Vamp/synaptobrevin isoforms 1 and 2 are widely and differentially expressed in nonneuronal tissues

Journal of Cell Biology

Volumn 132, Issue 1-2, 1996, Pages 167-179

  Rossetto, Ornella ^a   Gorza, Luisa ^a,b   Schiavo, Giampietro ^a   Schiavo, Nicola ^a   Scheller, Richard H ^c   Montecucco, Cesare ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b CNR Ctro Stud Biol Fisiopatol M

^c STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SYNAPTOBREVIN;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL FUSION; CELLULAR DISTRIBUTION; EXOCYTOSIS; GENE EXPRESSION; GENE LOCATION; LANGERHANS CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; TISSUE SPECIFICITY;

ANIMALIA;

EID: 0030023904     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.132.1.167     Document Type: Article

References (78)

1. Almers, W. 1994. How fast can you get. Nature (Lond.). 367:682-683
2. Archer, B. T , T Ozcelik, R. Jahn, U. Francke, and T.C. Südhof. 1990. Structures and chromosomal localizations of two human genes encoding synaptobrevins 1 and 2. J. Biol Chem 265:17267-17273
3. Baumert, M., P. R. Maycox, F. Navone, P De Camilli, and R Jahn. 1989. Synaptobrevin: an integral membrane protein of 18,000 daltons present in small synaptic vesicles of rat brain. EMBO (Eur. Mol Biol Organ.) J. 8:379-384.
4. Bennett, M K., and R. H. Scheller. 1993 The molecular machinery for secretion is conserved from yeast to neurons Proc Natl Acad Sci USA. 90:2559-2563.
5. Bennett, M K , and R. H Scheller. 1994. A molecular description of synaptic vesicle membrane trafficking. Annu Rev. Biochem. 63:63-100
6. Bennett, M. K., N. Calakos, and R. H. Scheller. 1992. Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones Science (Wash. DC). 257:255-259.
7. Bennett, M K., J. E. Garcia-Arras, L. A. Elferink, K Peterson, A. M. Fleming, C. D. Hazuka, and R. H. Scheller. 1993. The syntaxin family of vesicular transport receptors. Cell 74:863-873.
8. Braun, J. E. A., B. A. Fritz, S. M E. Wong, and A. W. Lowe. 1994 Identification of a vesicle-associated membrane protein (VAMP-like) membrane protein in zymogen granules of the rat exocrine pancreas J. Biol Chem. 269: 5328-5335.
9. Burgoyne, R. D., and A. Morgan. 1993. Regulated exocytosis. Biochem J. 293: 305-316.
10. Calakos, N., and R. H. Scheller. 1994. Vesicle-associated membrane protein and synaptophysin are associated on the synaptic vesicle. J. Biol. Chem. 269: 24534-24537.
11. Chapman, E. R., S. An, N. Barton, and R. Jahn. 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.
12. Chin, A. C., R. W. Burgess, B. O. Wong, T. L. Schwarz, and R. H. Scheller. 1993. Differential expression of transcripts from syb, a Drosophila melanogaster gene encoding VAMP (synaptobrevin) that is abundant in non-neuronal cells. Gene (Amst ). 131:175-181.
13. Chomczynski, P., and N. Sacchi. 1987. Single step methods of RNA isolation by acid guanidinium thyocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
14. Clary, D. O., I. C. Griff, and J. E. Rothman. 1990. SNAPs family of NSF attachment proteins involved in intracellular membrane fusion in animal and yeast. Cell. 61:709-721.
15. Corley-Cain, C., W. S. Trimble, and G. E. Lienhard 1992. Members of the VAMP family of synaptic vesicle proteins are components of glucose transporter-containing vesicles from rat adipocytes. J. Biol. Chem 267:11681-11684.
16. De Camilli, P. 1995. Keeping synapses up to speed. Nature (Lond.) 375:450-451
17. Di Antonio, A., R. W. Burgess, A. C. Chin, D. L. Deitcher, R. H. Scheller, and T. L. Schwarz. 1993. Identification and characterization of Drosophila genes for synaptic vesicle proteins. J. Neurosci 13:4924-4935.
