SNARE bundle and syntaxin N-peptide constitute a minimal complement for Munc18-1 activation of membrane fusion

Journal of Cell Biology

Volumn 190, Issue 1, 2010, Pages 55-63

  Shen, Jingshi ^a   Rathore, Shailendra S ^a   Khandan, Lavan ^b   Rothman, James E ^b  

^a UNIVERSITY OF COLORADO   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; MUNC18 PROTEIN; PROTEIN SUBUNIT; SNARE PROTEIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNTAXIN;

ARTICLE; BILAYER MEMBRANE; COMPLEX FORMATION; INTRACELLULAR MEMBRANE; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SYNAPTIC MEMBRANE;

AMINO ACID MOTIFS; ANIMALS; MEMBRANE FUSION; MICE; MUNC18 PROTEINS; MUTATION; PEPTIDES; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SYNAPTOSOMAL-ASSOCIATED PROTEIN 25; SYNTAXIN 1;

EID: 77954715092     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.201003148     Document Type: Article

References (62)

1. Antonin, W., I. Dulubova, D. Arac, S. Pabst, J. Plitzner, J. Rizo, and R. Jahn. 2002. The N-terminal domains of syntaxin 7 and vti1b form three-helix bundles that differ in their ability to regulate SNARE complex assembly. J. Biol. Chem. 277:36449-36456. doi:10.1074/jbc.M204369200
2. Basu, J., N. Shen, I. Dulubova, J. Lu, R. Guan, O. Guryev, N.V. Grishin, C. Rosenmund, and J. Rizo. 2005. A minimal domain responsible for Munc13 activity. Nat. Struct. Mol. Biol. 12:1017-1018.
3. Bergink, S., and S. Jentsch. 2009. Principles of ubiquitin and SUMO modifications in DNA repair. Nature. 458:461-467. doi:10.1038/nature07963
4. 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 (Pubitemid 40961796)
5. Bracher, A., and W. Weissenhorn. 2002. Structural basis for the Golgi membrane recruitment of Sly1p by Sed5p. EMBO J. 21:6114-6124. doi:10.1093/emboj/cdf608 (Pubitemid 35415328)
6. Brunger, A.T. 2006. Structure and function of SNARE and SNARE-interacting proteins. Q. Rev. Biophys. 38:1-47. doi:10.1017/S0033583505004051
7. Burkhardt, P., D.A. Hattendorf, W.I. Weis, and D. Fasshauer. 2008. Munc18a controls SNARE assembly through its interaction with the syntaxin N-peptide. EMBO J. 27:923-933. doi:10.1038/emboj.2008.37 (Pubitemid 351508147)
8. 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
9. 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
10. Dulubova, I., T. Yamaguchi, Y. Gao, S.W. Min, I. Huryeva, T.C. Südhof, and J. Rizo. 2002. How Tlg2p/syntaxin 16 'snares' Vps45. EMBO J. 21:3620-3631. doi:10.1093/emboj/cdf381
11. Dulubova, I., T. Yamaguchi, D. Arac, H. Li, I. Huryeva, S.W. Min, J. Rizo, and T.C. Südhof. 2003. Convergence and divergence in the mechanism of SNARE binding by Sec1/Munc18-like proteins. Proc. Natl. Acad. Sci. USA. 100:32-37. doi:10.1073/pnas.232701299
12. Dulubova, I., M. Khvotchev, S. Liu, I. Huryeva, T.C. Südhof, and J. Rizo. 2007. Munc18-1 binds directly to the neuronal SNARE complex. Proc. Natl. Acad. Sci. USA. 104:2697-2702. doi:10.1073/pnas.0611318104
13. Fernandez, I., J. Ubach, I. Dulubova, X. Zhang, T.C. Südhof, and J. Rizo. 1998. Three-dimensional structure of an evolutionarily conserved N-terminal domain of syntaxin 1A. Cell. 94:841-849. doi:10.1016/S0092-8674(00) 81742-0 (Pubitemid 28436015)
14. Fukuda, R., J.A. McNew, T. Weber, F. Parlati, T. Engel, W. Nickel, J.E. Rothman, and T.H. Söllner. 2000. Functional architecture of an intracellular membrane t-SNARE. Nature. 407:198-202. doi:10.1038/35025084
15. 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
16. 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
17. Harrison, S.D., K. Broadie, J. van de Goor, and G.M. Rubin. 1994. Mutations in the Drosophila Rop gene suggest a function in general secretion and synaptic transmission. Neuron. 13:555-566. doi:10.1016/0896-6273(94)90025-6
18. Hu, C., M. Ahmed, T.J. Melia, T.H. Söllner, T. Mayer, and J.E. Rothman. 2003. Fusion of cells by flipped SNAREs. Science. 300:1745-1749. doi:10.1126/science.1084909
