Evidence against an acute inhibitory role of nSec-1 (Munc-18) in late steps of regulated exocytosis in chromaffin and PC12 cells

Journal of Neurochemistry

Volumn 69, Issue 6, 1997, Pages 2369-2377

  Graham, Margaret E ^a   Sudlow, Allan W ^a   Burgoyne, Robert D ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Chromaffin cells; Exocytosis; Growth hormone secretion; NSec 1 (munc 18) protein; PC12 cells; Soluble N ethylmaleimide sensitive fusion protein attachment protein

Indexed keywords

SYNAPTOBREVIN;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CELL STRAIN; CHROMAFFIN CELL; DROSOPHILA; EXOCYTOSIS; GENE EXPRESSION; GROWTH HORMONE RELEASE; HORMONE SYNTHESIS; MAMMAL; NEUROTRANSMISSION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS;

ANIMALIA; CAENORHABDITIS ELEGANS; MAMMALIA;

EID: 0030719996     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1997.69062369.x     Document Type: Article

References (63)

1. Aalto M. K., Ronne H., and Keranen S. (1993) Yeast syntaxins Sso1p and Sso2p belong to a family of related membrane proteins that function in vesicular transport. EMBO J. 12, 4095-4104.
2. 2+ activated exocytosis. J. Biol. Chem. 271, 20223-20226.
3. Barnard R. J. O., Morgan A., and Burgoyne R. D. (1996) Domains of α-SNAP required for the stimulation of exocytosis and for NSF binding and activation. Mol. Biol. Cell 7, 693-701.
4. Baumert M., Maycox P. R., Navone F., De Camilli P., and Jahn R. (1989) Synaptobrevin: an integral membrane protein of 18,000 daltons in small synaptic vesicles of rat brain. EMBO J. 8, 379-384.
5. Bennett M. K., Calakos N., and Scheller R. H. (1992) Syntaxin: a synaptic protein implicated in docking of synaptic vesicle at presynaptic active zones. Science 257, 255-259.
6. Bennett M. K., Garcia-Arraras G., Elferink L. A., Peterson K., Fleming A. M., Hazuka C. D., and Scheller R. H. (1993) The syntaxin family of vesicular transport receptors. Cell 74, 863-873.
7. Blasi J., Chapman E. R., Yamasaki S., Binz T., Niemann H., and Jahn R. (1993) Botulinum neurotoxin C1 blocks neurotransmitter release by means of cleaving HPC-1/syntaxin. EMBO J. 12, 4821-4828.
8. Burgoyne R. D. (1992) Investigation of the intracellular regulators and components of the exocytotic pathway, in Neuromethods, Vol. 20: Intracellular Messengers (Boulton A. A., Baker G., and Taylor C., eds), pp. 433-470. Humana Press, Totowa, New Jersey.
9. Calakos N. and Scheller R. H. (1996) Synaptic vesicle biogenesis, docking, and fusion: a molecular description. Physiol. Rev. 76, 1-29.
10. Chamberlain L. H., Roth D., Morgan A., and Burgoyne R. D. (1995) Distinct effects of α-SNAP, 14-3-3 proteins and calmodulin on priming and triggering of regulated exocytosis. J. Cell Biol. 130, 1063-1071.
11. Chamberlain L. H., Henry J., and Burgoyne R. D. (1996) Cysteine string proteins are associated with chromaffin granules. J. Biol. Chem. 271, 19514-19517.
12. Ferro-Novick S. and Jahn R. (1994) Vesicle fusion from yeast to man. Nature 370, 191-193.
13. Gaisano H. Y., Ghai M., Malkus P. N., Sheu L., Bouquillon A., Bennett M. K., and Trimble W. S. (1996) Distinct cellular locations of the syntaxin family of proteins in rat pancreatic acinar cells. Mol. Biol. Cell 7, 2019-2027.
14. Garcia E. P., Gatti E., Butler M., Burton J., and De Cammille P. (1994) A rat brain Sec1 homologue related to Rop and UNC18 interacts with syntaxin. Proc. Natl. Acad. Sci. USA 91, 2003-2007.
15. Garcia E. P., McPherson P. S., Chilcote T. J., Takei K., and DeCamilli P. (1995) rbSec1A and B colocalize with syntaxin 1 and SNAP-25 throughout the axon but are not in a stable complex with syntaxin. J. Cell Biol. 129, 105-120.
