Zimmerberg J., Coorssen J.R., Vogel S.S., Blank P.S. Topical review: sea urchin egg preparations as systems for the study of calcium-triggered exocytosis. J. Physiol. 520:1999;15-21.
119. Hu K., Carroll J., Rickman C., Davletov B. Action of complexin on SNARE complex. J. Biol. Chem. 277:2002;41652-41656.
120. Scales S.J., Hesser B.A., Masuda E.S., Scheller R.H. Amisyn, a novel syntaxin-binding protein that may regulate SNARE complex assembly. J. Biol. Chem. 277:2002;28271-28279.
121. Conner S., Leaf D., Wessel G. Members of the SNARE hypothesis are associated with cortical granule exocytosis in the sea urchin egg. Mol. Reprod. Dev. 48:1997;106-118.
122. Coorssen J.R., Blank P.S., Kolosova I., Backlund P., Zimmerberg J. Are SNARE proteins necessary and sufficient for membrane fusion? Mol. Biol. Cell. 10:1999;219a.
123. Coorssen J.R., Blank P.S., Albertorio F., Bezrukov L., Kolosova I., Chen X., Backlund P., Zimmerberg J. Regulated secretion: SNARE density, vesicle fusion, and calcium dependence. J. Cell Sci. 116:2003;2087-2097.
124. Leikin S., Parsegian V.A., Rau D.C., Rand R.P. Hydration forces. Annu. Rev. Phys. Chem. 44:1993;369-395.
125. Siegel D.P. Energetics of intermediates in membrane fusion: comparison of stalk and inverted micellar intermediate mechanisms. Biophys. J. 65:1993;2124-2140.
126. David D., Sundarababu S., Gerst J.E. Involvement of long chain fatty acid elongation in the trafficking of secretory vesicles in yeast. J. Cell Biol. 143:1998;1167-1182.
127. Grote E., Baba M., Ohsumi Y., Novick P.J. Geranylgeranylated SNAREs are dominant inhibitors of membrane fusion. J. Cell Biol. 151:2000;453-465.
128. Langosh D., Crane J.M., Brosig B., Hellwig A., Tamm L.K., Reed J. Peptide mimics of SNARE transmembrane segments drive membrane fusion depending on their conformational plasticity. J. Mol. Biol. 311:2001;709-721.
129. Vogel S.S., Chernomordik L.V., Zimmerberg J. Calcium-triggered fusion of exocytotic granules requires proteins in only one membrane. J. Biol. Chem. 267:1992;25640-25643.
130. Chanturiya A., Whitaker M., Zimmerberg J. Calcium-induced fusion of sea urchin egg secretory vesicles with planar phospholipid bilayer membranes. Mol. Membr. Biol. 16:1999;89-94.
131. Kagiwada S., Murata M., Hishida R., Tagaya M., Yamashina S., Ohnishi S. In vitro fusion of rabbit liver golgi membranes with liposomes. J. Biol. Chem. 268:1993;1430-1435.
132. Vidal M., Hoekstra D. In vitro fusion of reticulocyte endocytic vesicles with liposomes. J. Biol. Chem. 270:1995;17823-17829.
133. Smit J.M., Li G., Schoen P., Corver J., Bittman R., Lin K.C., Wilschut J. Fusion of alphavirus with liposomes is a non-leaky process. FEBS Lett. 521:2002;62-66.
134. Mizuguchi H., Nakanishi T., Kondoh M., Nakagawa T., Nakanishi M., Matsuyama T., Tsutsumi Y., Nakagawa S., Mayumi T. Fusion of sendai virus with liposome depends on only F protein, but not HN protein. Virus Res. 59:1999;191-201.
135. Hernandez-Jimenez E.I., Razinkov V.I., Mikhalyov I.I., Kozminykh A.V., Cohen F.S., Molotkovsky J.G. Selective labeling of the inner liposome leaflet by fluorescent lipid probes, and studies of liposome fusion with influenza virus. Membr. Cell Biol. 11:1997;515-527.
