Cytosolic ATPases, p97 and NSF, are sufficient to mediate rapid membrane fusion

EMBO Journal

Volumn 18, Issue 8, 1999, Pages 2074-2083

  Otter Nilsson, Marlies ^a,b   Hendriks, Rob ^c   Pecheur Huet, Eve Isabelle ^b   Hoekstra, Dick ^b   Nilsson, Tommy ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c ZMBH   (Germany)

Author keywords

ATPases; Membrane fusion; NSF; p97

Indexed keywords

ADENOSINE TRIPHOSPHATASE; HYBRID PROTEIN; LIPOSOME; N ETHYLMALEIMIDE; REGULATOR PROTEIN;

ANIMAL CELL; ARTICLE; CYTOSOL; ENZYME ACTIVITY; MEMBRANE BINDING; MEMBRANE FUSION; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; RAT;

EID: 0033560750     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.8.2074     Document Type: Article

References (47)

1. Acharya, U., Jacobs, K., Peter, J.M., Watson, N., Farquhar, M.G. and Malhotra, V. (1995) The formation of Golgi stacks from vesiculated Golgi membranes requires two distinct fusion events. Cell, 82, 895-904.
2. Ames, B.N. (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol., 8, 115-118.
3. Barnard, R.J.O., Morgan, A. and Burgoyne, R.D. (1997) Stimulation of NSF ATPase activity by α-SNAP is required for SNARE complex disassembly and exocytosis. J. Cell Biol., 139, 875-883.
4. Bartlett, G.R. (1959) Phosphorus assay in column chromatography. J. Biol. Chem., 234, 466-468.
5. Chernomordik, L.V. and Zimmerberg, J. (1995) Bending membranes to the task: structural intermediates in bilayer fusion. Curr. Opin. Struct. Biol., 5, 541-547.
6. Chernomordik, L.V., Leikina, E., Frolov, V., Bronk, P. and Zimmerberg, J. (1997) An early stage of membrane fusion mediated by the low pH conformation of influenza hemagglutinin depends upon membrane lipids. J. Cell Biol., 136, 81-93.
7. Düzgünes, N., Allen, T.M., Fedor, J. and Papahadjopoulos, D. (1987) Lipid mixing during membrane aggregation and fusion: why fusion assays disagree. Biochemistry, 26, 8435-8442.
8. Düzgünes, N. and Wilschut, J. (1993) Fusion assays monitoring intermixing of aqueous contents. Methods Enzymol., 220, 3-14.
9. Ellens, H., Bentz, J. and Szoka, F.C. (1984) pH-induced destabilization of phosphatidylethanolamine-containing liposomes: role of bilayer contact. Biochemistry, 23, 1532-1538.
10. Epand, R.M., Epand, R.F., Richardson, C.D. and Yeagle, P.L. (1993) Structural requirements for inhibition of membrane fusion by carbobenzoxy-D-Phe-Phe-Gly. Biochim. Biophys. Acta, 1152, 128-134.
11. Epand, R.M., Shai, Y., Segrest, J.P. and Anantharamaiah, G.M. (1995) Mechanisms for modulation of membrane bilayer properties by amphipathic helical peptides. Biopolymers, 37, 319-338.
12. Hanson, P.I., Roth, R., Morisaki, H., Jahn, R. and Heuser, J.E. (1997) Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch electron microscopy. Cell. 90, 523-535.
13. Hoekstra, D. and Düzgünes, N. (1993) Lipid mixing assays to determine fusion in liposome systems. Methods Enzymol., 220, 15-32.
14. Hoekstra, D., Buist-Arkema, R., Klappe, K. and Reutelingsperger, C.P.M. (1993) Interaction of annexins with membranes: The N-terminus as a governing parameter as revealed with a chimeric annexin. Biochemistry, 32, 14194-14202.
15. Kessel, M., Maurixi, M.R., Kim, B., Kocsis, E. Trus, B.L., Singh, S.K. and Steven, A.C. (1995) Homology in structural organization between E.coli ClpAP protease and the eukaryotic 26S proteasome. J. Mol. Biol., 250, 587-594.
16. Kondo, H., Rabouille, C., Newman, R., Levine, T.P., Pappin, D., Freemont, P. and Warren, G. (1997) p47 is a cofactor for p97-mediated membrane fusion. Nature, 388, 75-78.
17. Kleinsmith, L.J. and Kish, V.M. (1995) In McLaughlin, S., Trost, K. and MacElree (eds), Principles of Cell Biology. Harper-Collins College Publishers, New York, NY, pp. 155-193.
18. Latterich, M., Frohlich, K.U. and Schekman, R. (1995) Membrane fusion and the cell cycle: Cdc48p participates in the fusion of ER membranes. Cell, 82, 885-893.
19. Malhotra, V., Serafini, T., Orci, L., Shepherd, J.C. and Rothman, J.E. (1989) Purification of a novel class of coated vesicles mediating biosynthetic protein transport through the Golgi stack. Cell, 58, 329-336.
20. Matveeva, E.A., He, P. and Whiteheart, S.W. (1997) N-Ethylmaleimide-sensitive fusion protein contains high and low affinity ATP-binding sites that are functionally distinct. J. Biol. Chem., 272, 26413-26418.
21. Mayer, A., Wickner, W. and Haas, A. (1996) Sec18p (NSF)-driven release of Sec17p (α-SNAP) can precede docking and fusion of yeast vacuoles. Cell, 85, 83-94.
