SNAREpins are functionally resistant to disruption by NSF and αSNAP

Journal of Cell Biology

Volumn 149, Issue 5, 2000, Pages 1063-1072

  Weber, Thomas ^a,b   Parlati, Francesco ^a   McNew, James A ^a   Johnston, Robert J ^a   Westermann, Benedikt ^a,c   Söllner, Thomas H ^a   Rothman, James E ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MUNICH   (Germany)

Author keywords

SNAP; Liposomes; Membrane fusion; NSF; SNARE

Indexed keywords

SNARE PROTEIN;

ARTICLE; CELL FUSION; GENE DISRUPTION; GENE FUNCTION; MEMBRANE STRUCTURE; MEMBRANE VESICLE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; REGULATORY MECHANISM;

ADENOSINE TRIPHOSPHATE; ANIMALS; CARRIER PROTEINS; CELLS, CULTURED; GENE EXPRESSION; INTRACELLULAR MEMBRANES; LIPID BILAYERS; LIPOSOMES; MEMBRANE FUSION; MEMBRANE PROTEINS; MICE; MUTAGENESIS; N-ETHYLMALEIMIDE-SENSITIVE PROTEINS; PROTEIN STRUCTURE, TERTIARY; QA-SNARE PROTEINS; R-SNARE PROTEINS; RATS; SNARE PROTEINS; SOLUBLE N-ETHYLMALEIMIDE-SENSITIVE FACTOR ATTACHMENT PROTEINS; TEMPERATURE; VESICULAR TRANSPORT PROTEINS;

EID: 0034729298     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.149.5.1063     Document Type: Article

References (70)

