Capture and release of partially zipped trans-SNARE complexes on intact organelles

Journal of Cell Biology

Volumn 185, Issue 3, 2009, Pages 535-549

  Schwartz, Matthew L ^a   Merz, Alexey J ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CHAPERONE; MEMBRANE LIPID; SEC17 PROTEIN; SEC18 PROTEIN; SNARE PROTEIN; UNCLASSIFIED DRUG; CALCIUM; LIPID; PROTEOLIPID; PROTEOLIPOSOMES;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ORGANELLE; COMPLEX FORMATION; CONTROLLED STUDY; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; BIOLOGICAL MODEL; CELL FUSION; CELL MEMBRANE; CELL VACUOLE; DRUG EFFECT; EXOCYTOSIS; KINETICS; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE;

CALCIUM; CELL FUSION; CELL MEMBRANE; EXOCYTOSIS; KINETICS; LIPIDS; MEMBRANE FUSION; MODELS, BIOLOGICAL; ORGANELLES; PROTEOLIPIDS; SACCHAROMYCES CEREVISIAE; SNARE PROTEINS; VACUOLES;

EID: 65649153795     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200811082     Document Type: Article

References (71)

1. 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.
2. Armstrong, R.T., A.S. Kushnir, and J.M. White. 2000. The transmembrane domain of influenza hemagglutinin exhibits a stringent length requirement to support the hemifusion to fusion transition. J. Cell Biol. 151:425-437.
3. Barnard, R.J., A. Morgan, and R.D. Burgoyne. 1996. Domains of alpha-SNAP required for the stimulation of exocytosis and for N-ethylmalemide- sensitive fusion protein (NSF) binding and activation. Mol. Biol. Cell. 7:693-701.
4. Binz, T., J. Blasi, S. Yamasaki, A. Baumeister, E. Link, T.C. Sudhof, R. Jahn, and H. Niemann. 1994. Proteolysis of SNAP-25 by types E and A botulinal neurotoxins. J. Biol. Chem. 269:1617-1620.
5. Boeddinghaus, C., A.J. Merz, R. Laage, and C. Ungermann. 2002. A cycle of Vam7p release from and Ptdlns 3-P-dependent rebinding to the yeast vacuole is required for homotypic vacuole fusion. J. Cell Biol. 157:79-89.
6. Brett, C.L., and A.J. Merz. 2008. Osmotic regulation of Rab-mediated organelle docking. Curr. Biol. 18:1072-1077.
7. Brett, C.L., R.L. Plemel, B.T. Lobinger, M. Vignali, S. Fields, and A.J. Merz. 2008. Efficient termination of vacuolar Rab GTPase signaling requires coordinated action by a GAP and a protein kinase. J. Cell Biol. 182:1141-1151.
8. Chapman, E.R. 2008. How does synaptotagmin trigger neurotransmitter release? Annu. Rev. Biochem. 77:615-641.
9. Cheever, M.L., T.K. Sato, T. de Beer, T.G. Kutateladze, S.D. Emr, and M. Overduin. 2001. Phox domain interaction with PtdIns(3)P targets the Vam7 t-SNARE to vacuole membranes. Nat. Cell Biol. 3:613-618.
10. Chernomordik, L.V., and M.M. Kozlov. 2008. Mechanics of membrane fusion. Nat. Struct. Mol. Biol. 15:675-683.
11. Collins, K.M., and W.T. Wickner. 2007. Trans-SNARE complex assembly and yeast vacuole membrane fusion. Proc. Natl. Acad. Sci. USA. 104:8755-8760.
12. Collins, K.M., N.L. Thorngren, R.A. Fratti, and W.T. Wickner. 2005. Sec17p and HOPS, in distinct SNARE complexes, mediate SNARE complex disruption or assembly for fusion. EMBO J. 24:1775-1786.
