Dimerization of the synaptic vesicle protein synaptobrevin (vesicle-associated membrane protein) II depends on specific residues within the transmembrane segment

European Journal of Biochemistry

Volumn 249, Issue 2, 1997, Pages 540-546

  Laage, Rico ^a   Langosch, Dieter ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Neurotransmitter release; Quaternary structure; Synaptobrevin (VAMP) II; Transmembrane segment

Indexed keywords

MEMBRANE PROTEIN; RECOMBINANT PROTEIN; SYNAPTOBREVIN;

AMINO ACID COMPOSITION; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIMERIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; RAT; SYNAPSE VESICLE;

ANIMALIA;

EID: 0030661912     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1997.00540.x     Document Type: Article

References (40)

1. Adams, P. D., Engelman, D. M. & Brünger, A. T. (1996) Improved prediction for the structure of the dimeric transmembrane domain of glycophorin A obtained through global searching, Proteins 26, 257-261.
2. Alvarez, E., Girones, N. & Davis, R. J. (1989) Intermolecular disulfide bonds are not required for the expression of the dimeric state and functional activity of the transferrin receptor, EMBO J. 8, 2231-2240.
3. Arkin, I. T., Adams, P. D., MacKenzie, K. R., Lemmon, M. A., Brünger, A. T. & Engelman, D. M. (1994) Structural organization of the pentameric transmembrane α-helices of phospholamban, a cardiac ion channel, EMBO J. 13, 4757-4764.
4. Bennett, M. K. & Scheller, R. H. (1994) A molecular description of synaptic vesicle membrane trafficking, Annu. Rev. Biochem. 63, 63-100.
5. Broadie, K., Prokop, A., Bellen, H. J., O'Kane, C. J., Schulze, K. L. & Sweeney, S. T. (1995) Syntaxin and synaptobrevin function downstream of vesicle docking in Drosphila, Neuron 15, 663-673.
6. Bruns, D. & Jahn, R. (1995) Real-time measurements of transmitter release from single synaptic vesicles, Nature 377, 62-65.
7. Calakos, N. & Scheller, R. H. (1994) Vesicle-associated membrane protein and synaptophysin are associated on the synaptic vesicle, J. Biol. Chem. 269, 24 534-24 537.
8. Calakos, N., Bennett, M. K., Peterson, K. E. & Scheller, R. H. (1994) Protein-protein interactions contributing to the specificity of intracellular vesicular trafficking, Science 263, 1146-1149.
9. Cosson, P. & Bonifacino, J. S. (1992) Role of transmemhrane domain interactions in the assembly of class II MHC molecules, Science 258, 659-662.
10. Deber, C. M., Khan, A. R., Zuomei, L., Joensson, C., Glibowicka, M. & Wang, J. (1993) Val-Ala mutations selectively alter helix-helix packing in the transmembrane segment of phage M13 coat protein, Proc. Natl Acad. Sci. USA 90, 11 648-11 652.
11. Doms, R. W. & Helenius, A. (1986) Quaternary structure of influenza virus hemagglutinin after acid treatment, J. Virol. 60, 833-839.
12. Edelman, L., Hanson, P. I., Chapman, E. R. & Jahn, R. (1995) Synaptobrevin binding to synaptophysin: a potential mechanism for controlling the exocytotic fusion machine, EMBO J. 14, 224-231.
13. Elferink, L. A., Trimble, W. S. & Scheller, R. H. (1989) Two vesicle-associated membrane protein genes are differentially expressed in the rat central nervous system, J. Biol. Chem. 264, 11 061-11 064.
14. Hayashi, T., McMahon, H., Yamasaki, S., Binz, T., Hata, Y., Südhof, T. C. & Niemann, H. (1994) Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly, EMBO J. 13, 5051-5061.
15. Heynes, T. H. & Fox, R. O. (1991) The crystal structure of Staphylococcus nuclease refined at 1.7 Ångstroms resolution, Proteins 5, 183-201.
16. Hunt, J. M., Bommert, K., Charlton, M. P., Kistner, A., Habermann, E., Augustine, G. J. & Betz, H. (1994) A post-docking role for synaptobrevin in synaptic vesicle fusion, Neuron 12, 1269-1270.