136. Kozlov M.M., Chernomordik L.V. A mechanism of protein-mediated fusion: coupling between refolding of the influenza hemagglutinin and lipid rearrangements. Biophys. J. 75:1998;1384-1396.
137. Weber T., Zemelman B.V., McNew J.A., Westermann B., Gmachl M., Parlati F., Söllner T.H., Rothman J.E. SNAREpins: minimal machinery for membrane fusion. Cell. 92:1998;759-772.
138. Pabst S., Margittai M., Vainius D., Langen R., Jahn R., Fasshauer D. Rapid and selective binding to the synaptic SNARE complex suggests a modulatory role of complexins in neuroexicytosis. J. Biol. Chem. 277:2002;7838-7848.
139. Lang C., Bruns D., Wenzel D., Riedel D., Holroyd P., Thiele C., Jahn R. SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J. 20:2001;2202-2213.
140. Parlati F., Weber T., McNew J.A., Westermann B., Söllner T.H., Rothman J.E. Rapid and efficient fusion of phospholipid vesicles by the a-core of a SNARE complex in the absence of an N-terminal regulatory domain. Proc. Natl. Acad. Sci. U. S. A. 96:1999;12565-12570.
141. Nickel W., Weber T., McNew J.A., Parlati F., Söllner T.H., Rothman J.E. Content mixing and membrane integrity during membrane fusion driven by pairing of isolated v-SNAREs and t-SNAREs. Proc. Natl. Acad. Sci. U. S. A. 96:1999;12571-12576.
142. Mahal L.K., Sequeira S.M., Gureasko J.M., Söllner T.H. Calcium-independent stimulation of membrane fusion and SNAREpin formation by synaptotagmin I. J. Cell Biol. 158:2002;273-282.
143. Melia T.J., Weber T., McNew J.A., Fisher L.E., Johnston R.J., Parlati F., Mahal L.K., Söllner T.H., Rothman J.E. Regulation of membrane fusion by the membrane-proximal coil of the t-SNARE during zippering of SNAREpins. J. Cell Biol. 158:2002;929-940.
144. Fukuda R., McNew J.A., Weber T., Parlati F., Engel T., Nickel W., Rothman J.E., Söllner T.H. Functional architecture of an intracellular membrane t-SNARE. Nature. 407:2000;198-202.
145. Weber T., Parlati F., McNew J.A., Johnston R.J., Westermann B., Söllner T.H., Rothman J.E. SNAREpins are functionally resistant to disruption by NSF and αSNAP. J. Cell Biol. 149:2000;1063-1072.
146. McNew J.A., Weber T., Parlati F., Johnston R.J., Melia T.J., Söllner T.H., Rothman J.E. Close is not enough: SNARE-dependent membrane fusion requires an active mechanism that transduces force to membrane anchors. J. Cell Biol. 150:2000;105-117.
147. Sutton R.B., Fasshauer D., Jahn R., Brunger A.T. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution. Nature. 395:1998;347-353.
148. Pincet F., Lebeau L., Cribier S. Short-range specific forces are able to induce hemifusion. Eur. Biophys. J. 30:2001;91-97.
149. Cajal Y., Boggs J.M., Jain M.K. Salt-triggered intermembrane exchange of phospholipids and hemifusion by myelin basic protein. Biochemistry. 36:1997;2566-2576.
150. Sabatini B.L., Regehr W.G. Timing of neurotransmission at fast synapses in the mammalian brain. Nature. 384:1996;170-172.
151. Shafi N.I., Vogel S.S., Zimmerberg J. Using caged calcium to study sea urchin egg corticle granule exocytosis in vitro. Methods. 6:1994;82-92.
152. Hu K., Carroll J., Fedorovich S., Rickman C., Sukhodub A., Davletov B. Vesicular restriction of synaptobrevin suggests a role for calcium in membrane fusion. Nature. 415:2002;646-650.
