Synaptic vesicle membrane proteins interact to form a multimeric complex

doi:10.1083/jcb.116.3.761

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Synaptic vesicle membrane proteins interact to form a multimeric complex

MK Bennett, N Calakos, T Kreiner and RH Scheller
Department of Molecular and Cellular Physiology, Howard Hughes Medical Institute, Stanford University Medical Center, California 94305.

Potential interactions between membrane components of rat brain synaptic vesicles were analyzed by detergent solubilization followed by size fractionation or immunoprecipitation. The behavior of six synaptic vesicle membrane proteins as well as a plasma membrane protein was monitored by Western blotting. Solubilization of synaptic vesicle membranes in CHAPS resulted in the recovery of a large protein complex that included SV2, p65, p38, vesicle-associated membrane protein, and the vacuolar proton pump. Solubilization in octylglucoside resulted in the preservation of interactions between SV2, p38, and rab3A, while solubilization of synaptic vesicles with Triton X-100 resulted in two predominant interactions, one involving p65 and SV2, and the other involving p38 and vesicle-associated membrane protein. The multicomponent complex preserved with CHAPS solubilization was partially reconstituted following octylglucoside solubilization and subsequent dialysis against CHAPS. Reduction of the CHAPS concentration by gel filtration chromatography resulted in increased recovery of the multicomponent complex. Examination of the large complex isolated from CHAPS-solubilized vesicles by negative stain EM revealed structures with multiple globular domains, some of which were specifically labeled with gold-conjugated antibodies directed against p65 and SV2. The protein interactions defined in this report are likely to underlie aspects of neurotransmitter secretion, membrane traffic, and the spatial organization of vesicles within the nerve terminal.
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Steveson, T. C., Zhao, G. C., Keutmann, H. T., Mains, R. E., Eipper, B. A. (2001). Access of a Membrane Protein to Secretory Granules Is Facilitated by Phosphorylation. J. Biol. Chem. 276: 40326-40337 [Abstract] [Full Text]
Zhao, H., Nonet, M. L. (2001). A Conserved Mechanism of Synaptogyrin Localization. Mol. Biol. Cell 12: 2275-2289 [Abstract] [Full Text]
Braun, J. E. A., Madison, D. V. (2000). A Novel SNAP25-Caveolin Complex Correlates with the Onset of Persistent Synaptic Potentiation. J. Neurosci. 20: 5997-6006 [Abstract] [Full Text]
Buckley, K. M, Melikian, H. E, Provoda, C. J, Waring, M. T (2000). Regulation of neuronal function by protein trafficking: a role for the endosomal pathway. J. Physiol. 525: 11-19 [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]
Son, Y.-J., Scranton, T. W., Sunderland, W. J., Baek, S. J., Miner, J. H., Sanes, J. R., Carlson, S. S. (2000). The Synaptic Vesicle Protein SV2 Is Complexed with an alpha 5-Containing Laminin on the Nerve Terminal Surface. J. Biol. Chem. 275: 451-460 [Abstract] [Full Text]
Caldwell, B. D., Darlington, D. N., Penzes, P., Johnson, R. C., Eipper, B. A., Mains, R. E. (1999). The Novel Kinase Peptidylglycine alpha -Amidating Monooxygenase Cytosolic Interactor Protein 2 Interacts with the Cytosolic Routing Determinants of the Peptide Processing Enzyme Peptidylglycine alpha -Amidating Monooxygenase. J. Biol. Chem. 274: 34646-34656 [Abstract] [Full Text]