18. Edelmann L., P. I. Hanson, E. R Chapman, and R. Jahn. 1995. Synaptobrevin binding to synaptophysin. A potential mechanism for controlling the exocytotic fusion machine. EMBO (Eur. Mol. Biol. Organ.) J. 14:224-231.
19. Elferink, L. A., W. S. Trimble, and R. H. Scheller 1989. Two vesicle-associated membrane protein genes are differently expressed in the rat central nervous system. J. Biol. Chem. 264:11061-11064.
20. Ferro-Novick, S., and R. Jahn. 1994. Vesicle fusion from yeast to man Nature (Lond ). 370:191-193.
21. Gaisano, H. Y., L. Sheu, J. K. Foskett, and W. S Trimble. 1994. Tetanus toxin light chain cleaves a vesicle-associated membrane protein (VAMP) isoform 2 in rat pancreatic zymogen granules and inhibits enzyme secretion. J. Biol. Chem. 269:17062-17066.
22. Gorza, L., S. Ausoni, N. Merciai, K. E. Hastings, and S. Schiaffino. 1993. Regional differences in troponin I isoform switching during rat heart development. Dev. Biol. 156:253-264
23. Greengard, P , F. Valtorta, A. J. Czernik, and F. Benfenati. 1993. Synaptic vesicle phosphoproteins and regulation of synaptic function. Science (Wash. DC) 259:780-785.
24. Hayashi, T., H. McMahon, S Yamasaki, T. Binz, Y. Hata, T. C. Südhof, and H. Niemann. 1994. Synaptic vesicle membrane-fusion complex. Action of clostridial neurotoxins on assembly. EMBO (Eur Mol. Biol. Organ.) J. 13: 5051-5061.
25. Heuser, J. E., and T. S Reese 1973 Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57:315-344
26. Hirokawa, N , K. Sobue, K. Kanda, A. Harada, and H. Yorifuji. 1989. The cytoskeletal architecture of the presynaptic terminal and the molecular structure of synapsin I. J. Cell Biol. 108:111-126.
27. Höhne-Zell, B., B. Stecher, and M. Gratzl. 1993. Functional characterization of the catalytic site of the tetanus toxin light chain using permeabilized adrenal chromaffin cells. FEBS Lett 336:175-180.
28. Horikawa, H. P. M., H. Saisu, T. Ishizuka, Y. Sekine, A. Tsugita, S. Odani, and T. Abe 1993. A complex of rab3A, SNAP-25, VAMP/synaptobrevin-2 and syntaxin in brain presynaptic terminals FEBS Lett 330:236-240
29. Hunt, J. M., K. Bommert, M. P. Charlton, A. Kistner, E. Habermann, G J Augustine, and H. Betz 1994. A post-docking role for synaptobrevin in synaptic vesicle fusion. Neuron 12:1269-1279.
30. Hüttner, W. B., W. Schiebler, P. Greengard, and P. De Camilli. 1983. Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J. Cell Biol. 96:1374-1388
31. Kelly, R., S. Alonso, S Tajbakhsh, G Cossu, and M. Buckingham. 1995. Myosin light chain 3F regulatory sequences confer regionalized cardiac and skeletal muscle expression in transgenic mice. J Cell Biol 129:383-396
32. Kelly, R B. 1993a. Storage and release of neurotransmitters. Cell. 72:43-53.
33. Kelly, R B 1993b. Much do about docking. Curr. Biol 3:474-476.
34. Kutay, U., E. Hartmann, and T. A. Rapoport. 1993. A class membrane proteins with a C-terminal anchor. Trends Cell Biol. 3:72-75.
35. Kutay, U., G. Ahnert-Hilger, E. Hartmann, B. Wiedenmann, and T. A Rapoport. 1995. Transport route for synaptobrevin via a novel pathway of insertion into the endoplasmic-reticulum membrane. EMBO (Eur. Mol. Biol. Organ.) J. 14:217-223.
36. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of head of bacteriophage T4. Nature (Lond.). 227:680-685.
37. Malhorta, V , L. Orci, B. S. Glick, M R. Block, and J. E. Rothman. 1988 Role of an N-ethyl maleimide-sensitive protein (NSF) catalyzing transport component in promoting fusion of transport vesicles with cisternae of the Golgi stack. Cell. 54:221-227.
