Evidence for a functional link between Rab3 and the SNARE complex

Journal of Cell Science

Volumn 109, Issue 12, 1996, Pages 2875-2884

  Johannes, Ludger ^a   Doussau, Frédéric ^b,c   Clabecq, Aude ^a   Henry, Jean Pierre ^a   Darchen, François ^a   Poulain, Bernard ^b,c  

^a INST DE BIOLOGIE PHYSICO CHIMIQUE   (France)

^b CNRS   (France)

^c CENTRE DE NEUROCHIMIE   (France)

Author keywords

Exocytosis; Neurotoxin; Rab; SNAP 25; Synaptobrevin

Indexed keywords

BOTULINUM TOXIN A; GUANINE NUCLEOTIDE BINDING PROTEIN; SYNAPTOBREVIN; SYNTAXIN; TETANUS TOXIN;

ACETYLCHOLINE RELEASE; ANIMAL CELL; APLYSIA; ARTICLE; EXOCYTOSIS; NERVE CELL; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; SYNAPSE VESICLE;

ACETYLCHOLINE; ANIMALS; APLYSIA; CLOSTRIDIUM; GTP PHOSPHOHYDROLASES; GTP-BINDING PROTEINS; GUANOSINE TRIPHOSPHATE; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS; NERVE TISSUE PROTEINS; NEUROTOXINS; PROTEIN ISOPRENYLATION; RAB3 GTP-BINDING PROTEINS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; SNARE PROTEINS; VESICULAR TRANSPORT PROTEINS;

ANIMALIA; APLYSIA;

EID: 0030466294     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (53)