1. Barlowe, C. 1997. Coupled ER to Golgi transport reconstituted with purified cytosolic proteins. J. Cell Biol. 139:1097-1108.
2. Barr, F.A. 1999. A novel Rab6-interacting domain defines a family of Golgi-targeted coiled-coil proteins. Curr. Biol. 9:381-384.
3. Block, M.R., B.S. Glick, C.A. Wilcox, F.T. Wieland, and J.E. Rothman. 1998. Purification of an N-ethylmaleimide-sensitive protein catalyzing vesicular transport. Proc. Natl. Acad. Sci. USA. 85:7852-7856.
4. Bock, J.B., and R.H. Scheller. 1999. SNARE proteins mediate lipid bilayer fusion. Proc. Natl. Acad. Sci. USA. 96:12227-12229.
5. Brügger, B., W. Nickel, T. Weber, F. Parlati, J.A. McNew, J.E. Rothman, and T. Söllner. 2000. Putative fusogenic activity of NSF is restricted to lipid mixtures whose coalescence is also triggered by other factors. EMBO (Eur. Mol. Biol. Organ.) J. 19:101-107.
6. Chen, Y.A., S.J. Scales, S.M. Patel, Y.C. Doung, and R.H. Scheller. 1999. SNARE complex formation is triggered by Ca2+ and drives membrane fusion. Cell. 97:165-174.
7. Clary, D.O., I.C. Griff, and J.E. Rothman. 1990. SNAPs, a family of NSF attachment proteins involved in intracellular membrane fusion in animals and yeast. Cell. 61:709-721.
8. Coorssen, J.R., P.S. Blank, M. Tahara, and J. Zimmerberg. 1998. Biochemical and functional studies of cortical vesicle fusion: the SNARE complex and Ca2+ sensitivity. J. Cell Biol. 143:1845-1857.
9. Dulubova, I., S. Sugita, S. Hill, M. Hosaka, I. Fernandez, T.C. Sudhof, and J. Rizo. 1999. A conformational switch in syntaxin during exocytosis: role of munc18. EMBO (Eur. Mol. Biol. Organ.) J. 18:4372-4382.
10. Fasshauer, D., W.K. Eliason, A.T. Brunger, and R. Jahn. 1998. Identification of a minimal core of the synaptic SNARE complex sufficient for reversible assembly and disassembly. Biochemistry. 37:10354-10362.
11. Fiebig, K.M., L.M. Rice, F. Pollock, and A.T. Brunger. 1999. Folding intermediates of SNARE complex assembly. Nat. Struct. Biol. 6:117-123.
12. Fleming, K.G., T.M. Hohl, R.C. Yu, S.A. Muller, B. Wolpensinger, A. Engel, H. Engelhardt, A.T. Brunger, T.H. Sollner, and P.I. Hanson. 1998. A revised model for the oligomeric state of the N-ethylmaleimide-sensitive fusion protein, NSF. J. Biol. Chem. 273:15675-15681.
13. Gerst, J.F. 1999. SNAREs and SNARE regulators in membrane fusion and exocytosis. Cell. Mol. Life Sci. 55:707-734.
14. Glenn, D.E., and R.D. Burgoyne. 1996. Botulinum neurotoxin light chains inhibit both Ca(2+)-induced and GTP analogue-induced catecholamine release from permeabilized adrenal chromaffin cells. FEBS Lett. 386:137-140.
15. Gonzalez, L., Jr., and R.H. Scheller. 1999. Regulation of membrane trafficking: structural insights from a Rab/effector complex. Cell. 96:755-758.
16. Griff, I.C., R. Schekman, J.E. Rothman, and C.A. Kaiser. 1992. The yeast SEC17 gene product is functionally equivalent to mammalian alpha-SNAP protein. J. Biol. Chem. 267:12106-12115.
17. Grindstaff, K.K., C. Yeaman, N. Anandasabapathy, S.C. Hsu, E. Rodriguez- Boulan, R.H. Scheller, and W.J. Nelson. 1998. Sec6/8 complex is recruited to cell-cell contacts and specifies transport vesicle delivery to the basal-lateral membrane in epithelial cells. Cell. 93:731-740.
18. Halachmi, N., and Z. Lev. 1996. The Sec1 family: a novel family of proteins involved in synaptic transmission and general secretion. J. Neurochem. 66: 889-897.
19. Hanson, P.I., H. Otto, N. Barton, and R. Jahn. 1995. The N-ethylmaleimide-sensitive fusion protein and alpha-SNAP induce a conformational change in syntaxin. J. Biol. Chem. 270:16955-16961.
20. Hanson, P.I., R. Roth, H. Morisaki, R. Jahn, and J.E. Heuser. 1997. Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch electron microscopy. Cell. 90:523-535.
21. Hayashi, T., H. McMahon, S. Yamasaki, T. Binz, Y. Hata, T.C. Sudhof, and H. Niemann. 1994. Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly. EMBO (Eur. Mol. Biol. Organ.) J. 13: 5051-5061.
22. Hayashi, T., S. Yamasaki, S. Nauenburg, T. Binz, and H. Niemann. 1995. Disassembly of the reconstituted synaptic vesicle membrane fusion complex in vitro. EMBO (Eur. Mol. Biol. Organ.) J. 14:2317-2325.