38. Markwell, M. A. K., S. M. Haas, N. E. Tolbert, and L. L. Bieber. 1981. Protein determination in membrane and lipoprotein samples: manual and automated procedures. Methods Enzymol. 72:296-303
39. Mastrogiacomo, A , S. M Parsons, G. A. Zampighi, D. J. Jenden, J. A. Umbach, and C. B. Gundersen 1994. Science (Wash. DC). 263:981-982.
40. McMahon, H. T., Y. A. Ushkaryov, L. Edelmann, E. Link, T. Binz, H. Niemann, R. Jahn, and T. C. Südhof. 1993. Cellubrevin is a ubiquitous tetanus-toxin substrate homologous to a putative synaptic vesicle fusion protein. Nature (Lond.). 364:346-349.
41. Mellanby, J., M. Beaumont, and P. A. Thompson. 1988. The effect of lanthanum on the nerve terminals in goldfish muscle after paralysis with tetanus toxin. Neuroscience. 25:1095-1106.
42. Montecucco, C , and G. Schiavo. 1993. Tetanus and botulism neurotoxins: a new group of zinc proteases. Trends Biochem. Sci. 18:324-327.
43. Moschella, M. C., J. Watras, T. Jayaraman, and A. R. Marks. 1995 Inositol 1,4,5-trisphosphate receptor in skeletal muscle: differential expression in myofibres. J Muscle Cell Motil. 16:390-400.
44. Neale, E. A., W. H. Habig, B. K. Schrier, G. K. Bergey, L. M. Bowers, and J. Koh. 1989. Application of tetanus toxin for structure-function studies in neuronal cell cultures In Eighth International Conference on Tetanus. G. Nisticò, B. Bizzini, B. Bytchenko, and R. Triau, editors. Pythagora Press Rome-Milan. pp. 58-65.
45. Oyler, G. A., G A. Higgins, R. A Hart, E Battenberg, M. Billingsley, F. E. Bloom, and M. C. Wilson. 1989. The identification of a novel synaptosomal-associated protein, SNAP-25, differently expressed by neuronal subpopulations. J. Cell Biol. 109:3039-3052
46. Pitzurra, L., P. Marconi, F. Bistoni, and E. Blasi. 1989. Selective inhibition of cytokine-induced lysozyme activity by tetanus toxin in the GG2EE macrophages cell line. Infect. Immun 57:2452-2456.
47. Protopopov, V., B. Govindan, P. Novick, and J. E. Gerst. 1993. Homolog of the synaptobrevin/V AMP family of synaptic vesicle proteins function on the late secretory pathway in S. cerevisiae. Cell. 74:855-861.
48. Pryer, N. K., L. J. Wuestehube, and R. Schekman. 1992 Vesicles-mediated protein sorting. Annu. Rev Biochem 61:471-516.
49. Ralston, E., S. Beushausen, and T. Ploug. 1994 Expression of the synaptic vesicle proteins VAMPs/synaptobrevins 1 and 2 in non-neuronal tissue. J. Biol. Chem. 269:15403-15406.
50. 2+ but not GTPpS-induced secretion. EMBO (Eur. Mol Biol. Organ.) J. 14:2723-2730.
51. Rothman, J. E., and L. Orci. 1992. Molecular dissection of the secretory pathway. Nature (Lond ) 355 409-415.
52. Rothman J. E., and G. Warren. 1994. Implication of the SNARE hypothesis for intracellular membrane topology and dynamics. Curr. Biol. 4:220-233.
53. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 7.43-7.52.
54. Schiavo, G., B. Poulain, O. Rossetto, F. Benfenati, L Tauc, and C. Montecucco. 1992a. Tetanus toxin is a zinc protein and its inhibition of neurotransmitter release and protease activity depend on zinc. EMBO (Eur. Mol. Biol Organ.) J 11:3577-3583.
55. Schiavo, G , F. Benfenati, B Poulain, O. Rossetto, P. Polverino de Laureto, B. R DasGupta, and C. Montecucco. 1992b. Tetanus and botulinum-B neurotoxins block neurotransmitter release by a proteolytic cleavage of synaptobrevin. Nature (Lond ) 359:832-835.
56. Schiavo, G., C. C. Shone, O. Rossetto, F. C G. Alexandre, and C. Montecucco. 1993a Botulinum neurotoxin serotype F is a zinc endopeptidase specific for VAMP/synaptobrevin. J. Biol Chem 268:11516-11519.