1. Bennett, M. K. and Scheller, R. H. (1993). The molecular machinery for secretion is conserved from yeast to neurons. Proc. Nat. Acad. Sci. USA 90, 2559-2563.
2. Bittner, M. A. and Holz, R. W. (1993). Protein kinase C and clostridial neurotoxins affect discrete and related steps in the secretory pathway. Cell. Mol. Neurobiol. 13, 649-664.
3. Brennwald, P., Kearns, B., Champion, K., Keränen, S., Bankaitis, V. and Novick, P. (1994). Sec9 is a SNAP-25-like component of a yeast SNARE complex that may be the effector of Sec4 function in exocytosis. Cell 79, 245-258.
4. Brondyk, W. H., McKiernan, C. J., Burstein, E. S. and Macara, I. G. (1993). Mutants of Rab3A analogous to oncogenic Ras mutants. J. Biol. Chem. 268, 9410-9415.
5. 2+ and guanine nucleotides. Biochem. J. 282, 387-392.
6. Calakos, N. and Scheller, R. H. (1994). Vesicle-associated membrane protein and synaptophysin are associated on the synaptic vesicle. J. Biol. Chem. 269, 24534-24537.
7. Chavrier, P., Gorvel, J. P., Stelzer, E., Simons, K., Gruenberg, J. and Zerial, M. (1991). Hypervariable C-terminal domain of Rab proteins acts as a targeting signal. Nature 353, 769-772.
8. Cornille, F., Deloye, F., Fournie-Zaluski, M.-C., Roques, B. P. and Poulain, B. (1995). Inhibition of neurotransmitter release by synthetic proline-rich peptides shows that the N-terminal domain of vesicle-associated membrane protein/synaptobrevin is critical for neuro-exocytosis. J. Biol. Chem. 270, 16826-16832.
9. Cremers, F. P. M., Armstrong, S. A., Seabra, M. C., Brown, M. S. and Goldstein, J. L. (1994). REP-2, a Rab escort protein encoded by the choroideremia-like gene. J. Biol. Chem. 269, 2111-2117.
10. Darchen, F., Zahraoui, A., Hammel, F., Monteils, M.-P., Tavitian, A. and Scherman, D. (1990). Association of the GTP-binding protein Rab3A with bovine adrenal chromaffin granules. Proc. Nat. Acad. Sci. USA 87, 5692-5696.
11. Darchen, F., Senyshyn, J., Brondyk, W. H., Taatjes, D. J., Holz, R. W., Henry, J.-P., Denizot, J.-P. and Macara, I. G. (1995). The GTPase Rab3a is associated with large dense core vesicles in bovine chromaffin cells and rat PC12 cells. J. Cell Sci. 108, 1639-1649.
12. Dascher, C., Ossig, R., Gallwitz, D. and Schmitt, H. D. (1991). Identification and structure of 4 yeast genes (SLY) that are able to suppress the functional loss of YPT1, a member of the RAS superfamily. Mol. Cell. Biol. 11, 872-885.
13. Edelmann, L., Hanson, P. I., Chapman, E. R. and Jahn, R. (1995). Synaptobrevin binding to synaptophysin: a potential mechanism for controlling the exocytotic fusion machine. EMBO J. 14, 224-231.
14. Ferro-Novick, S. and Jahn, R. (1994). Vesicle fusion from yeast to man. Nature 370, 191-193.
15. Fischer von Mollard, G., Mignery, G. A., Baumert, M., Perin, M. S., Hanson, T. J., Burger, P. M., Jahn, R. and Südhof, T. C. (1990). Rab3 is a small GTP-binding protein exclusively localized to synaptic vesicles. Proc. Nat. Acad. Sci. USA 87, 1988-1992.
16. Geppert, M., Bolshakov, V, Y., Siegelbaum, S. A., Takei, K., De Camilli, P., Hammer, R. E. and Südhof, T. C. (1994). The role of Rab3A in neurotransmitter release. Nature 369, 493-497.
17. Hanson, P. I., Otto, H., Barton, N. and Jahn, R. (1995). The N-ethylmaleimide-sensitive fusion protein and α-SNAP induce a conformational change in syntaxin. J. Biol. Chem. 270, 16955-16961.
18. Hayashi, T., McMahon, H., Yamasaki, S., Binz, T., Hata, Y., Südhof, T. C. and Niemann, H. (1994). Synaptic vesicle membrane fusion complex: Action of clostridial neurotoxins on assembly. EMBO J. 13, 5051-5061.
19. 2+-dependent exocytosis from adrenal chromaffin cells. J. Biol. Chem. 269, 10229-10234.
20. Johannes, L., Lledo, P.-M., Roa, M., Vincent, J.-D., Henry, J.-P. and Darchen, F. (1994). The GTPase Rab3a negatively controls calcium-dependent exocytosis in neuroendocrine cells. EMBO J. 13, 2029-2037.
21. Lawrence, G. W., Weller, U. and Dolly, J. O. (1994). Botulinum A and the light chain of tetanus toxins inhibit distinct stages of Mg.ATP-dependent catecholamine exocytosis from permeabilized chromaffin cells. Eur. J. Biochem. 222, 325-333.
22. Lian, J. P., Stone, S., Jiang, Y., Lyons, P. and Ferro-Novick, S. (1994). Ypt 1p implicated in v-SNARE activation. Nature 372, 698-701.
23. 2+-dependent exocytosis in rat anterior pituitary cells. Nature 364, 540-544.
24. Lledo, P.-M., Johannes, L., Vernier, P., Zorec, R., Darchen, F., Vincent, J.-D., Henry, J.-P. and Mason, W. T. (1994). Rab3 proteins: Key players in the control of exocytosis. Trends Neurosci. 17, 426-432.
25. Lombardi, D., Soldati, T., Riederer, M. A., Goda, Y., Zerial, M. and Pfeffer, S. R. (1993). Rab9 functions in transport between late endosomes and the trans Golgi network. EMBO J. 12, 677-682.
26. Lupashin, V. V., Hamamoto, S. and Scheckman, R. W. (1996). Biochemical requirements for the targeting and fusion of ER-derived transport vesicles with purified yeast Golgi membranes. J. Cell Biol. 132, 277-289.
27. Martinez, O., Schmidt, A., Salamero, J., Hoflack, B., Roa, M. and Goud, B. (1994). The small GTP-binding protein rab6 functions in intra-Golgi transport. J. Cell Biol. 127, 1575-1588.
