A multisubunit particle implicated in membrane fusion

doi:10.1083/jcb.117.3.531

This Article

Full Text (PDF, 852K)

Alert me when this article is cited

Citation Map

Services

Email this article

Similar articles in this journal

Similar articles in PubMed

Alert me to new content in the JCB

Download to citation manager

Citing Articles

Citing Articles via HighWire

Citing Articles via CrossRef

Citing Articles via Google Scholar

Google Scholar

Articles by Wilson, D. W.

Articles by Rothman, J. E.

Search for Related Content

PubMed

PubMed Citation

Articles by Wilson, D. W.

Articles by Rothman, J. E.

Pubmed/NCBI databases

Gene	GEO Profiles
HomoloGene	Protein
UniGene
Compound via MeSH
Substance via MeSH

Social Bookmarking

What's this?

ARTICLES

A multisubunit particle implicated in membrane fusion

DW Wilson, SW Whiteheart, M Wiedmann, M Brunner and JE Rothman
Program in Cellular Biochemistry and Biophysics, Rockefeller Research Laboratory, Sloan-Kettering Institute, New York 10021.

The N-ethylmaleimide sensitive fusion protein (NSF) is required for fusion of lipid bilayers at many locations within eukaryotic cells. Binding of NSF to Golgi membranes is known to require an integral membrane receptor and one or more members of a family of related soluble NSF attachment proteins (alpha-, beta-, and gamma-SNAPs). Here we demonstrate the direct interaction of NSF, SNAPs and an integral membrane component in a detergent solubilized system. We show that NSF only binds to SNAPs in the presence of the integral receptor, resulting in the formation of a multisubunit protein complex with a sedimentation coefficient of 20S. Particle assembly reveals striking differences between members of the SNAP protein family; gamma-SNAP associates with the complex via a binding site distinct from that used by alpha- and beta-SNAPs, which are themselves equivalent, alternative subunits of the particle. Once formed, the 20S particle is subsequently able to disassemble in a process coupled to the hydrolysis of ATP. We suggest how cycles of complex assembly and disassembly could help confer specificity to the generalized NSF-dependent fusion apparatus.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Barszczewski, M., Chua, J. J., Stein, A., Winter, U., Heintzmann, R., Zilly, F. E., Fasshauer, D., Lang, T., Jahn, R. (2008). A Novel Site of Action for {alpha}-SNAP in the SNARE Conformational Cycle Controlling Membrane Fusion. Mol. Biol. Cell 19: 776-784 [Abstract] [Full Text]
Siddiqi, S. A., Siddiqi, S., Mahan, J., Peggs, K., Gorelick, F. S., Mansbach, C. M. II (2006). The Identification of a Novel Endoplasmic Reticulum to Golgi SNARE Complex Used by the Prechylomicron Transport Vesicle. J. Biol. Chem. 281: 20974-20982 [Abstract] [Full Text]
Brandon, E., Szul, T., Alvarez, C., Grabski, R., Benjamin, R., Kawai, R., Sztul, E. (2006). On and Off Membrane Dynamics of the Endoplasmic Reticulum-Golgi Tethering Factor p115 In Vivo. Mol. Biol. Cell 17: 2996-3008 [Abstract] [Full Text]
Sztul, E., Lupashin, V. (2006). Role of tethering factors in secretory membrane traffic. Am. J. Physiol. Cell Physiol. 290: C11-C26 [Abstract] [Full Text]
Andreeva, A. V., Kutuzov, M. A., Vaiskunaite, R., Profirovic, J., Meigs, T. E., Predescu, S., Malik, A. B., Voyno-Yasenetskaya, T. (2005). G{alpha}12 Interaction with {alpha}SNAP Induces VE-cadherin Localization at Endothelial Junctions and Regulates Barrier Function. J. Biol. Chem. 280: 30376-30383 [Abstract] [Full Text]
Morrell, C. N., Matsushita, K., Lowenstein, C. J. (2005). A Novel Inhibitor of N-Ethylmaleimide-Sensitive Factor Decreases Leukocyte Trafficking and Peritonitis. J. Pharmacol. Exp. Ther. 314: 155-161 [Abstract] [Full Text]