16. Gengyo-Ando K., Kitayama H., Mukaida M., and Ikawa Y. (1996) A murine neural specific homolog corrects cholinergic defects in Caenorhabditis elegans unc-18 mutants. J. Neurosci. 16, 6695-6702.
17. 2+-dependent exocytosis. Mol. Biol. Cell 8, 431-442.
18. Harrison S. D., Broadie K., van de Goor J., and Rubin G. M. (1994) Mutations in the Drosophila rop gene suggest a function in general secretion and synaptic transmission. Neuron 13, 555-566.
19. Hata Y. and Südhof T. C. (1995) A novel ubiquitous form of Munc-18 interacts with multiple syntaxins. J. Biol. Chem. 270, 13022-13028.
20. Hata Y., Slaughter C. A., and Südhof T. C. (1993) Synaptic vesicle fusion complex contains unc-18 homologue bound to syntaxin. Nature 366, 347-351.
21. Hayashi T., Yamasaki S., Nauenburg S., Binz T., and Niemann H. (1995) Disassembly of the reconstituted synaptic vesicle membrane complex in vitro. EMBO J. 14, 2317-2325.
22. Hodel A., Schafer T., Gerosa D., and Burger M. M. (1994) In chromaffin cells, the mammalian Sec1p homologue is a syntaxin 1A-binding protein associated with chromaffin granules. J. Biol. Chem. 269, 8623-8626.
23. 2+-dependent exocytosis from adrenal chromaffin cells. J. Biol. Chem. 269, 10229-10234.
24. Hosono R., Hekimi S., Kamiya Y., Sassa T., Murakami S., Nishiwaki K., Miwa J., Taketo A., and Kodaira K.-I. (1992) The unc-18 gene encodes a novel protein affecting the kinetics of acetylcholine metabolism in the nematode Caenorhabditis elegans. J. Neurochem. 58, 1517-1525.
25. 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.
26. Katagiri H., Terasaki J., Murata T., Ishihara H., Ogihara T., Inukai K., Fukushima Y., Anai M., Kikuchi M., Miyazaki J.-I., Yazaki Y., and Oka Y. (1995) A novel isoform of syntaxin-binding protein homologues to yeast Sec1 expressed ubiquitously in mammalian cells. J. Biol. Chem. 270, 4963-4966.
27. Kibble A. V., Barnard R. J. O., and Burgoyne R. D. ( 1996) Patchclamp capacitance analysis of the effects of alpha-SNAP on exocytosis in adrenal chromaffin cells. J. Cell Sci. 109, 2417-2422.
28. Koenig J. H. and Ikeda K. (1989) Disappearance and reformation of synaptic vesicle membrane upon transmitter release observed under reversible blockage of membrane retrieval. J. Neurosci. 11, 3844-3860.
29. Kretzschmar S., Volknandt W., and Zimmermann H. (1996) Colocalisation on the same synaptic vesicles of syntaxin and SNAP-25 with synaptic vesicle proteins: a re-evaluation of functional models required? Neurosci. Res. 26, 141-148.
30. Matsuuchi L. and Kelly R. B. (1991) Constitutive and basal secretion from the endocrine cell line, AtT-20. J. Cell Biol. 112, 843-852.
31. McClenaghan M., Springbett A., Wallace R. M., Wile C. J., and Clark A. J. (1995) Secretory protens compete for production in the mammary gland of transgenic mice. Biochem. J. 310, 637-641.
32. McMahon H. T., Missler M., Li C., and Sudhof T. C. (1995) Complexins: cytosolic proteins that regulate SNAP receptor function. Cell 83, 111-119.
33. Montecucco C. and Schiavo G. (1994) Molecular mechanisms of action of bacterial protein toxins. Mol. Microbiol. 13, 1-8.
34. Morgan A. and Burgoyne R. D. (1992) Exo1 and Exo2 proteins stimulate calcium-dependent exocytosis in permeabilized adrenal chromaffin cells. Nature 355, 833-835.
35. Morgan A. and Burgoyne R. D. (1995a) A role for soluble NSF attachment proteins (SNAPs) in regulated exocytosis in adrenal chromaffin cells. EMBO J. 14, 232-239.
36. Morgan A. and Burgoyne R. D. (1995b) Is NSF a fusion protein? Trends Cell Biol. 5, 335-339.