Nonet, M. L., Holgado, A. M., Brewer, F., Serpe, C. J., Norbeck, B. A., Holleran, J., Wei, L., Hartwieg, E., Jorgensen, E. M., Alfonso, A. (1999). UNC-11, a Caenorhabditis elegans AP180 Homologue, Regulates the Size and Protein Composition of Synaptic Vesicles. Mol. Biol. Cell 10: 2343-2360 [Abstract] [Full Text]
Costa, M. C. R., Mani, F., Santoro, W. Jr., Espreafico, E. M., Larson, R. E. (1999). Brain Myosin-V, a Calmodulin-carrying Myosin, Binds to Calmodulin-dependent Protein Kinase II and Activates Its Kinase Activity. J. Biol. Chem. 274: 15811-15819 [Abstract] [Full Text]
SPIJKER, S., SMIT, A. B., EIPPER, B. A., MALIK, A., MAINS, R. E., GERAERTS, W. P. M. (1999). A molluscan peptide {alpha}-amidating enzyme precursor that generates five distinct enzymes. FASEB J. 13: 735-748 [Abstract] [Full Text]
Prekeris, R., Terrian, D. M. (1997). Brain Myosin V Is a Synaptic Vesicle-associated Motor Protein: Evidence for a Ca2+-dependent Interaction with the Synaptobrevin-Synaptophysin Complex. JCB 137: 1589-1601 [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]
Tellam, J. T., Macaulay, S. L., McIntosh, S., Hewish, D. R., Ward, C. W., James, D. E. (1997). Characterization of Munc-18c and Syntaxin-4 in 3T3-L1 Adipocytes. PUTATIVE ROLE IN INSULIN-DEPENDENT MOVEMENT OF GLUT-4. J. Biol. Chem. 272: 6179-6186 [Abstract] [Full Text]
Igarashi, M., Tagaya, M., Komiya, Y. (1997). The Soluble N-Ethylmaleimide-Sensitive Factor Attached Protein Receptor Complex in Growth Cones: Molecular Aspects of the Axon Terminal Development. J. Neurosci. 17: 1460-1470 [Abstract] [Full Text]
Schivell, A. E., Batchelor, R. H., Bajjalieh, S. M. (1996). Isoform-specific, Calcium-regulated Interaction of the Synaptic Vesicle Proteins SV2 and Synaptotagmin. J. Biol. Chem. 271: 27770-27775 [Abstract] [Full Text]
Fujita-Yoshigaki, J., Dohke, Y., Hara-Yokoyama, M., Kamata, Y., Kozaki, S., Furuyama, S., Sugiya, H. (1996). Vesicle-associated Membrane Protein 2 Is Essential for cAMP-regulated Exocytosis in Rat Parotid Acinar Cells. THE INHIBITION OF cAMP-DEPENDENT AMYLASE RELEASE BY BOTULINUM NEUROTOXIN B. J. Biol. Chem. 271: 13130-13134 [Abstract] [Full Text]
Galli, T., McPherson, P. S., De Camilli, P. (1996). The V(0) Sector of the V-ATPase, Synaptobrevin, and Synaptophysin Are Associated on Synaptic Vesicles in a Triton X-100-resistant, Freeze-thawing Sensitive, Complex. J. Biol. Chem. 271: 2193-2198 [Abstract] [Full Text]
de Curtis, I, Gatti, G (1994). Identification of a large complex containing the integrin alpha 6 beta 1 laminin receptor in neural retinal cells. J. Cell Sci. 107: 3165-3172 [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]
Stachelek, S. J., Tuft, R. A., Lifschitz, L. M., Leonard, D. M., Farwell, A. P., Leonard, J. L. (2001). Real-time Visualization of Processive Myosin 5a-mediated Vesicle Movement in Living Astrocytes. J. Biol. Chem. 276: 35652-35659 [Abstract] [Full Text]
Bell-Parikh, L. C., Eipper, B. A., Mains, R. E. (2001). Response of an Integral Granule Membrane Protein to Changes in pH. J. Biol. Chem. 276: 29854-29863 [Abstract] [Full Text]
Mody, M., Cao, Y., Cui, Z., Tay, K.-Y., Shyong, A., Shimizu, E., Pham, K., Schultz, P., Welsh, D., Tsien, J. Z. (2001). Genome-wide gene expression profiles of the developing mouse hippocampus. Proc. Natl. Acad. Sci. USA 98: 8862-8867 [Abstract] [Full Text]