Predescu, D., Vogel, S. M., Malik, A. B. (2004). Functional and morphological studies of protein transcytosis in continuous endothelia. Am. J. Physiol. Lung Cell. Mol. Physiol. 287: L895-L901 [Abstract] [Full Text]
Whalley, T., Timmers, K., Coorssen, J., Bezrukov, L., Kingsley, D. H., Zimmerberg, J. (2004). Membrane fusion of secretory vesicles of the sea urchin egg in the absence of NSF. J. Cell Sci. 117: 2345-2356 [Abstract] [Full Text]
Weimer, R. M., Jorgensen, E. M. (2003). Controversies in synaptic vesicle exocytosis. J. Cell Sci. 116: 3661-3666 [Full Text]
Abonyo, B. O., Wang, P., Narasaraju, T. A., Rowan, W. H. III, McMillan, D. H., Zimmerman, U.-J., Liu, L. (2003). Characterization of {alpha}-Soluble N-Ethylmaleimide-Sensitive Fusion Attachment Protein in Alveolar Type II Cells: Implications in Lung Surfactant Secretion. Am. J. Respir. Cell Mol. Bio. 29: 273-282 [Abstract] [Full Text]
Tani, K., Shibata, M., Kawase, K., Kawashima, H., Hatsuzawa, K., Nagahama, M., Tagaya, M. (2003). Mapping of Functional Domains of gamma -SNAP. J. Biol. Chem. 278: 13531-13538 [Abstract] [Full Text]
Rancour, D. M., Dickey, C. E., Park, S., Bednarek, S. Y. (2002). Characterization of AtCDC48. Evidence for Multiple Membrane Fusion Mechanisms at the Plane of Cell Division in Plants. Plant Physiol. 130: 1241-1253 [Abstract] [Full Text]
Muller, J. M.M., Shorter, J., Newman, R., Deinhardt, K., Sagiv, Y., Elazar, Z., Warren, G., Shima, D. T. (2002). Sequential SNARE disassembly and GATE-16-GOS-28 complex assembly mediated by distinct NSF activities drives Golgi membrane fusion. JCB 157: 1161-1173 [Abstract] [Full Text]
Pullikuth, A. K., Gill, S. S. (2002). In vivo membrane trafficking role for an insect N-ethylmaleimide-sensitive factor which is developmentally regulated in endocrine cells. J. Exp. Biol. 205: 911-926 [Abstract] [Full Text]
Errico, A., Ballabio, A., Rugarli, E. I. (2002). Spastin, the protein mutated in autosomal dominant hereditary spastic paraplegia, is involved in microtubule dynamics. Hum Mol Genet 11: 153-163 [Abstract] [Full Text]
Predescu, S. A., Predescu, D. N., Palade, G. E. (2001). Endothelial Transcytotic Machinery Involves Supramolecular Protein-Lipid Complexes. Mol. Biol. Cell 12: 1019-1033 [Abstract] [Full Text]
Boehmelt, G., Fialka, I., Brothers, G., McGinley, M. D., Patterson, S. D., Mo, R., Hui, C. C., Chung, S., Huber, L. A., Mak, T. W., Iscove, N. N. (2000). Cloning and Characterization of the Murine Glucosamine-6-phosphate Acetyltransferase EMeg32. DIFFERENTIAL EXPRESSION AND INTRACELLULAR MEMBRANE ASSOCIATION. J. Biol. Chem. 275: 12821-12832 [Abstract] [Full Text]
Cao, X., Barlowe, C. (2000). Asymmetric Requirements for a Rab Gtpase and Snare Proteins in Fusion of Copii Vesicles with Acceptor Membranes. JCB 149: 55-66 [Abstract] [Full Text]
Bishop, N., Woodman, P. (2000). ATPase-defective Mammalian VPS4 Localizes to Aberrant Endosomes and Impairs Cholesterol Trafficking. Mol. Biol. Cell 11: 227-239 [Abstract] [Full Text]
Babor, S. M., Fass, D. (1999). Crystal structure of the Sec18p N-terminal domain. Proc. Natl. Acad. Sci. USA 96: 14759-14764 [Abstract] [Full Text]
Bernstein, A. M., Whiteheart, S. W. (1999). Identification of a Cellubrevin/Vesicle Associated Membrane Protein 3�Homologue in Human Platelets. Blood 93: 571-579 [Abstract] [Full Text]
YEAMAN, C., GRINDSTAFF, K. K., NELSON, W. J. (1999). New Perspectives on Mechanisms Involved in Generating Epithelial Cell Polarity. Physiol. Rev. 79: 73-98 [Abstract] [Full Text]