23. Hohl, T.M., F. Parlati, C. Wimmer, J.E. Rothman, T.H. Söllner, and H. Engelhardt. 1998. Arrangement of subunits in 20 S particles consisting of NSF, SNAPs, and SNARE complexes. Mol. Cell. 2:539-548.
24. Hong, W. 1998. Protein transport from the endoplasmic reticulum to the Golgi apparatus. J. Cell Sci. 111:2831-2839.
25. Hua, S.Y., and M.P. Charlton. 1999. Activity-dependent changes in partial VAMP complexes during neurotransmitter release. Nat. Neurosci. 2:1078-1083.
26. Kaiser, C.A., and R. Schekman. 1990. Distinct sets of SEC genes govern transport vesicle formation and fusion early in the secretory pathway. Cell. 61: 723-733.
27. Katz, L., P.I. Hanson, J.E. Heuser, and P. Brennwald. 1998. Genetic and morphological analyses reveal a critical interaction between the C-termini of two SNARE proteins and a parallel four helical arrangement for the exocytic SNARE complex. EMBO (Eur. Mol. Biol. Organ.) J. 17:6200-6209.
28. Kee, Y., R.C. Lin, S.C. Hsu, and R.H. Scheller. 1995. Distinct domains of syntaxin are required for synaptic vesicle fusion complex formation and dissociation. Neuron. 14:991-998.
29. Kjer-Nielsen, L., R.D. Teasdale, C. van Vliet, and P.A. Gleeson. 1999. A novel Golgi-localization domain shared by a class of coiled-coil peripheral membrane proteins. Curr. Biol. 9:385-388.
30. Kooy, J., B.H. Toh, J.M. Pettitt, R. Erlich, and P.A. Gleeson. 1992. Human autoantibodies as reagents to conserved Golgi components. Characterization of a peripheral. 230-kDa compartment-specific Golgi protein. J. Biol. Chem. 267:20255-20263.
31. Lin, R.C., and R.H. Scheller. 1997. Structural organization of the synaptic exocytosis core complex. Neuron. 19:1087-1094.
32. Lindau, M., and W. Almers. 1995. Structure and function of fusion pores in exocytosis and ectoplasmic membrane fusion. Curr. Opin. Cell Biol. 7:509-517.
33. Littleton, J.T., E.R. Chapman, R. Kreber, M.B. Garment, S.D. Carlson, and B. Ganetzky. 1998. Temperature-sensitive paralytic mutations demonstrate that synaptic exocytosis requires SNARE complex assembly and disassembly. Neuron. 21:401-413.
34. Malhotra, V., L. Orci, B.S. Glick, M.R. Block, and J.E. Rothman. 1988. Role of an N-ethylmaleimide-sensitive transport component in promoting fusion of transport vesicles with cisternae of the Golgi stack. Cell. 54:221-227.
35. Mayer, A., W. Wickner, and A. Haas. 1996. Sec18p (NSF)-driven release of Sec17p (alpha-SNAP) can precede docking and fusion of yeast vacuoles. Cell. 85:83-94.
36. Munro, S., and B.J. Nichols. 1999. The GRIP domain - a novel Golgi-targeting domain found in several coiled-coil proteins. Curr. Biol. 9:377-380.
37. Nakamura, N., C. Rabouille, R. Watson, T. Nilsson, N. Hui, P. Slusarewicz, T.E. Kreis, and G. Warren. 1995. Characterization of a cis-Golgi matrix protein, GM130. J. Cell Biol. 131:1715-1726.
38. Nakamura, N., M. Lowe, T.P. Levine, C. Rabouille, and G. Warren. 1997. The vesicle docking protein p115 binds GM130, a cis-Golgi matrix protein, in a mitotically regulated manner. Cell. 89:445-455.
39. Nichols, B.J., and H.R. Pelham. 1998. SNAREs and membrane fusion in the Golgi apparatus. Biochim. Biophys. Acta. 1404:9-31.
40. Nicholson, K.L., M. Munson, R.B. Miller, T.J. Filip, R. Fairman, and F.M. Hughson. 1998. Regulation of SNARE complex assembly by an N-terminal domain of the t-SNARE Sso1p. Nat. Struct. Biol. 5:793-802.
41. Nickel, W., T. Weber, J.A. McNew, F. Parlati, T.H. Söllner, and J.E. Rothman. 1999. Content mixing and membrane integrity during membrane fusion driven by pairing of isolated v-SNAREs and t-SNAREs. Proc. Natl. Acad. Sci. USA. 96:12571-12576.
42. Novick, P., and M. Zerial. 1997. The diversity of Rab proteins in vesicle transport. Curr. Opin. Cell Biol. 9:496-504.
43. Orci, L., A. Perrelet, and J.E. Rothman. 1998. Vesicles on strings: morphological evidence for processive transport within the Golgi stack. Proc. Natl. Acad. Sci. USA. 95:2279-2283.
44. Otter-Nilsson, M., R. Hendriks, E.I. Pecheur-Huet, D. Hoekstra, and T. Nilsson. 1999. Cytosolic ATPases, p97 and NSF, are sufficient to mediate rapid membrane fusion. EMBO (Eur. Mol. Biol. Organ.) J. 18:2074-2083.
45. 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.
46. Pelham, H.R. 1999. SNAREs and the secretory pathway-lessons from yeast. Exp. Cell Res. 247:1-8.
