Mutational analysis of VAMP domains implicated in Ca2+-induced insulin exocytosis

EMBO Journal

Volumn 15, Issue 24, 1996, Pages 6951-6959

  Regazzi, Romano ^a   Sadoul, Karin ^a   Meda, Paolo ^a   Kelly, Regis B ^b   Halban, Philippe A ^a   Wollheim, Claes B ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Islets of langerhans; Neurotoxins; Pancreas; Secretion; Targeting

Indexed keywords

CALCIUM ION; CELLUBREVIN; INSULIN; MEMBRANE PROTEIN; MUTANT PROTEIN; SYNAPTOBREVIN; SYNTAXIN; TETANUS TOXIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA TRANSFECTION; EXOCYTOSIS; INSULIN RELEASE; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RAT; SECRETORY GRANULE; STRUCTURE ACTIVITY RELATION; SYNAPSE VESICLE;

BOTULINUM TOXINS; CALCIUM; CELL LINE; CYTOPLASMIC GRANULES; EXOCYTOSIS; INSULIN; MEMBRANE PROTEINS; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHOSPHORYLATION; PROTEIN BINDING; R-SNARE PROTEINS;

EID: 0030454433     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb01087.x     Document Type: Article

References (41)

1. Asfari,M., Janjie,D., Meda,P., Li,G., Halban,P.A. and Wollheim,C.B. (1992) Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines. Endocrinology, 130, 167-178.
2. 2+-dependent protease activity is removed. J. Biol. Chem., 270, 31386-31390.
3. Bauerfeind,R., Ohashi,M. and Huttner,W.B. (1994) Biogenesis of secretory granules and synaptic vesicles. Facts and hypothesis. Ann. N.Y. Acad. Sci., 733, 233-244.
4. Binscheck,T., Bartels,F., Bergel,H., Bigalke,H., Yamasaki,S., Hayashi,T., Niemann,H. and Pohlner,J. (1995) IgA protease from Neisseria gonorrhoeae inhibits exocytosis in bovine chromaffin cells like tetanus toxin. J. Biol. Chem., 270, 1770-1774.
5. Bungay,P.J., Potter,J.M. and Griffin,M. (1984) The inhibition of glucose-stimulated insulin secretion by primary amines. A role for transglutaminase in the secretory process. Biochem. J., 219, 819-827.
6. Calakos,N., Bennett,M.K., Peterson,K.E. and Scheller,R.H. (1994) Protein-protein interactions contributing to the specificity of intracellular vesicular trafficking. Science, 263, 1146-1149.
7. Chapman,E.R., An,S., Barton,N. and Jahn,R. (1994) SNAP-25, a t-SNARE which binds to both syntaxin and synaptobrevin via domains that may form coiled coils. J. Biol. Chem., 269, 27427-27432.
8. Chilcote,T.J., Galli,T., Mundigl,O., Edelmann,L., McPherson,P.S., Takei,K. and De Camilli,P (1995) Cellubrevin and synaptobrevins: similar subcellular localization and biochemical properties in PC 12. J. Cell Biol., 129, 219-231.
9. Dascher,C. and Balch,W.E. (1996) Mammalian Sly1 regulates syntaxin 5 function in endoplasmic reticulum to Golgi transport. J. Biol. Chem., 271, 15866-15869.
10. Dascher,C., Ossig,R., Gallwitz,D. and Schmitt,H.D. (1991) Identification and structure of four 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.
11. Elferink,L.A., Trimble,W.S. and Scheller,R.H. (1989) Two vesicle-associated membrane protein genes are differentially expressed in the rat central nervous system. J. Biol. Chem., 264, 11061-11064.
12. Ferro-Novick,S. and Jahn,R. (1994) Vesicle fusion from yeast to man. Nature, 370, 191-193.
13. Galli,T., Chilcote,T., Binz,T., Niemann,H. and De Camilli,P. (1994) Tetanus toxin-mediated cleavage of cellubrevin impairs exocytosis of transferrin receptor-containing vesicles in CHO cells. J. Cell Biol., 125, 1015-1024.
14. Grote,E., Hao,J.C., Bennett,M.K. and Kelly,R.B. (1995) A targeting signal in VAMP regulating transport to synaptic vesicles. Cell. 81, 581-589.
15. Hayashi,T., McMahon,H., Yamasaki,S., Binz,T., Hata,Y., Sudhof,T.C. and Niemann,H. (1994) Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly. EMBO J., 13, 5051-5061.
16. Jacobsson,G., Bean,A.J., Scheller,R.H., Juntti-Berggren,L., Deeney,J.T., Berggren,P.-O. and Meister,B. (1994) Identification of synaptic proteins and their isoform mRNAs in compartments of pancreatic endocrine cells. Proc. Natl Acad. Sci. USA. 91, 12487-12491.
17. Kunkel,T.A., Roberts,J.D. and Zakour,R.A. (1987) Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol., 154, 367-382.