Wong, S. H., Xu, Y., Zhang, T., Griffiths, G., Lowe, S. L., Subramaniam, V. N., Seow, K. T., Hong, W. (1999). GS32, a Novel Golgi SNARE of 32�kDa, Interacts Preferentially with Syntaxin 6. Mol. Biol. Cell 10: 119-134 [Abstract] [Full Text]
Hackam, D. J., Rotstein, O. D., Sjolin, C., Schreiber, A. D., Trimble, W. S., Grinstein, S. (1998). v-SNARE-dependent secretion is required for phagocytosis. Proc. Natl. Acad. Sci. USA 95: 11691-11696 [Abstract] [Full Text]
Lichtenstein, Y., Desnos, C., Faundez, V., Kelly, R. B., Clift-O'Grady, L. (1998). Vesiculation and sorting from PC12-derived endosomes in vitro. Proc. Natl. Acad. Sci. USA 95: 11223-11228 [Abstract] [Full Text]
Swanton, E., Sheehan, J., Bishop, N., High, S., 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 [Abstract] [Full Text]
Shuang, R., Zhang, L., Fletcher, A., Groblewski, G. E., Pevsner, J., Stuenkel, E. L. (1998). Regulation of Munc-18/Syntaxin 1A Interaction by Cyclin-dependent Kinase 5�in Nerve Endings. J. Biol. Chem. 273: 4957-4966 [Abstract] [Full Text]
Mullock, B. M., Bright, N. A., Fearon, C. W., Gray, S. R., Luzio, J. (1998). Fusion of Lysosomes with Late Endosomes Produces a Hybrid Organelle of Intermediate Density and Is NSF Dependent. JCB 140: 591-601 [Abstract] [Full Text]
Rowe, T., Dascher, C., Bannykh, S., Plutner, H., Balch, W. E. (1998). Role of Vesicle-Associated Syntaxin 5 in the Assembly of Pre-Golgi Intermediates. Science 279: 696-700 [Abstract] [Full Text]
Colombo, M. I., Gelberman, S. C., Whiteheart, S. W., Stahl, P. D. (1998). N-Ethylmaleimide-Sensitive Factor-dependent alpha -SNAP Release, an Early Event in the Docking/Fusion Process, Is Not Regulated by Rab GTPases. J. Biol. Chem. 273: 1334-1338 [Abstract] [Full Text]
Itin, C., Rancano, C., Nakajima, Y., Pfeffer, S. R. (1997). A Novel Assay Reveals a Role for Soluble N-Ethylmaleimide-sensitive Fusion Attachment Protein in Mannose 6-Phosphate Receptor Transport from Endosomes to the Trans Golgi Network. J. Biol. Chem. 272: 27737-27744 [Abstract] [Full Text]
Lemons, P. P., Chen, D., Bernstein, A. M., Bennett, M. K., Whiteheart, S.W. (1997). Regulated Secretion in Platelets: Identification of Elements of the Platelet Exocytosis Machinery. Blood 90: 1490-1500 [Abstract] [Full Text]
Xu, Y., Wong, S. H., Zhang, T., Subramaniam, V. N., Hong, W. (1997). GS15, a 15-Kilodalton Golgi Soluble N-Ethylmaleimide-sensitive Factor Attachment Protein Receptor (SNARE) Homologous to rbet1. J. Biol. Chem. 272: 20162-20166 [Abstract] [Full Text]
Paek, I., Orci, L., Ravazzola, M., Erdjument-Bromage, H., Amherdt, M., Tempst, P., Sollner, T. H., Rothman, J. E. (1997). ERS-24, a Mammalian v-SNARE Implicated in Vesicle Traffic between the ER and the Golgi. JCB 137: 1017-1028 [Abstract] [Full Text]
Mastick, C. C., Falick, A. L. (1997). Association of N-Ethylmaleimide Sensitive Fusion (NSF) Protein and Soluble NSF Attachment Proteins-{alpha} and -{gamma} with Glucose Transporter-4-Containing Vesicles in Primary Rat Adipocytes. Endocrinology 138: 2391-2397 [Abstract] [Full Text]
Mukhopadhyay, A., Barbieri, A. M., Funato, K., Roberts, R., Stahl, P. D. (1997). Sequential Actions of Rab5 and Rab7 Regulate Endocytosis in the Xenopus Oocyte. JCB 136: 1227-1237 [Abstract] [Full Text]
Orlandi, P. A., Orlandi, P. A. (1997). Protein-disulfide Isomerase-mediated Reduction of the A Subunit of Cholera Toxin in a Human Intestinal Cell Line. J. Biol. Chem. 272: 4591-4599 [Abstract] [Full Text]
Mayer, A., Wickner, W. (1997). Docking of Yeast Vacuoles Is Catalyzed by the Ras-like GTPase Ypt7p after Symmetric Priming by Sec18p (NSF). JCB 136: 307-317 [Abstract] [Full Text]
