Opposing functions of two sub-domains of the SNARE-complex in neurotransmission

EMBO Journal

Volumn 29, Issue 15, 2010, Pages 2477-2490

  Weber, Jens P ^a   Reim, Kerstin ^b   Sørensen, Jakob B ^a,c  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

exocytosis; SNAP 25; SNARE complex; spontaneous neurotransmitter release; synaptic transmission

Indexed keywords

SNARE PROTEIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; HIPPOCAMPUS; MOUSE; MUTANT; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION;

AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; GENE DELETION; HIPPOCAMPUS; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; MUTATION; SEQUENCE ALIGNMENT; SYNAPTIC TRANSMISSION; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25;

MUS;

EID: 77955432137     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.130     Document Type: Article

References (75)

1. Basu J, Betz A, Brose N, Rosenmund C (2007) Munc13-1 C1 domain activation lowers the energy barrier for synaptic vesicle fusion. J Neurosci 27: 1200-1210
2. Baumert M, Maycox PR, Navone F, De Camilli P, Jahn R (1989) Synaptobrevin: an integral membrane protein of 18,000 daltons present in small synaptic vesicles of rat brain. EMBO J 8: 379-384
3. Bekkers JM, Stevens CF (1991) Excitatory and inhibitory autaptic currents in isolated hippocampal neurons maintained in cell culture. Proc Natl Acad Sci USA 88: 7834-7838
4. Bennett MK, Calakos N, Scheller RH (1992) Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257: 255-259
5. Birks RI, Macintosh FC (1957) Acetylcholine metabolism at nerveendings. Br Med Bull 13: 157-161
6. Bronk P, Deak F, Wilson MC, Liu X, Sudhof TC, Kavalali ET (2007) Differential effects of SNAP-25 deletion on Ca2+-dependent and Ca2+-independent neurotransmission. J Neurophysiol 98: 794-806
7. Capogna M, McKinney RA, O'Connor V, Gahwiler BH, Thompson SM (1997) Ca2+ or Sr2+ partially rescues synaptic transmission in hippocampal cultures treated with botulinum toxin A and C, but not tetanus toxin. J Neurosci 17: 7190-7202
8. Chen X, Tomchick DR, Kovrigin E, Arac D, Machius M, Sudhof TC, Rizo J (2002) Three-dimensional structure of the complexin/SNARE complex. Neuron 33: 397-409
9. Criado M, Gil A, Viniegra S, Gutierrez LM (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
10. De Wit H, Walter AM, Milosevic I, Gulyas-Kovacs A, Riedel D, Sorensen JB, Verhage M (2009) Synaptotagmin-1 docks secretory vesicles to syntaxin-1/SNAP-25 acceptor complexes. Cell 138: 935-946
11. Deak F, Shin OH, Kavalali ET, Sudhof TC (2006) Structural determinants of synaptobrevin 2 function in synaptic vesicle fusion. J Neurosci 26: 6668-6676
12. Deak F, Xu Y, Chang WP, Dulubova I, Khvotchev M, Liu X, Sudhof TC, Rizo J (2009) Munc18-1 binding to the neuronal SNARE complex controls synaptic vesicle priming. J Cell Biol 184: 751-764
13. Deitcher DL, Ueda A, Stewart BA, Burgess RW, Kidokoro Y, Schwarz TL (1998) Distinct requirements for evoked and spontaneous release of neurotransmitter are revealed by mutations in the Drosophila gene neuronal-synaptobrevin. J Neurosci 18: 2028-2039
14. Delgado-Martinez I, Nehring RB, Sorensen JB (2007) Differential abilities of SNAP-25 homologs to support neuronal function. J Neurosci 27: 9380-9391