18. Lang,J., Nishimoto,I., Okamoto,T., Regazzi,R., Kiraly,C., Weller,U. and Wollheim,C.B. (1995) Direct control of exocytosis by receptor-mediated activation of the heterotrimeric GTPases Gi and Go or by the expression of their active Ga subunits. EMBO J., 14, 3635-3644.
19. Lupas,A., Van Dyke,M. and Stock,J. (1991) Predicting coiled coils from protein sequences. Science, 252, 1162-1164.
20. McMahon,H.T., Ushkaryov,Y.A., Edelman,L., Link,E., Binz,T., Niemann,H., Jahn,R. and Südhof,T.C. (1993) Cellubrevin is a ubiquitous tetanus-toxin substrate homologous to a putative synaptic vesicle fusion protein. Nature, 364, 346-349.
21. Nagamatsu,S., Fujiwara,T., Nakamichi,Y. Watanabe,T., Katahira,H., Sawa,H. and Akagawa,K. (1996) Expression and functional role of syntaxin 1/HPC-l in pancreatic beta cells: syntaxin 1A, but not 1B, plays a negative role in regulatory insulin release pathway. J. Biol. Chem., 271, 1160-1165.
22. Nielander,H.B., Onofri,F., Valtorta,F., Schiavo,G., Montecucco,C., Greengard,P. and Benfenati,F. (1995) Phosphorylation of VAMP/synaptobrevin in synaptic vesicles by endogenous protein kinases. J. Neurochem., 65, 1712-1720.
23. Niemann,H., Blasi,J. and Jahn,R. (1994) Clostridial neurotoxins: new tools for dissecting exocytosis. Trends Cell Biol., 4, 179-185.
24. Pellizzari,R., Rossetto,O., Lozzi,L., Giovedi,S., Johnson,E., Shone,C.C. and Montecucco,C. (1996) Structural determinants of the specificity for VAMP/synaptobrevin of tetanus and botulinum type B and G neurotoxins. J. Biol. Chem., 271, 20353-20358.
25. Protopopov,V. Govindan,B., Novick,P. and Gerst,J.E. (1993) Homologs of the synaptobrevin/VAMP family of synaptic vesicle proteins function on the late secretory pathway in S.cerevisiae. Cell, 74, 855-861.
26. Reetz,A., Solimena,M., Matteoli,M., Folli,F., Takei,K. and De Camilli,P. (1991) GABA and pancreatic β-cells: colocalization of glutamic acid decarboxylase (GAD) and GABA with synaptic-like microvesicles suggests their role in GABA storage and secretion. EMBO J., 10, 1275-1284.
27. Regazzi,R., Li,G., Deshusses,J. and Wollheim,C.B. (1990) Stimulus-response coupling in insulin-secreting HIT cells. J. Biol. Chem., 265, 15003-15009.
28. 2+- but not for GTPγS-induced insulin secretion. EMBO J., 14, 2723-2730.
29. Regazzi,R., Ravazzola,M., Iezzi,M., Lang,J., Zahraoui,A., Andereggen,E., Morel,P., Takai,Y. and Wollheim,C.B. (1996) Expression, localization and functional role of small GTPases of the Rab3 family in insulin-secreting cells. J. Cell Sci., 109, 2265-2273.
30. Rossetto,O., Schiavo,G., Montecucco,C., Poulain,B., Deloye,F., Lozzi,L. and Shone,C.C. (1994) SNARE motif and neurotoxins. Nature, 372, 415-416.
31. Rossetto,O., Deloye,F., Poulain,B., Pellizzari,R., Schiavo,G. and Montecucco,C. (1995) The metallo-proteinase activity of tetanus and botulism neurotoxins. J. Physiol., 89, 43-50.
32. Rossetto,O., Gorza,L., Schiavo,G., Schiavo,N., Scheller,R.H. and Montecucco,C. (1996) Vamp/synaptobrevin isoforms 1 and 2 are widely and differentially expressed in nonneuronal tissues. J. Cell Biol., 132, 167-179.
33. Rothman,J.E. (1994) Mechanisms of intracellular protein transport. Nature, 372, 55-63.
34. Rothman,J.E. and Warren,G. (1994) Implications of the SNARE hypothesis for intracellular membrane topology and dynamics. Curr. Biol., 4, 220-233.
35. Sadoul,K., Lang,J., Montecucco,C., Weller,U., Regazzi,R., Catsicas,S., Wollheim,C.B. and Halban,P.A. (1995) SNAP-25 is expressed in islets of Langerhans and is involved in insulin release. J. Cell Biol., 128, 1019-1028.
36. Schiavo,G., Benfenati,F., Poulain,B., Rossetto,O., Polverino de Laureto,P., DasGupta,B.R. and Montecucco,C. (1992) Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature, 359, 832-835.
37. Söllner,T., Whiteheart,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.
38. 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.
39. Vozzi,C., Ullrich,S., Charollais,A., Philippe,J., Orci,O. and Meda,P. (1995) Adequate connexin-mediated coupling is required for proper insulin production. J. Cell Biol., 131, 1561-1572.
40. Wheeler,M.B. et al. (1996) Characterization of SNARE protein expression in β cell lines and pancreatic islets. Endocrinology, 137, 1340-1348.
41. 2+ and G-proteins. Diabetes Rev., 4, 276-297.