47. Pevsner, J., S.C. Hsu, J.K. Braun, N. Calakos, A.E. Ting, M.K. Bennett, and R.H. Scheller. 1994. Specificity and regulation of a synaptic vesicle docking complex. Neuron. 13:353-361.
48. Poirier, M.A., J.C. Hao, P.N. Malkus, C. Chan, M.F. Moore, D.S. King, and M.K. Bennett. 1998a. Protease resistance of syntaxin.SNAP-25.VAMP complexes. Implications for assembly and structure. J. Biol. Chem. 273:11370-11377.
49. Poirier, M.A., W. Xiao, J.C. Macosko, C. Chan, Y.K. Shin, and M.K. Bennett. 1998b. The synaptic SNARE complex is a parallel four-stranded helical bundle. Nat. Struct. Biol. 5:765-769.
50. Sacher, M., Y. Jiang, J. Barrowman, A. Scarpa, J. Burston, L. Zhang, D. Schieltz, J.R. Yates III, H. Abeliovich, and S. Ferro-Novick. 1998. TRAPP, a highly conserved novel complex on the cis-Golgi that mediates vesicle docking and fusion. EMbO (Eur. Mol. Biol. Organ.) J. 17:2494-2503.
51. Schaffner, W., and C. Weissman. 1973. A rapid, sensitive, and specific method for the determination of protein in dilute solution. Anal. Biochem. 56:502-514.
52. Skehel, J.J., and D.C. Wiley. 1998. Coiled coils in both intracellular vesicle and viral membrane fusion. Cell. 95:871-874.
53. Söllner, T., M.K. Bennett, S.W. Whiteheart, R.H. Scheller, and J.E. Rothman. 1993a. 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. Söllner, T., S.W. Whiteheart, M. Brunner, H. Erdjument-Bromage, S. Geromanos, P. Tempst, and J.E. Rothman. 1993b. SNAP receptors implicated in vesicle targeting and fusion. Nature. 362:318-324.
55. Struck, D.K., D. Hoekstra, and R.E. Pagano. 1981. Use of resonance energy transfer to monitor membrane fusion. Biochemistry. 20:4093-4099.
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. Tahara, M., J.R. Coorssen, K. Timmers, P.S. Blank, T. Whalley, R. Scheller, and J. Zimmerberg. 1998. Calcium can disrupt the SNARE protein complex on sea urchin egg secretory vesicles without irreversibly blocking fusion. J. Biol. Chem. 273:33667-33673.
58. TerBush, D.R., and P. Novick. 1995. Sec6, Sec8, and Sec15 are components of a multisubunit complex which localizes to small bud tips in Saccharomyces cerevisiae. J. Cell Biol. 130:299-312.
59. TerBush, D.R., T. Maurice, D. Roth, and P. Novick. 1996. The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO (Eur. Mol. Biol. Organ.) J. 15:6483-6494.
60. Ungermann, C., and W. Wickner. 1998. Vam7p, a vacuolar SNAP-25 homolog, is required for SNARE complex integrity and vacuole docking and fusion. EMBO (Eur. Mol. Biol. Organ.) J. 17:3269-3276.
61. Ungermann, C., K. Sato, and W. Wickner. 1998. Defining the functions of trans-SNARE pairs. Nature. 396:543-548.
62. Wang, Y., M. Okamoto, F. Schmitz, K. Hofmann, and T.C. Sudhof. 1997. Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature. 388: 593-598.
63. Waters, M.G., and S.R. Pfeffer. 1999. Membrane tethering in intracellular transport. Curr. Opin. Cell Biol. 11:453-459.
64. Waters, M.G., D.O. Clary, and J.E. Rothman. 1992. A novel 115-kD peripheral membrane protein is required for intercisternal transport in the Golgi stack. J. Cell Biol. 118:1015-1026.
65. 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.
66. Whiteheart, S.W., and E.W. Kubalek. 1995. SNAPs and NSF: general members of the fusion apparatus. Trends Cell Biol. 5:64-68.
67. Whiteheart, S.W., I.C. Griff, M. Brunner, D.O. Clary, T. Mayer, S.A. Buhrow, and J.E. Rothman. 1993. SNAP family of NSF attachment proteins includes a brain-specific isoform. Nature. 362:353-355.
68. Whiteheart, S.W., K. Rossnagel, S.A. Buhrow, M. Brunner, R. Jaenicke, and J.E. Rothman. 1994. N-ethylmaleimide-sensitive fusion protein: a trimeric ATPase whose hydrolysis of ATP is required for membrane fusion. J. Cell Biol. 126:945-954.
69. Wilson, D.W., C.A. Wilcox, G.C. Flynn, E. Chen, W.J. Kuang, W.J. Henzel, M.R. Block, A. Ullrich, and J.E. Rothman. 1989. A fusion protein required for vesicle-mediated transport in both mammalian cells and yeast. Nature. 339:355-359.
70. Xu, T., B. Rammner, M. Margiltai, A.R. Artalejo, E. Neher, and R. Jahn. 1999. Inhibition of SNARE complex assembly differentially affects kinetic components of exocytosis. Cell. 99:713-722.