15. Elferink LA, Trimble WS, Scheller RH (1989) Two vesicle-associated membrane protein genes are differentially expressed in the rat central nervous system. J Biol Chem 264: 11061-11064
16. Fasshauer D, Margittai M (2004) A transient N-terminal interaction of SNAP-25 and syntaxin nucleates SNARE assembly. J Biol Chem 279: 7613-7621
17. Fasshauer D, Sutton RB, Brunger AT, Jahn R (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
18. Finley MF, Patel SM, Madison DV, Scheller RH (2002) The core membrane fusion complex governs the probability of synaptic vesicle fusion but not transmitter release kinetics. J Neurosci 22: 1266-1272
19. Geppert M, Goda Y, Hammer RE, Li C, Rosahl TW, Stevens CF, Sudhof TC (1994) Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell 79: 717-727
20. Gil A, Gutierrez LM, Carrasco-Serrano C, Alonso MT, Viniegra S, Criado M (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
21. Giraudo CG, Garcia-Diaz A, Eng WS, Chen Y, Hendrickson WA, Melia TJ, Rothman JE (2009) Alternative zippering as an on-off switch for SNARE-mediated fusion. Science 323: 512-516
22. Glitsch MD (2008) Spontaneous neurotransmitter release and Ca2+\how spontaneous is spontaneous neurotransmitter release? Cell Calcium 43: 9-15
23. Grosse G, Grosse J, Tapp R, Kuchinke J, Gorsleben M, Fetter I, Hohne-Zell B, Gratzl M, Bergmann M (1999) SNAP-25 requirement for dendritic growth of hippocampal neurons. J Neurosci Res 56: 539-546
24. Hanson PI, Roth R, Morisaki H, Jahn R, Heuser JE (1997) Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch electron microscopy. Cell 90: 523-535
25. Hessler NA, Shirke AM, Malinow R (1993) The probability of transmitter release at a mammalian central synapse. Nature 366: 569-572
26. Holt M, Varoqueaux F, Wiederhold K, Takamori S, Urlaub H, Fasshauer D, Jahn R (2006) Identification of SNAP-47, a novel Qbc-SNARE with ubiquitous expression. J Biol Chem 281: 17076-17083
27. Huntwork S, Littleton JT (2007) A complexin fusion clamp regulates spontaneous neurotransmitter release and synaptic growth. Nat Neurosci 10: 1235-1237
28. Jahn R, Scheller RH (2006) SNAREs\engines for membrane fusion. Nat Rev Mol Cell Biol 7: 631-643
29. Junge HJ, Rhee JS, Jahn O, Varoqueaux F, Spiess J, Waxham MN, Rosenmund C, Brose N (2004) Calmodulin and Munc13 form a Ca2+ sensor/effector complex that controls short-term synaptic plasticity. Cell 118: 389-401
30. Kerr AM, Reisinger E, Jonas P (2008) Differential dependence of phasic transmitter release on synaptotagmin 1 at GABAergic and glutamatergic hippocampal synapses. Proc Natl Acad Sci USA 105: 15581-15586
31. Lan JY, Skeberdis VA, Jover T, Grooms SY, Lin Y, Araneda RC, Zheng X, Bennett MV, Zukin RS (2001) Protein kinase C modulates NMDA receptor trafficking and gating. Nat Neurosci 4: 382-390
32. Littleton JT, Stern M, Schulze K, Perin M, Bellen HJ (1993) Mutational analysis of Drosophila synaptotagmin demonstrates its essential role in Ca(2+)-activated neurotransmitter release. Cell 74: 1125-1134
33. Liu H, Dean C, Arthur CP, Dong M, Chapman ER (2009) Autapses and networks of hippocampal neurons exhibit distinct synaptic transmission phenotypes in the absence of synaptotagmin I. J Neurosci 29: 7395-7403
34. Lou X, Korogod N, Brose N, Schneggenburger R (2008) Phorbol esters modulate spontaneous and Ca2+-evoked transmitter release via acting on both Munc13 and protein kinase C. J Neurosci 28: 8257-8267