28. McMahon, H. T., Foran, P., Dolly, J. O., Verhage, M., Wiegant, V. M. and Nicholls, D. G. (1992). Tetanus toxin and botulinum toxins type A and B inhibit glutamate, γ-aminobutyric acid, aspartate, and met-enkephalin release from synaptosomes. J. Biol. Chem. 267, 21338-21343.
29. McKiernan, C. J., Brondyk, W. H. and Macara, I. G. (1993). The Rab3A GTPase interacts with multiple factors through the same effector domain - mutational analysis of cross-linking of Rab3A to a putative target protein. J. Biol. Chem. 268, 24449-24452.
30. Montecucco, C. and Schiavo, G. (1995). Structure and function of tetanus and botulinum neurotoxins. Quart. Rev. Biophys. 28, 423-472.
31. Musha, T., Kawata, M. and Takai, Y. (1992). The geranylgeranyl moiety but not the methyl moiety of the smg-25A/rab3A protein is essential for the interactions with membrane and its inhibitory GDP/GTP exchange protein. J. Biol. Chem. 267, 9821-9825.
32. Niemann, H., Blasi, J. and Jahn, R. (1994). Clostridial neurotoxins: new tools for dissecting exocytosis. Trends Cell Biol. 4, 179-185.
33. Pellegrini, L. L., O'Connor, V. and Betz, H. (1994). Fusion complex formation protects synaptobrevin against proteolysis by tetanus toxin light chain. FEBS Lett. 353, 319-323.
34. Pellegrini, L. L., O'Connor, V., Lottspeich, F. and Betz, H. (1995). Clostridial neurotoxins compromise the stability of a low energy SNARE complex mediating NSF activation of synaptic vesicle fusion. EMBO J. 14, 4705-4713
35. Pfeffer, S. R. (1994). Rab GTPases: Master regulators of membrane trafficking. Curr. Opin. Cell Biol. 6, 522-526.
36. Poulain, B., Rossetto, O., Deloye, F., Schiavo, G., Tauc, L. and Montecucco, C. (1993). Antibodies against rat brain vesicle-associated membrane protein (synaptobrevin) prevent inhibition of acetylcholine release by tetanus toxin or botulinum neurotoxin type B. J. Neurochem. 61, 1175-1178.
37. Poulain, B., Molgo, J. and Thesleff, S. (1995). Quantal neurotransmitter release and the clostridial neurotoxins' targets. Curr. Top. Microbiol. Immunol. 195, 243-255.
38. Poulain, B., de Paiva, A., Deloye, F., Doussau, F., Tauc, L., Weller, U. and Dolly, J. O. (1996). Differences in the mutiple step process of inhibition of neurotransmitter release induced by tetanus toxin and botulinum neurotoxins type A and B at Aplysia synapses. Neuroscience 70, 567-576.
39. Rossetto, O., Schiavo, G., Montecucco, C., Poulain, B., Deloye, F., Lozzi, L. and Shone, C. (1994). SNARE motif and neurotoxins. Nature 372, 415-416.
40. Rothman, J. E. (1994). Mechanisms of intracellular protein transport. Nature 372, 55-63.
41. Rothman, J. E. and Warren, G. (1994). Implications of the SNARE hypothesis for intracellular membrane topology and dynamics. Curr. Biol. 4, 220-233.
42. Schiavo, G., Benfenati, F., Poulain, B., Rossetto, O., Polverino de Laureto, P., DasGupta, B. R. and Montecucco, C. (1992a). Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359, 832-835.
43. Schiavo, G., Poulain, B., Rossetto, O., Benfenati, F., Tauc, L. and Montecucco, C. (1992b). Tetanus toxin is a zinc protein and its inhibition of neurotransmitter release and protease activity depend on zinc. EMBO J. 11, 3577-3583.
44. Schiavo, G., Rossetto, O., Santucci, A., DasGupta, B. R. and Montecucco, C. (1992c). Botulinum neurotoxins are zinc proteins. J. Biol. Chem. 267, 23479-23483.
45. Simons, K. and Zerial, M. (1993). Rab proteins and the road maps for intracellular transport. Neuron 11, 789-799.
46. Skehel, P. A., Martin, K. C., Kandel, E. R. and Bartsch, D. (1995). A VAMP-binding protein from Aplysia required for neurotransmitter release. Science 269, 1580-1583.
47. Søgaard, M., Tani, K., Ye, R. R., Geromanos, S., Tempst, P., Kirchhausen, T., Rothman, J. E. and Söllner, T. (1994). A rab protein is required for the assembly of SNARE complexes in the docking of transport vesicles. Cell 78, 937-948.
48. Söllner, T., Whitehart, S. W., Brunner, M., Erdjument-Bromage, H., Geromanos, S., Tempst, P. and Rothman, J. E. (1993a). SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318-324.
49. Söllner, T., Bennett, M. K., Whiteheart, S. W., Scheller, R. H. and Rothman, J. E. (1993b). A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75, 409-418.
50. Stenmark, H., Valencia, A., Martinez, O., Ullrich, O., Goud, B. and Zerial, B. (1994). Distinct structural elements of rab5 define its functional specificity. EMBO J. 13, 575-583.
51. Tisdale, E. J., Bourne, J. R., Khosravi-Far, R., Der, C. J. and Balch, W. E. (1992). GTP-binding mutants of Rab1 and Rab2 are potent inhibitors of vesicular transport from the endoplasmic reticulum to the Golgi complex. J. Cell Biol. 119, 749-761.
52. Washbourne, P., Schiavo, G. and Montecucco, C. (1995). Vesicle-associated membrane protein-2 (synaptobrevin 2) forms a complex with synaptophysin. Biochem. J. 305, 721-724.
53. Zahraoui, A., Touchot, N., Chardin, P. and Tavitian A. (1989). The human Rab genes encode a family of GTP-binding proteins related to Yeast YPT1 and SEC4 products involved in secretion. J. Biol. Chem. 264, 12394-12401.