13. Dodge, F.A.J., and R. Rahamimoff. 1967. Co-operative action a calcium ions in transmitter release at the neuromuscular junction. J. Physiol. 193:419-432.
14. Fratti, R.A., Y. Jun, A.J. Merz, N. Margolis, and W. Wickner. 2004. Interdependent assembly of specific regulatory lipids and membrane fusion proteins into the vertex ring domain of docked vacuoles. J. Cell Biol. 167:1087-1098.
15. Giraudo, C.G., C. Hu, D. You, A.M. Slovic, E.V. Mosharov, D. Sulzer, T.J. Melia, and J.E. Rothman. 2005. SNAREs can promote complete fusion and hemifusion as alternative outcomes. J. Cell Biol. 170:249-260.
16. Haas, A. 1995. A quantitative assay to measure homotypic vacuole fusion in vitro. Methods Cell Sci. 17:283-294.
17. Haas, A., and W. Wickner. 1996. Homotypic vacuole fusion requires Sec17p (yeast a-SNAP) and Sec18p (yeast NSF). EMBO J. 15:3296-3305.
18. Han, X., C.T. Wang, J. Bai, E.R. Chapman, and M.B. Jackson. 2004. Transmembrane segments of syntaxin line the fusion pore of Ca2+-triggered exocytosis. Science. 304:289-292.
19. Hanson, P.I., J.E. Heuser, and R. Jahn. 1997a. Neurotransmitter release - four years of SNARE complexes. Curr. Opin. Neurobiol. 7:310-315.
20. 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.
21. Hohl, T.M., F. Parlati, C. Wimmer, J.E. Rothman, T.H. Sollner, and H. Engelhardt. 1998. Arrangement of subunits in 20 S particles consisting of NSF, SNAPs, and SNARE complexes. Mol. Cell. 2:539-548.
22. Hua, S.Y., and M.P. Charlton. 1999. Activity-dependent changes in partial VAMP complexes during neurotransmitter release. Nat. Neurosci. 2:1078-1083.
23. Hua, Y., and R.H. Scheller. 2001. Three SNARE complexes cooperate to mediate membrane fusion. Proc. Natl. Acad. Sci. USA. 98:8065-8070.
24. Jackson, M.B., and E.R. Chapman. 2008. The fusion pores of Ca(2+)-triggered exocytosis. Nat. Struct. Mol. Biol. 15:684-689.
25. Jahn, R., and R.H. Scheller. 2006. SNAREs-engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7:631-643.
26. Jun, Y., and W. Wickner. 2007. Assays of vacuole fusion resolve the stages of docking, lipid mixing, and content mixing. Proc. Natl. Acad. Sci. USA. 104:13010-13015.
27. Kemble, G.W., T. Danieli, and J.M. White. 1994. Lipid-anchored influenza hem- agglutinin promotes hemifusion, not complete fusion. Cell. 76:383-391.
28. Kesavan, J., M. Borisovska, and D. Bruns. 2007. v-SNARE actions during Ca(2+)-triggered exocytosis. Cell. 131:351-363.
29. Lagow, R.D., H. Bao, E.N. Cohen, R.W. Daniels, A. Zuzek, W.H. Williams, G.T. Macleod, R.B. Sutton, and B. Zhang. 2007. Modification of a hydro- phobic layer by a point mutation in syntaxin 1A regulates the rate of synaptic vesicle fusion. PLoS Biol. 5:e72.
30. Lando, L., and R.S. Zucker. 1994. Ca2+ cooperativity in neurosecretion measured using photolabile Ca2+ chelators. J. Neurophysiol. 72:825-830.
31. Langosch, D., J.M. Crane, B. Brosig, A. Hellwig, L.K. Tamm, and J. Reed. 2001. Peptide mimics of SNARE transmembrane segments drive membrane fusion depending on their conformational plasticity. J. Mol. Biol. 311:709-721.
32. 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 bi- layers. Nat. Struct. Mol. Biol. 14:890-896.