35. Maximov A, Tang J, Yang X, Pang ZP, Sudhof TC (2009) Complexin controls the force transfer from SNARE complexes to membranes in fusion. Science 323: 516-521
36. McNew JA,Weber T, Engelman DM, Sollner TH, Rothman JE (1999) The length of the flexible SNAREpin juxtamembrane region is a critical determinant of SNARE-dependent fusion. Mol Cell 4: 415-421
37. Moulder KL, Mennerick S (2005) Reluctant vesicles contribute to the total readily releasable pool in glutamatergic hippocampal neurons. J Neurosci 25: 3842-3850
38. Oyler GA, Higgins GA, Hart RA, Battenberg E, Billingsley M, Bloom FE, Wilson MC (1989) The identification of a novel synaptosomal-associated protein, SNAP-25, differentially expressed by neuronal subpopulations. J Cell Biol 109: 3039-3052
39. Pabst S, Margittai M, Vainius D, Langen R, Jahn R, Fasshauer D (2002) Rapid and selective binding to the synaptic SNARE complex suggests a modulatory role of complexins in neuroexocytosis. J Biol Chem 277: 7838-7848
40. Pang ZP, Sun J, Rizo J, Maximov A, Sudhof TC (2006) Genetic analysis of synaptotagmin 2 in spontaneous and Ca2+-triggered neurotransmitter release. EMBO J 25: 2039-2050
41. Reim K, Mansour M, Varoqueaux F, McMahon HT, Sudhof TC, Brose N, Rosenmund C (2001) Complexins regulate a late step in Ca2+-dependent neurotransmitter release. Cell 104: 71-81
42. Reim K, Wegmeyer H, Brandstatter JH, Xue M, Rosenmund C, Dresbach T, Hofmann K, Brose N (2005) Structurally and functionally unique complexins at retinal ribbon synapses. J Cell Biol 169: 669-680
43. Rizo J, Rosenmund C (2008) Synaptic vesicle fusion. Nat Struct Mol Biol 15: 665-674
44. Rosenmund C, Clements JD, Westbrook GL (1993) Nonuniform probability of glutamate release at a hippocampal synapse. Science 262: 754-757
45. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16: 1197-1207
46. Sakaba T (2006) Roles of the fast-releasing and the slowly releasing vesicles in synaptic transmission at the calyx of held. J Neurosci 26: 5863-5871
47. Sakaba T, Neher E (2001) Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse. Neuron 32: 1119-1131
48. Sakaba T, Stein A, Jahn R, Neher E (2005) Distinct kinetic changes in neurotransmitter release after SNARE protein cleavage. Science 309: 491-494
49. Schneggenburger R, Meyer AC, Neher E (1999) Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23: 399-409
50. Schoch S, Deak F, Konigstorfer A, Mozhayeva M, Sara Y, Sudhof TC, Kavalali ET (2001) SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 294: 1117-1122
51. Selak S, Paternain AV, Aller MI, Pico E, Rivera R, Lerma J (2009) A role for SNAP25 in internalization of kainate receptors and synaptic plasticity. Neuron 63: 357-371
52. Shen J, Tareste DC, Paumet F, Rothman JE, Melia TJ (2007) Selective activation of cognate SNAREpins by Sec1/Munc18 proteins. Cell 128: 183-195
53. Siddiqui TJ, Vites O, Stein A, Heintzmann R, Jahn R, Fasshauer D (2007) Determinants of synaptobrevin regulation in membranes. Mol Biol Cell 18: 2037-2046
54. Sorensen JB (2004) Formation, stabilisation and fusion of the readily releasable pool of secretory vesicles. Pflugers Arch 448: 347-362
55. Sorensen JB (2009) Conflicting views on the membrane fusion machinery and the fusion pore. Annu Rev Cell Dev Biol 25: 513-537