153. Creutz C.E. Cis-unsaturated fatty acids induce the fusion of chromaffin granules aggregated by synexin. J. Cell Biol. 91:1981;247-256.
154. Schenkman S., De Araujo P.S., Sesso A., Quina F.H., Chaimovich H. A kinetic and structural study of two-step aggregation and fusion of neutral phospholipid vesicles promoted by serum albumin at low pH. Chem. Phys. Lipids. 28:1981;165-180.
155. Blumenthal R., Henkart M., Steer C.J. Clathrin-induced pH-dependent fusion of phosphatidylcholine vesicles. J. Biol. Chem. 258:1983;3409-3415.
156. 2+-induced fusion of phosphatidate-containing membranes. Biochim. Biophys. Acta. 730:1983;391-394.
157. Young T.M., Young J.D. Protein-mediated intermembrane contact facilitates fusion of lipid vesicles with planar bilayers. Biochim. Biophys. Acta. 775:1984;441-445.
158. Fujii G., Selsted M.E., Eisenberg D. Defensins promote fusion and lysis of negatively charged membranes. Protein Sci. 2:1993;1301-1312.
159. Glaser P.E., Gross R.W. Rapid plasmenylethanolamine-selective fusion of membrane bilayers catalyzed by an isoform of glyceraldehyde-3-phosphate dehydrogenase: discrimination between glycolytic and fusogenic roles of individual isoforms. Biochemistry. 34:1995;12193-12203.
160. 2+-dependent fusogen in human neutrophil cytosol. J. Leukoc. Biol. 63:1998;331-336.
161. Otter-Nilsson M., Hendriks R., Pecheur-Huet E.I., Hoekstra D., Nilsson T. Cytosolic ATPases, p97 and NSF, are sufficient to mediate rapid membrane fusion. EMBO J. 18:1999;2074-2083.
162. Brügger B., Nickel W., Weber T., Parlati F., McNew J.A., Rothman J.E., Söllner T.H. Putative fusogenic activity of NSF is restricted to a lipid mixture whose coalescence is also triggered by other factors. EMBO J. 19:2000;1272-1278.
163. Agirre A., Nir S., Nieva J.L., Dijkstra J. Induction of aggregation and fusion of cholesterol-containing membrane vesicles by an anti-cholesterol monoclonal antibody. J. Lipid Res. 41:2000;621-628.
164. Cho S.J., Kelly M., Rognlien K.T., Cho J.A., Horber J.K.H., Jena B.P. SNAREs in opposing bilayers interact in a circular array to form conducting pores. Biophys. J. 83:2002;2522-2527.
165. Pécheur E.I., Martin I., Maier O., Bakowski U., Ruysschaert J.M., Hoekstra D. Phospholipid species act as modulators in p97/p47-mediated fusion of golgi membranes. Biochemistry. 41:2002;9813-9823.
166. Haque M.E., McIntosh T.J., Lentz B.R. Influence of lipid composition on physical properties and PEG-mediated fusion of curved and uncurved model membrane vesicles: Nature's own" fusogenic lipid bilayer. Biochemistry. 40:2001;4340-4348.
167. Bracher A., Kadlec J., Betz H., Weissenhorn W. X-ray structure of a neuronal complexin-SNARE complex from squid. J. Biol. Chem. 277:2002;26517-26523.
168. Archer D.A., Graham M.E., Burgoyne R.D. Complexin regulates the closure of the fusion pore during regulated vesicle exocytosis. J. Biol. Chem. 277:2002;18249-18252.
169. Parlati F., McNew J.A., Fukuda R., Miller R., Söllner T.H., Rothman J.E. Topological restriction of SNARE-dependent membrane fusion. Nature. 407:2000;194-198.