19. Hu, S.H., C.F. Latham, C.L. Gee, D.E. James, and J.L. Martin. 2007. Structure of the Munc18c/Syntaxin4 N-peptide complex defines universal features of the N-peptide binding mode of Sec1/Munc18 proteins. Proc. Natl. Acad. Sci. USA. 104:8773-8778. doi:10.1073/pnas.0701124104
20. Jackson, M.B., and E.R. Chapman. 2006. Fusion pores and fusion machines in Ca2+-triggered exocytosis. Annu. Rev. Biophys. Biomol. Struct. 35:135-160. doi:10.1146/annurev.biophys.35.040405.101958
21. Jahn, R. 2004. Principles of exocytosis and membrane fusion. Ann. N. Y. Acad. Sci. 1014:170-178. doi:10.1196/annals.1294.018
22. Jahn, R., and R.H. Scheller. 2006. SNAREs - engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7:631-643. doi:10.1038/nrm2002
23. Jahn, R., and T.C. Südhof. 1994. Synaptic vesicles and exocytosis. Annu. Rev. Neurosci. 17:219-246. doi:10.1146/annurev.ne.17.030194.001251
24. 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
25. Johnson, J.R., P. Ferdek, L.Y. Lian, J.W. Barclay, R.D. Burgoyne, and A. Morgan. 2009. Binding of UNC-18 to the N-terminus of syntaxin is essential for neurotransmission in Caenorhabditis elegans. Biochem. J. 418:73-80. doi:10.1042/BJ20081956
26. Koh, T.W., and H.J. Bellen. 2003. Synaptotagmin I, a Ca2+ sensor for neurotransmitter release. Trends Neurosci. 26:413-422. doi:10.1016/S0166- 2236(03)00195-4
27. Latham, C.F., J.A. Lopez, S.H. Hu, C.L. Gee, E. Westbury, D.H. Blair, C.J. Armishaw, P.F. Alewood, N.J. Bryant, D.E. James, and J.L. Martin. 2006. Molecular dissection of the Munc18c/syntaxin4 interaction: implications for regulation of membrane trafficking. Traffic. 7:1408-1419. doi:10.1111/j.1600- 0854.2006.00474.x
28. Martens, S., M.M. Kozlov, and H.T. McMahon. 2007. How synaptotagmin promotes membrane fusion. Science. 316:1205-1208. doi:10.1126/science.1142614 (Pubitemid 46877485)
29. McEwen, J.M., and J.M. Kaplan. 2008. UNC-18 promotes both the anterograde trafficking and synaptic function of syntaxin. Mol. Biol. Cell. 19:3836-3846. doi:10.1091/mbc.E08-02-0160
30. 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
31. Mima, J., C.M. Hickey, H. Xu, Y. Jun, and W. Wickner. 2008. Reconstituted membrane fusion requires regulatory lipids, SNAREs and synergistic SNARE chaperones. EMBO J. 27:2031-2042. doi:10.1038/emboj.2008.139
32. Misura, K.M., R.H. Scheller, and W.I. Weis. 2000. Three-dimensional structure of the neuronal-Sec1-syntaxin 1a complex. Nature. 404:355-362. doi:10.1038/35006120
33. Novick, P., and R. Schekman. 1979. Secretion and cell-surface growth are blocked in a temperature-sensitive mutant of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 76:1858-1862. doi:10.1073/pnas.76.4.1858
34. Parlati, F., T. Weber, J.A. McNew, B. Westermann, T.H. Söllner, and J.E. Rothman. 1999. Rapid and efficient fusion of phospholipid vesicles by the alpha-helical core of a SNARE complex in the absence of an N-terminal regulatory domain. Proc. Natl. Acad. Sci. USA. 96:12565-12570. doi:10.1073/pnas.96.22. 12565
35. 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
36. Rickman, C., and R.R. Duncan. 2010. Munc18/Syntaxin interaction kinetics control secretory vesicle dynamics. J. Biol. Chem. 285:3965-3972. doi:10.1074/jbc.M109.040402
37. Rickman, C., C.N. Medine, A. Bergmann, and R.R. Duncan. 2007. Functionally and spatially distinct modes of munc18-syntaxin 1 interaction. J. Biol. Chem. 282:12097-12103. doi:10.1074/jbc.M700227200
38. Rodkey, T.L., S. Liu, M. Barry, and J.A. McNew. 2008. Munc18a scaffolds SNARE assembly to promote membrane fusion. Mol. Biol. Cell. 19:5422-5434. doi:10.1091/mbc.E08-05-0538
39. Scott, B.L., J.S. Van Komen, H. Irshad, S. Liu, K.A. Wilson, and J.A. McNew. 2004. Sec1p directly stimulates SNARE-mediated membrane fusion in vitro. J. Cell Biol. 167:75-85. doi:10.1083/jcb.200405018
40. Shen, J., D.C. Tareste, F. Paumet, J.E. Rothman, and T.J. Melia. 2007. Selective activation of cognate SNAREpins by Sec1/Munc18 proteins. Cell. 128:183-195. doi:10.1016/j.cell.2006.12.016 (Pubitemid 46048894)