Robinson, L., Aniento, F, Gruenberg, J (1997). NSF is required for transport from early to late endosomes. J. Cell Sci. 110: 2079-2087 [Abstract]
Colombo, M. I., Taddese, M., Whiteheart, S. W., Stahl, P. D. (1996). A Possible Predocking Attachment Site for N-Ethylmaleimide-sensitive Fusion Protein. INSIGHTS FROM IN VITRO ENDOSOME FUSION. J. Biol. Chem. 271: 18810-18816 [Abstract] [Full Text]
Mayer, T., Touchot, N., Elazar, Z. (1996). Transport between cis and medial Golgi Cisternae Requires the Function of the Ras-related Protein Rab6. J. Biol. Chem. 271: 16097-16103 [Abstract] [Full Text]
Tagaya, M., Furuno, A., Mizushima, S. (1996). SNAP Prevents Mg[IMAGE]-ATP-induced Release of N-Ethylmaleimide-sensitive Factor from the Golgi Apparatus in Digitonin-permeabilized PC12 Cells. J. Biol. Chem. 271: 466-470 [Abstract] [Full Text]
Nagiec, E. E., Bernstein, A., Whiteheart, S. W. (1995). Each Domain of the N-Ethylmaleimide-sensitive Fusion Protein Contributes to Its Transport Activity. J. Biol. Chem. 270: 29182-29188 [Abstract] [Full Text]
Roy, S. N., Kudryk, B., Redman, C. M. (1995). Secretion of Biologically Active Recombinant Fibrinogen by Yeast. J. Biol. Chem. 270: 23761-23767 [Abstract] [Full Text]
Hanson, P. I., Otto, H., Barton, N., Jahn, R. (1995). The N-Ethylmaleimide-sensitive Fusion Protein and [IMAGE]-SNAP Induce a Conformational Change in Syntaxin. J. Biol. Chem. 270: 16955-16961 [Abstract] [Full Text]
Parsons, T.D., Coorssen, J.R., Hortmann, H., Lee, A.K., Tse, F.W., Almers, W. (1995). The Last Seconds in the Life of a Secretory Vesicle. Cold Spring Harb Symp Quant Biol 60: 389-396 [Abstract]
Levine, T.P., Misteli, T., Rabouille, C., Warren, G. (1995). Mitotic Disassembly and Reassembly of the Golgi Apparatus. Cold Spring Harb Symp Quant Biol 60: 549-557 [Abstract]
Jantti, J, Keranen, S, Toikkanen, J, Kuismanen, E, Ehnholm, C, Soderlund, H, Olkkonen, V. (1994). Membrane insertion and intracellular transport of yeast syntaxin Sso2p in mammalian cells. J. Cell Sci. 107: 3623-3633 [Abstract]
Lawrence, B., Brown, W. (1993). Inhibition of protein synthesis separates autophagic sequestration from the delivery of lysosomal enzymes. J. Cell Sci. 105: 473-480 [Abstract]
White, J. (1992). Membrane fusion. Science 258: 917-924 [Abstract]
Plattner, H., Knoll, G., Erxleben, C. (1992). The mechanics of biological membrane fusion. Merger of aspects from electron microscopy and patch-clamp analysis. J. Cell Sci. 103: 613-618
Bennett, M., Calakos, N, Scheller, R. (1992). Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257: 255-259 [Abstract]
Matveeva, E. A., Whiteheart, S. W., Vanaman, T. C., Slevin, J. T. (2001). Phosphorylation of the N-Ethylmaleimide-sensitive Factor Is Associated with Depolarization-dependent Neurotransmitter Release from Synaptosomes. J. Biol. Chem. 276: 12174-12181 [Abstract] [Full Text]
Chen, D., Xu, W., He, P., Medrano, E. E., Whiteheart, S. W. (2001). Gaf-1, a gamma -SNAP-binding Protein Associated with the Mitochondria. J. Biol. Chem. 276: 13127-13135 [Abstract] [Full Text]
Wimmer, C., Hohl, T. M., Hughes, C. A., Muller, S. A., Sollner, T. H., Engel, A., Rothman, J. E. (2001). Molecular Mass, Stoichiometry, and Assembly of 20 S Particles. J. Biol. Chem. 276: 29091-29097 [Abstract] [Full Text]
Lamb, J. R., Fu, V., Wirtz, E., Bangs, J. D. (2001). Functional Analysis of the Trypanosomal AAA Protein TbVCP with trans-Dominant ATP Hydrolysis Mutants. J. Biol. Chem. 276: 21512-21520 [Abstract] [Full Text]
May, A. P., Whiteheart, S. W., Weis, W. I. (2001). Unraveling the Mechanism of the Vesicle Transport ATPase NSF, the N-Ethylmaleimide-sensitive Factor. J. Biol. Chem. 276: 21991-21994 [Full Text]