170. Pelham H.R.B. SNAREs and the specificity of membrane fusion. Trends Cell Biol. 11:2001;99-101.
171. Gutierrez L.M., Viniegra S., Rueda J., Ferrer-Montiel A.V., Canaves J.M., Montal M. A peptide that mimics the C-terminal sequence of SNAP-25 inhibits secretory vesicle docking in chromaffin cells. J. Biol. Chem. 272:1997;2634-2639.
172. Apland J.P., Biser J.A., Adler M., Ferrer-Montiel A.V., Montal M., Filbert M.G. Peptides that mimic the carboxy-terminal domain of SNAP-25 block acetylcholine release at an aplysia synapse. J. Appl. Toxicol. 19:1999;S23-S26.
173. Kozlov M.M., Markin V.S. Possible mechanism of membrane fusion. Biofizika. 28:1983;242-247.
174. Chernomordik L., Chanturiya A., Green J., Zimmerberg J. The hemifusion intermediate and its conversion to complete fusion: regulation by membrane composition. Biophys. J. 69:1995;922-929.
175. Rand R.P. Interacting phospholipid bilayers: measured forces and induced structural changes. Annu. Rev. Biophys. Bioeng. 10:1981;277-314.
176. Gruner S.M. Intrinsic curvature hypothesis for biomembrane lipid composition: a role for non-bilayer lipids. Proc. Natl. Acad. Sci. U. S. A. 82:1985;3665-3669.
177. Gawrisch K., Parsegian V.A., Hajduk D.A., Tate M.W., Gruner S.M. Energetics of a hexagonal-lamellar-hexagonal-phase transition sequence in dioleoylphosphatidylethanolamine membranes. Biochemistry. 31:1992;2856-2864.
178. Kozlov M.M., Leikin S., Rand R.P. Bending, hydration and interstitial energies quantitatively account for the hexagonal-lamellar-hexagonal reentrant phase transition in dioleoylphosphatidylethanolamine. Biophys. J. 67:1994;1603-1611.
179. Chen Z., Rand R.P. Comparative study of the effects of several
180. Luzzati V., Husson F. The structure of the liquid-crystalline phases of lipid-water systems. J. Cell Biol. 12:1962;207-219.
181. Chernomordik L., Kozlov M.M., Zimmerberg J. Lipids in biological membrane fusion. J. Membr. Biol. 146:1995;1-14.
182. Yang L., Huang H.W. Observation of a membrane fusion intermediate structure. Science. 297:2002;1877-1879.
183. Marrink S.J., Tieleman P. Molecular dynamics simulation of spontaneous membrane fusion during a cubic-hexagonal phase transition. Biophys. J. 83:2002;2386-2392.
184. 2+-, GTP- and pH-dependent fusion of biological membranes. FEBS Lett. 318:1993;71-76.
185. Vogel S.S., Leikina E.A., Chernomordik L.V. Lysophosphatidylcholine reversibly arrests exocytosis and viral fusion at a stage between triggering and membrane merger. J. Biol. Chem. 268:1993;25764-25768.
186. Johns L.M., Levitan E.S., Shelden E.A., Holz R.W., Axelrod D. Restriction of secretory granule motion near the plasma membrane of chromaffin cells. J. Cell Biol. 153:2001;177-190.
187. Pevsner J., Hsu S.C., Braun J.E.A., Calakos N., Ting A.E., Bennett M.K., Scheller R.H. Specificity and regulation of a synaptic vesicle docking complex. Neuron. 13:1994;353-361.
188. Takahashi N., Kishimoto T., Nemoto T., Kadowaki T., Kasai H. Fusion pore dynamics and insulin granule exocytosis in the pancreatic islet. Science. 297:2002;1349-1352.
189. Bezprozvanny I., Scheller R.H., Tsien R.W. Functional impact of syntaxin on gating of N-type and Q-type calcium channels. Nature. 378:1995;623-626.
190. 2+ channels. Proc. Natl. Acad. Sci. U. S. A. 95:1998;14523-14528.