56. Sorensen JB, Wiederhold K, Muller EM, Milosevic I, Nagy G, De Groot BL, Grubmuller H, Fasshauer D (2006) Sequential N-to Cterminal SNARE complex assembly drives priming and fusion of secretory vesicles. EMBO J 25: 955-966
57. Steegmaier M, Yang B, Yoo JS, Huang B, Shen M, Yu S, Luo Y, Scheller RH (1998) Three novel proteins of the syntaxin/SNAP-25 family. J Biol Chem 273: 34171-34179
58. Stevens CF, Wesseling JF (1998) Activity-dependent modulation of the rate at which synaptic vesicles become available to undergo exocytosis. Neuron 21: 415-424
59. Stevens CF, Williams JH (2007) Discharge of the readily releasable pool with action potentials at hippocampal synapses. J Neurophysiol 98: 3221-3229
60. Sudhof TC, Rothman JE (2009) Membrane fusion: grappling with SNARE and SM proteins. Science 323: 474-477
61. Sutton RB, Fasshauer D, Jahn R, Brunger AT (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395: 347-353
62. Tafoya LC, Mameli M, Miyashita T, Guzowski JF, Valenzuela CF, Wilson MC (2006) Expression and function of SNAP-25 as a universal SNARE component in GABAergic neurons. J Neurosci 26: 7826-7838
63. Trudeau LE, Fang Y, Haydon PG (1998) Modulation of an early step in the secretory machinery in hippocampal nerve terminals. Proc Natl Acad Sci USA 95: 7163-7168
64. Verderio C, Pozzi D, Pravettoni E, Inverardi F, Schenk U, Coco S, Proux-Gillardeaux V, Galli T, Rossetto O, Frassoni C, Matteoli M (2004) SNAP-25 modulation of calcium dynamics underlies differences in GABAergic and glutamatergic responsiveness to depolarization. Neuron 41: 599-610
65. Voets T, Toonen RF, Brian EC, De Wit H, Moser T, Rettig J, Sudhof TC, Neher E, Verhage M (2001) Munc18-1 promotes large densecore vesicle docking. Neuron 31: 581-591
66. Walter AM, Wiederhold K, Bruns D, Fasshauer D, Sorensen JB (2010) Synaptobrevin N-terminally bound to syntaxin-SNAP-25 defines the primed vesicle state in regulated exocytosis. J Cell Biol 188: 401-413
67. Wang LY, Kaczmarek LK (1998) High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394: 384-388
68. Washbourne P, Thompson PM, Carta M, Costa ET, Mathews JR, Lopez-Bendito G, Molnar Z, Becher MW, Valenzuela CF, Partridge LD, Wilson MC (2002) Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat Neurosci 5: 19-26
69. Wasser CR, Kavalali ET (2009) Leaky synapses: regulation of spontaneous neurotransmission in central synapses. Neuroscience 158: 177-188
70. Wei S, Xu T, Ashery U, Kollewe A, Matti U, Antonin W, Rettig J, Neher E (2000) Exocytotic mechanism studied by truncated and zero layer mutants of the C-terminus of SNAP-25. EMBO J 19: 1279-1289
71. Wierda KD, Toonen RF, De Wit H, Brussaard AB, Verhage M (2007) Interdependence of PKC-dependent and PKC-independent pathways for presynaptic plasticity. Neuron 54: 275-290
72. Xu J, Pang ZP, Shin OH, Sudhof TC (2009) Synaptotagmin-1 functions as a Ca2+ sensor for spontaneous release. Nat Neurosci 12: 759-766
73. Xue M, Reim K, Chen X, Chao HT, Deng H, Rizo J, Brose N, Rosenmund C (2007) Distinct domains of complexin I differentially regulate neurotransmitter release. Nat Struct Mol Biol 14: 949-958
74. Young Jr SM (2005) Proteolysis of SNARE proteins alters facilitation and depression in a specific way. Proc Natl Acad Sci USA 102: 2614-2619
75. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405