57. Schiavo, G , O. Rossetto, S. Catsicas, P. Polverino de Laureto, B R DasGupta, F. Benfenati, and C. Montecucco. 1993b. Identification of the nerve-terminal targets of botulinum neurotoxins serotypes A, D and E. J. Biol Chem 268: 23784-23787.
58. Schiavo, G., A Santucci, B. R. DasGupta, P. P. Metha, J. Jontes, F. Benfenati, M. C. Wilson, and C. Montecucco. 1993c. Botulinum neurotoxins serotypes A and E cleave SNAP-25 at distinct COOH-terminal peptide bonds FEBS Lett 335:99-103.
59. Schiavo, G., C Malizio, W. S. Trimble, P Polverino de Laureto, G. Milan, H Sugiyama, E A. Johnson, and C Montecucco. 1994. Botulinum G neurotoxin cleaves VAMP/synaptobrevin at a single Ala/Ala peptide bond J. Biol. Chem. 269:20213-20216.
60. Schuldiner, S., A. Shirvan, and M. Linial 1995. Vesicular neurotransmitter transporters: from bacteria to humans Physiol. Rev. 75:369-392.
61. Simons, K., and M. Zerial. 1993. Rab proteins and the road maps for intracellular transport. Neuron 11:789-799.
62. Söllner, T., S. W. Whiteheart, M. Brunner, H Erdjument-Bromage, S. Geromanos, P. Tempst, and J. E. Rothman. 1993a. Snap receptors implicated in vesicle targeting and fusion. Nature (Lond ) 362:318-324.
63. Sollner, T., M. K. Bennett, S. W. Whiteheart, R. H. Scheller, and J. E. Rothman. 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.
64. Stecher, B., U. Weller, E. Habermann, M. Gratzl, and G. Ahnert-Hilger. 1989 The light chain but not the heavy chain of botulinum A toxin inhibits exocytosis from permeabilized adrenal chromaffin cells FEBS Lett. 255 391-394.
65. Südhof, T., M. Baumert, M. S. Perin, and R. Jahn. 1989. A synaptic vesicle membrane protein is conserved from mammals to Drosophila. Neuron 2, 1475-1481.
66. Südhot, T. 1995. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature (Lond ) 375:645-653.
67. Sweeney, S. T , K. Broadie, J Keane, H. Niemann, and J. O'Kane. 1995. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron. 14:341-351
68. Takei, K., P. S. McPherson, S. L. Schmid, and P. De Camilli. 1995. Tubular membrane invaginations coated by dynamin rings are induced by GTP-pS in nerve terminals. Nature (Lond ) 374:186-190.
69. Towbin, H., T. Stahelin, and J. Gordon. 1979 Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets, procedure and some applications. Proc. Natl Acad Sci USA 76:4350-4354
70. Trimble, W. S , D. M Cowan, and R. H. Scheller. 1988. VAMP-1, a synaptic vesicle-associated protein. Proc. Natl. Acad. Sci USA. 85:4538-4542.
71. Trimble, W. S., M. Linial, and R H. Scheller. 1991. Cellular and molecular biology of the presynaptic nerve terminal Annu Rev Neurosci 14:93-122.
72. Vaitukaitis, J. L. 1981. Production of antisera with small doses of immunogen: multiple intradermal injections. Methods Enzymol. 73:4652.
73. Valtorta, F., F. Benfenati, and P. Greengard. 1992. Structure and function of the synapsins. J. Biol. Chem. 267:7195-7198.
74. Walton, K. M., K. Sandberg, T. B. Rogers, and R. L Schnaar. 1988. Complex ganglioside expression and tetanus toxin binding by PC12 pheochromocytoma cells. J. Biol. Chem. 263:2055-2063.
75. Warren, G. 1993. Bridging the gap. Nature (Lond ) 362:297-298.
76. Washbourne, P., G Schiavo, and C Montecucco. 1995. VAMP-2 forms a complex with synaptophysin Biochem J. 305:721-724.
77. Yamasaki, S., Y. G. Hu, T. Binz, A. Kalkuhl, H Kurazono, T. Tamura, R. Jahn, E. Kandel, and H. Niemann. 1994. Synaptobrevin vesicle-associated membrane-protein (VAMP) of Aplysia californica Structure and proteolysis by tetanus toxin and botulinal neurotoxins type-D and type-F. Proc Natl Acad Sci. USA. 91:4688-4692.
78. Zinsmaier, K E., K. K. Eberle, E. Buchner, N. Walter, and S. Benzer. 1994. Science (Wash DC) 263:977-980.