191. 2+ channels and SNARE proteins in neurotransmitter release. Ann. N.Y. Acad. Sci. 868:1999;144-159.
192. 2+ channels, cytoplasmic messengers and proteins of the synaptic vesicle release complex. Trends Pharmacol. Sci. 22:2001;519-522.
193. Jarvis S.E., Zamponi G.W. Distinct molecular determinants govern syntaxin1A-mediated inactivation and G-protein inhibition of N-type calcium channels. J. Neurosci. 21:2001;2939-2948.
194. Stanley E.F., Mirotznik R.R. Cleavage of syntaxin prevents G-protein regulation of presynaptic calcium channels. Nature. 385:1997;340-343.
195. Ji J., Tsuk S., Salapatek A.M.F., Huang X., Chikvashvili D., Pasyk E.A., Kang Y., Sheu L., Tsushima R., Diamant N., Trimble W.S., Lotan I., Gaisano H.Y. The 25-kDa synaptosome-associated protein (SNAP-25) binds and inhibits delayed rectifier potassium channels in secretory cells. J. Biol. Chem. 277:2002;20195-20204.
196. + channel by syntaxin 1A requires the physical interaction of Gβγ with the channel. J. Biol. Chem. 277:2002;34909-34917.
197. Cormet-Boyaka E., Di A., Chang S.Y., Naren A.P., Tousson A., Nelson D.J., Kirk K.L. CFTR chloride channels are regulated by a SNAP-23/syntaxin 1A complex. Proc. Natl. Acad. Sci. U. S. A. 99:2002;12477-12482.
198. Spafford J.D., Munno D.W., Van Nierop P., Feng Z.P., Jarvis S.E., Gallin W.J., Smit A.B., Zamponi G.W., Syed N.I. Calcium channel structural determinants of synaptic transmission between identified invertebrate neurons. J. Biol. Chem. 278:2003;4258-4267.
199. 2+ channel is functionally coupled to the exocytotic machinery. Proc. Natl. Acad. Sci. U. S. A. 96:1999;248-253.
200. 2+ sensor of fast neurotransmitter release. Cell. Mol. Neurobiol. 21:2001;717-731.
201. Lang T., Margittai M., Holzler H., Jahn R. SNAREs in native plasma membranes are active and readily form core complexes with endogenous and exogenous SNAREs. J. Cell Biol. 158:2002;751-760.
202. Fasshauer D., Antonin W., Subramaniam V., Jahn R. SNARE assembly and disassembly exhibit a pronounced hysteresis. Nat. Struct. Biol. 9:2002;144-151.
203. Hagan S.J., Hofrichter J., Szabo A., Eaton W.A. Diffusion-limited contact formation in unfolded cytochrome c: estimating the maximum rate of protein folding. Proc. Natl. Acad. Sci. U. S. A. 93:1996;11615-11617.
204. Wittung-Stafshede P., Lee J.C., Winkler J.R., Gray H.B. Cytochrome b562 folding triggered by electron transfer: approaching the speed limit for formation of a four-helix-bundle protein. Proc. Natl. Acad. Sci. U. S. A. 96:1999;6587-6590.
205. Levy Y., Hanan E., Solomon B., Becker O.M. Helix-coil transition of PrP106-126: molecular dynamic study. Proteins. 45:2001;382-396.
206. Siegel D.P., Green W.J., Talmon Y. The mechanisms of lamellar-to-inverted hexagonal phase transitions: a study using temperature-jump cryo-electron microscopy. Biophys. J. 66:1994;402-412.
207. 2+, MgATP and botulinum toxin type A. J. Cell Sci. 115:2002;667-673.
208. 2+-dependent regulation of synaptic SNARE complex assembly via a calmodulin- and phospholipid-binding domain or synaptobrevin. Proc. Natl. Acad. Sci. U. S. A. 97:2000;9695-9700.
209. Palade G. Intracellular aspects of the process of protein synthesis. Science. 189:1975;347-358.