33. Lu, X., Y. Zhang, and Y.K. Shin. 2008. Supramolecular SNARE assembly precedes hemifusion in SNARE-mediated membrane fusion. Nat. Struct. Mol. Biol. 15:700-706.
34. Marz, K.E., J.M. Lauer, and P.I. Hanson. 2003. Defining the SNARE complex binding surface of alpha-SNAP: implications for SNARE complex disassembly. J. Biol. Chem. 278:27000-27008.
35. Matos, M.F., K. Mukherjee, X. Chen, J. Rizo, and T.C. Sudhof. 2003. Evidence for SNARE zippering during Ca2+-triggered exocytosis in PC12 cells. Neuropharmacology. 45:777-786.
36. Mayer, A., W. Wickner, and A. Haas. 1996. Sec18p (NSF)-driven release of Sec17p (a-SNAP) can precede docking and fusion of yeast vacuoles. Cell. 85:83-94.
37. McNew, J.A., T. Weber, D.M. Engelman, T.H. Sollner, 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.
38. McNew, J.A., T. Weber, F. Parlati, R.J. Johnston, T.J. Melia, T.H. Sollner, and J.E. Rothman. 2000. Close is not enough: SNARE-dependent membrane fusion requires an active mechanism that transduces force to membrane anchors. J. Cell Biol. 150:105-117.
39. Melia, T.J., D. You, D.C. Tareste, and J.E. Rothman. 2006. Lipidic antagonists to SNARE-mediated fusion. J. Biol. Chem. 281:29597-29605.
40. Melikyan, G.B., J.M. White, and F.S. Cohen. 1995. GPI-anchored influenza hemagglutinin induces hemifusion to both red blood cell and planar bilayer membranes. J. Cell Biol. 131:679-691.
41. Merz, A.J., and W.T. Wickner. 2004a. Resolution of organelle docking and fusion kinetics in a cell-free assay. Proc. Natl. Acad. Sci. USA. 101:11548-11553.
42. 2+ efflux from the yeast vacuole lumen. J. Cell Biol. 164:195-206.
43. Montecucco, C., G. Schiavo, and S. Pantano. 2005. SNARE complexes and neuro- exocytosis: how many, how close? Trends Biochem. Sci. 30:367-372.
44. Pobbati, A.V., A. Stein, and D. Fasshauer. 2006. N- to C-terminal SNARE complex assembly promotes rapid membrane fusion. Science. 313:673-676.
45. Reese, C., and A. Mayer. 2005. Transition from hemifusion to pore opening is rate limiting for vacuole membrane fusion. J. Cell Biol. 171:981-990.
46. Rice, L.M., and A.T. Brunger. 1999. Crystal structure of the vesicular transport protein Sec17: implications for SNAP function in SNARE complex disassembly. Mol. Cell. 4:85-95.
47. Rizo, J., and C. Rosenmund. 2008. Synaptic vesicle fusion. Nat. Struct. Mol. Biol. 15:665-674.
48. Rossi, G., A. Salminen, L.M. Rice, A.T. Brunger, and P. Brennwald. 1997. Analysis of a yeast SNARE complex reveals remarkable similarity to the neuronal SNARE complex and a novel function for the C terminus of the SNAP-25 homolog, Sec9. J. Biol. Chem. 272:16610-16617.
49. Roy, R., K. Peplowska, J. Rohde, C. Ungermann, and D. Langosch. 2006. Role of the Vam3p transmembrane segment in homodimerization and SNARE complex formation. Biochemistry. 45:7654-7660.
50. Sakaba, T., A. Stein, R. Jahn, and E. Neher. 2005. Distinct kinetic changes in neuro- transmitter release after SNARE protein cleavage. Science. 309:491-494.
51. 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.
52. Seals, D.F., G. Eitzen, N. Margolis, W.T. Wickner, and A. Price. 2000. A Ypt/Rab effector complex containing the Sec1 homolog Vps33p is required for homotypic vacuole fusion. Proc. Natl. Acad. Sci. USA. 97:9402-9407.