22. Membranes and membrane transport. In Kleinsmith, L.J. and Kish, V.M (eds), Principles of Cell and Molecular Biology. 2nd edn. Harper Collins College Publishers, pp. 155-193.
23. Meyer, H.H., Kondo, H. and Warren, G. (1998) The p47 co-factor regulates the ATPase activity of the membrane fusion protein, p97. FEBS Lett., 437, 255-257.
24. Nichols, B.J., Ungermann, C., Pelham, H.R., Wickner, W.T. and Haas, A. (1997) Homotypic fusion mediated by t-and v-SNAREs. Nature, 387, 199-202.
25. Otto, H., Hanson, P.I. and Jahn, R. (1997) Assembly and disassembly of a ternary complex of synaptobrevin, syntaxin and SNAP-25 in the membrane of synaptic vesicles. Proc. Natl Acad. Sci. USA, 94, 6197-6201.
26. Patel, S.K., Indig, F.E., Olivieri, N., Levine, N.D. and Latterich, M. (1998) Organelle membrane fusion: a novel function for the syntaxin homolog Ufe1p in ER membrane fusion. Cell, 92, 611-620.
27. Pecheur, E.I., Martin, I., Ruysschaert, J.M., Bienvenue, A. and Hoekstra, D. (1998) Membrane induced by 11-mer anionic and cationic peptides. A structure-function study. Biochemistry, 37, 2361-2371.
28. Peters, J.-M., Wals, M.J. and Franke, W.W. (1990) An abundant and ubiquitous homo-oligomeric ring-shaped ATPase particle related to the putative vesicle fusion proteins Sec18p and NSF. EMBO J., 9, 1757-1767.
29. 2+-ATPase complex. A structural study. J. Mol. Biol., 223, 557-571.
30. Rabouille, C., Levine, T.P, Peters, J.-M. and Warren, G. (1995) An NSF-like ATPase, p97 and NSF mediate cisternal regrowth from mitotic Golgi fragments. Cell, 82, 905-914.
31. Rabouille, C., Kondo, H., Newman, R., Hui, N., Freemont, P. and Warren, G. (1998) Syntaxin 5 is a common component of the NSF-and p97-mediated reassembly pathways of Golgi cistemae from mitotic Golgi fragments in vitro. Cell, 93, 603-610.
32. Rothman, J.E. (1994) Mechanisms of intracellular protein transport. Nature, 372, 55-63.
33. Sato, K. and Wickner, W. (1998) Functional reconstitution of Ypt7p GTPase and a purified vacuole SNARE complex. Science, 281, 700-702.
34. Slusarewicz, P., Nilsson, T., Hui, N., Watson, R. and Warren, G. (1994) Isolation of a matrix that binds medial Golgi enzymes. J. Cell Biol., 124, 405-413.
35. Söllner, T., Whiteheart, S.W., Brunner, M., Erdjument-Bromage, H., Geromans, S., Tempst, P. and Rothman, J.E. (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature, 362, 318-324.
36. Steel, G.J. and Morgan, A. (1998) Selective stimulation of the D1 ATPase domain of N-ethylmaleimide-sensitive fusion protein (NSF) by soluble NSF attachment proteins. FEBS Lett., 423, 113-116.
37. Struck, D.K., Hoekstra, D. and Pagano, R.E. (1981) Use of resonance energy transfer to monitor membrane fusion. Biochemistry, 20, 4093-4099.
38. 2+-regulated exocytosis. FEBS Lett., 393, 185-188.
39. Swanton, E., Sheehan, J., Bishop, N., High, S. and Woodman, P. (1998) Formation and turnover of NSF-and SNAP-containing 'fusion' complexes occur on undocked, clathrin-coated vesicle-derived membranes. Mol. Biol Cell, 9, 1633-1647.
40. Traub, L.M., Ostrom, J.A. and Kornfeld, S. (1993) Biochemical dissection of AP-1 recruitment onto Golgi membranes. J. Cell Biol., 123, 561-573.
41. Ungermann, C., Nichols, B.J., Pelham, H.R. and Wickner, W. (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.
42. Ungermann, C., Sato, K. and Wickner, W. (1998b) Defining the functions of trans-SNARE pairs. Nature, 396, 543-548.
43. Vidal, M. and Hoekstra, D. (1995) In vitro fusion of reticulocyte endocytic vesicles with liposomes. J. Biol. Chem., 270, 17823-17829.
44. Weber, T., Zemelman, B.V., McNew, J.A., Westermann, B., Gmachi, M., Parlati, F., Söllner, T. and Rothman, J.E. (1998) SNAREpins: minimal machinery for membrane fusion. Cell, 92, 759-772.
45. Whiteheart, S.W., Griff, I.C, Brunner, M., Clary, D.O., Mayer, T., Buhrow, S.A. and Rothman, J.E. (1993) SNAP family of NSF attachment proteins includes a brain-specific isoform. Nature, 362, 353-355.
46. Whiteheart, S.W., Rossnagel, K., Buhrow, S.A., Brunner, M., Jaenicke, R. and Rothman, J.E. (1994) N-ethylmaleimide-sensitive fusion protein: a trimeric ATPase whose hydrolysis of ATP is required for membrane fusion. J. Cell Biol., 126, 945-954.
47. Zhang, L., Ashendel, C.L., Becker, G.W. and Morre, D.J. (1994) Isolation and characterization of the principal ATPase associated with transitional endoplasmic reticulum of rat liver. J. Cell Biol., 127, 1871-1883.