17. Jahn, R. & Südhof, T. C. (1994) Synaptic vesicles and exocytosis, Annu. Rev. Neurosci. 17, 219-246.
18. Kemble, G. W., Henis, Y. I. & White, J. M. (1993) GPI- and transmembrane-anchored influenza hemagglutinin differ in structure and receptor binding activity, J. Cell Biol. 122, 1253-1265.
19. Kemble, G. W., Danieli, T. & White, J. M. (1994) Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion, Cell 76, 383-391.
20. Kunkel, T. A., Roberts, J. D. & Zakour, R. A. (1987) Rapid and efficient site-specific mutagenesis without phenotypic selection, Methods Enzymol. 154, 367-382.
21. Langosch, D. L., Brosig, B., Kolmar, H. & Fritz, H.-J. (1996) Dimerisation of the glycophorin A transmembrane segment in membranes probed with the ToxR transcription activator, J. Mol. Biol. 263, 525-530.
22. Lemmon, M. A., Flanagan, J. M., Treutlein, H. R., Zhang, J. & Engelman, D. M. (1992) Sequence specificity in the dimerization of transmembrane α-helices, Biochemistry 31, 12 719-12 725.
23. Lemmon, M. A. & Engelman, D. M. (1994) Specificity and promiscuity in membrane helix interactions, Quart. Rev. Biophys. 27, 157-218.
24. Lemmon, M. A., Treutlein, H. R., Adams, P. D., Brünger, A. T. & Engelman, D. (1994) A dimerization motif for transmembrane α-helices, Nature Struct. Biol. 1, 157-163.
25. Lindau, M. & Almers, W. (1995) Structure and function of fusion pores in exocytosis and ectoplasmic membrane fusion, Curr. Opin. Neurobiol 7, 509-517.
26. Mandal, K., Chakrabarti, B., Thomson, J. & Siezen, R. J. (1987) Structure and stability of γ-crystallins, J. Biol. Chem. 262, 8096-8102.
27. Manolius, N., Bonifacino, J. S. & Klausner, R. D. (1990) Transmembrane helical interactions and the assembly of the T cell receptor complex, Science 249, 274-277.
28. Matthews, G. (1996) Synaptic exocytosis and endocytosis: capacitance measurements, Curr. Opin. Neurobiol. 6, 358-364.
29. McGinnes, L., Sergel, T. & Morrison, T. (1993) Mutations in the transmembrane domain of the HN protein of Newcastle disease virus affect the structure and activity of the protein, Virology 196, 101-110.
30. McMahon, H. T. & Südhof, T. C. (1995) Synaptic core complex of synaptobrevin, syntaxin, and SNAP25 forms high affinity α-SNAP binding site, J. Biol. Chem. 270, 2213-2217.
31. Munro, S. & Pelham, H. R. B. (1986) An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein, Cell 46, 291-300.
32. Pakula, A. A. & Simon, M. I. (1992) Determination of transmembrane protein structure by disulfide cross-linking: the Escherichia coli Tar receptor, Proc. Natl Acad. Sci. USA 89, 4144-4148.
33. Protopopov, V., Govindan, B., Novick, P. & Gerst, J. B. (1993) Homologs of the synaptobrevin/VAMP family of synaptic vesicle proteins function on the late secretory pathway in S. cerevisiae, Cell 74, 855-861.
34. 2+-induced insulin exocytosis, EMBO J. 15, 6951-6959.
35. Schiavo, G., Benfenati, F., Poulain, B., Rossetto, O., Polverino de Laureto, P., DasGupta, B. R. & Montecucco, C. (1992) Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin, Nature 359, 832-835.
36. Südhof, T. C. (1995) The synaptic vesicle cycle: a cascade of protein-protein interactions, Nature 375, 645-653.
37. Washbourne, P., Schiavo, G. & Montecucco, C. (1995) Vesicle-associated membrane protein-2 (synaptobrevin-2) forms a complex with synaptophysin, Biochem. J. 305, 721-724.
38. Weis, W., Brown, J. H., Cusack, S., Paulson, J. C., Skehel, J. J. & Wiley, D. C. (1988) Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid, Nature 333, 426-431.
39. Wessel, D. & Flügge, U. I. (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detegents and lipids, Anal. Biochem. 138, 141-143.
40. White, J. M. (1992) Membrane fusion, Science 258, 917-924.