53. Sollner, 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.
54. Sorensen, J.B., K. Wiederhold, E.M. Muller, I. Milosevic, G. Nagy, B.L. de Groot, H. Grubmuller, and D. Fasshauer. 2006. Sequential N- to C-terminal SNARE complex assembly drives priming and fusion of secretory vesicles. EMBO J. 25:955-966.
55. Starai, V.J., Y. Jun, and W. Wickner. 2007. Excess vacuolar SNAREs drive lysis and Rab bypass fusion. Proc. Natl. Acad. Sci. USA. 104:13551-13558.
56. 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.
57. Thorngren, N., K.M. Collins, R.A. Fratti, W. Wickner, and A.J. Merz. 2004. A soluble SNARE drives rapid docking, bypassing ATP and Sec17/18p for vacuole fusion. EMBO J. 23:2765-2776.
58. Ungermann, C., B.J. Nichols, H.R. Pelham, and W. Wickner. 1998a. 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. 140:61-69.
59. Ungermann, C., K. Sato, and W. Wickner. 1998b. Defining the functions of trans- SNARE pairs. Nature. 396:543-548.
60. Wang, Y., I. Dulubova, J. Rizo, and T.C. Sudhof. 2001. Functional analysis of conserved structural elements in yeast syntaxin Vam3p. J. Biol. Chem. 276:28598-28605.
61. Weber, T., B.V. Zemelman, J.A. McNew, B. Westermann, M. Gmachl, F. Parlati, T.H. Sollner, and J.E. Rothman. 1998. SNAREpins: minimal machinery for membrane fusion. Cell. 92:759-772.
62. Weber, T., F. Parlati, J.A. McNew, R.J. Johnston, B. Westermann, T.H. Sollner, and J.E. Rothman. 2000. SNAREpins are functionally resistant to disruption by NSF and aSNAP. J. Cell Biol. 149:1063-1072.
63. Weiss, J.N. 1997. The Hill equation revisited: uses and misuses. FASEB J. 11:835-841.
64. Wimmer, C., T.M. Hohl, C.A. Hughes, S.A. Muller, T.H. Sollner, A. Engel, and J.E. Rothman. 2001. Molecular mass, stoichiometry, and assembly of 20 S particles. J. Biol. Chem. 276:29091-29097.
65. Wong, J.L., D.E. Koppel, A.E. Cowan, and G.M. Wessel. 2007. Membrane hemi- fusion is a stable intermediate of exocytosis. Dev. Cell. 12:653-659.
66. Wurmser, A.E., T.K. Sato, and S.D. Emr. 2000. New component of the vacuolar class C-Vps complex couples nucleotide exchange on the Ypt7 GTPase to SNARE-dependent docking and fusion. J. Cell Biol. 151:551-562.
67. Xiao, W., M.A. Poirier, M.K. Bennett, and Y.K. Shin. 2001. The neuronal t-SNARE complex is a parallel four-helix bundle. Nat. Struct. Biol. 8:308-311.
68. Xu, T., T. Binz, H. Niemann, and E. Neher. 1998. Multiple kinetic components of exocytosis distinguished by neurotoxin sensitivity. Nat. Neurosci. 1:192-200.
69. Xu, T., B. Rammner, M. Margittai, A.R. Artalejo, E. Neher, and R. Jahn. 1999. Inhibition of SNARE complex assembly differentially affects kinetic components of exocytosis. Cell. 99:713-722.
70. Xu, Y., F. Zhang, Z. Su, J.A. McNew, and Y.K. Shin. 2005. Hemifusion in SNARE-mediated membrane fusion. Nat. Struct. Mol. Biol. 12:417-422.
71. Zampighi, G.A., L.M. Zampighi, N. Fain, S. Lanzavecchia, S.A. Simon, and E.M. Wright. 2006. Conical electron tomography of a chemical synapse: vesicles docked to the active zone are hemi-fused. Biophys. J. 91:2910-2918.