41. Söllner, T., S.W. Whiteheart, M. Brunner, H. Erdjument-Bromage, S. Geromanos, P. Tempst, and J.E. Rothman. 1993. SNAP receptors implicated in vesicle targeting and fusion. Nature. 362:318-324. doi:10.1038/362318a0 (Pubitemid 23101303)
42. Sørensen, J.B., U. Matti, S.H. Wei, R.B. Nehring, T. Voets, U. Ashery, T. Binz, E. Neher, and J. Rettig. 2002. The SNARE protein SNAP-25 is linked to fast calcium triggering of exocytosis. Proc. Natl. Acad. Sci. USA. 99:1627-1632. doi:10.1073/pnas.251673298
43. Stein, A., G. Weber, M.C. Wahl, and R. Jahn. 2009. Helical extension of the neuronal SNARE complex into the membrane. Nature. 460:525-528.
44. Südhof, T.C. 2004. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27:509-547. doi:10.1146/annurev.neuro.26.041002.131412
45. 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
46. 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
47. 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 (Pubitemid 44380295)
48. Tareste, D., J. Shen, T.J. Melia, and J.E. Rothman. 2008. SNAREpin/Munc18 promotes adhesion and fusion of large vesicles to giant membranes. Proc. Natl. Acad. Sci. USA. 105:2380-2385. doi:10.1073/pnas.0712125105
49. Toonen, R.F., and M. Verhage. 2007. Munc18-1 in secretion: lonely Munc joins SNARE team and takes control. Trends Neurosci. 30:564-572.
50. Ungar, D., and F.M. Hughson. 2003. SNARE protein structure and function. Annu. Rev. Cell Dev. Biol. 19:493-517. doi:10.1146/annurev.cellbio.19.110701. 155609
51. Verhage, M., A.S. Maia, J.J. Plomp, A.B. Brussaard, J.H. Heeroma, H. Vermeer, R.F. Toonen, R.E. Hammer, T.K. van den Berg, M. Missler, et al. 2000. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science. 287:864-869. doi:10.1126/science.287.5454.864
52. Voets, T., R.F. Toonen, E.C. Brian, H. de Wit, T. Moser, J. Rettig, T.C. Südhof, E. Neher, and M. Verhage. 2001. Munc18-1 promotes large dense-core vesicle docking. Neuron. 31:581-591. doi:10.1016/S0896-6273(01)00391-9 (Pubitemid 32835113)
53. Walch-Solimena, C., J. Blasi, L. Edelmann, E.R. Chapman, G.F. von Mollard, and R. Jahn. 1995. The t-SNAREs syntaxin 1 and SNAP-25 are present on organelles that participate in synaptic vesicle recycling. J. Cell Biol. 128:637-645. doi:10.1083/jcb.128.4.637
54. Walter, A.M., K. Wiederhold, D. Bruns, D. Fasshauer, and J.B. Sørensen. 2010. Synaptobrevin N-terminally bound to syntaxin-SNAP-25 defines the primed vesicle state in regulated exocytosis. J. Cell Biol. 188:401-413. doi:10.1083/jcb.200907018
55. 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 (Pubitemid 28155315)
56. Weber, T., F. Parlati, J.A. McNew, R.J. Johnston, B. Westermann, T.H. Söllner, and J.E. Rothman. 2000. SNAREpins are functionally resistant to disruption by NSF and αSNAP. J. Cell Biol. 149:1063-1072. doi:10.1083/jcb.149.5.1063 (Pubitemid 30354256)
57. 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
58. Wickner, W., and R. Schekman. 2008. Membrane fusion. Nat. Struct. Mol. Biol. 15:658-664. doi:10.1038/nsmb.1451
59. Wu, M.N., J.T. Littleton, M.A. Bhat, A. Prokop, and H.J. Bellen. 1998. ROP, the Drosophila Sec1 homolog, interacts with syntaxin and regulates neurotransmitter release in a dosage-dependent manner. EMBO J. 17:127-139. doi:10.1093/emboj/17.1.127
60. Xu, Y., L. Su, and J. Rizo. 2010. Binding of Munc18-1 to synaptobrevin and to the SNARE four-helix bundle. Biochemistry. 49:1568-1576. doi:10.1021/bi9021878
61. Yoon, T.Y., X. Lu, J. Diao, S.M. Lee, T. Ha, and Y.K. Shin. 2008. Complexin and Ca2+ stimulate SNARE-mediated membrane fusion. Nat. Struct. Mol. Biol. 15:707-713. doi:10.1038/nsmb.1446
62. Zhou, K.M., Y.M. Dong, Q. Ge, D. Zhu, W. Zhou, X.G. Lin, T. Liang, Z.X. Wu, and T. Xu. 2007. PKA activation bypasses the requirement for UNC-31 in the docking of dense core vesicles from C. elegans neurons. Neuron. 56:657-669. doi:10.1016/j.neuron.2007.09.015