37. Morgan A. and Burgoyne R. D. (1997) Common mechanisms for regulated exocytosis in the chromaffin cell and the synapse. Semin. Cell Dev. Biol. 8, 141-149.
38. Niemann H., Blasi J., and Jahn R. (1994) Clostridial neurotoxins: new tools for dissecting exocytosis. Trends Cell Biol. 4, 179-185.
39. Novick P., Ferro S., and Schekman R. (1981) Order of events in the yeast secretory pathway. Cell 25, 461-469.
40. Oyler G. A., Higgins G. A., Hart R. A., Battenberg E., Billingsley M., Bloom F. E., and Wilson M. C. (1989) The identification of a novel synaptosomal-associated protein SNAP-25, differentially expressed by neuronal subpopulations. J. Cell Biol. 109, 3039-3052.
41. Pallanck L., Ordway R. W., and Ganetzky B. (1995) A Drosophila NSF mutant. Nature 376, 25.
42. Pevsner J. (1996) The role of Sec1p-related proteins in vesicle trafficking in the nerve terminal. J. Neurosci. Res. 45, 89-95.
43. Pevsner J., Hsu S.-C., Braun J. E. A., Calakos N., Ting A. E., Bennett M. K., and Scheller R. H. (1994a) Specificity and regulation of a synaptic vesicle docking complex. Neuron 13, 353-361.
44. Pevsner J., Hsu S. C., and Scheller R. (1994b) n-Sec1: a neuralspecific syntaxin-binding protein. Proc. Natl. Acad. Sci. USA 91, 1445-1449.
45. Pryer N. K., Wuestehube L. J., and Schekman R. (1992) Vesicle-mediated protein sorting. Annu. Rev. Biochem. 61, 471-516.
46. Roth D. and Burgoyne R. D. (1994) SNAP-25 is present in a SNARE complex in adrenal chromaffin cells. FEBS Lett. 351, 207-210.
47. Rothman J. E. (1994) Mechanisms of intracellular protein transport. Nature 372, 55-62.
48. Ryan T. A. (1996) Endocytosis at nerve terminals: timing is everything. Neuron 17, 1035-1037.
49. Schafer T., Karli U. O., Schweizer F. E., and Burger M. M. (1987) Docking of chromaffin granules - a necessary step in exocytosis. Biosci. Rep. 7, 269-279.
50. 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.
51. Schulze K. L., Littleton J. T., Salzberg A., Halachmi N., Stern M., Lev Z., and Bellen H. J. (1994) rop, a Drosophila homolog of yeast sec1 and vertebrate n-sec1/munc 18 proteins, is a negative regulator of neurotransmitter release in vivo. Neuron 13, 1099-1108.
52. Schweitzer E. S. and Kelly R. B. (1985) Selective packaging of human growth-hormone into synaptic vesicles in a rat neuronal (PC12) cell-line. J. Cell Biol. 101, 667-676.
53. Shetty K. T., Kaech S., Link W. T., Jaffe H., Flores C. M., Wray S., Pant H. C., and Beushausen S. (1995) Molecular characterization of a neuronal specific protein that stimulates the activity of Cdk5. J. Neurochem. 64, 1988-1995.
54. Sollner T., Bennett M. K., Whiteheart S. W., Scheller R., and Rothman J. (1993a) A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75, 409-418.
55. Sollner T., Whiteheart S. W., Brunner M., Erdjument-Bromage H., Geromanos S., Tempst P., and Rothman J. E. (1993b) SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318-324.
56. Südhof T. C. (1995) The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375, 645-653.
57. 2+-regulated exocytosis. FEBS Lett. 393, 185-188.
58. Tagaya M., Toyonaga S., Takahashi M., Yamamoto A., Fujiwara T., Akagawa K., Moriyama Y., and Mizushima S. (1995) Syntaxin 1 (HPC-1) is associated with chromaffin granules. J. Biol. Chem. 270, 15930-15933.
59. Tellam J. T., McIntosh S., and James D. E. (1995) Molecular identifications of two novel Munc-18 isoforms expressed in non-neuronal tissues. J. Biol. Chem. 270, 5857-5863.
60. Tooze S. A., Flatmark T., Tooze J., and Huttner W. B. (1991) Characterisation of the immature secretory granule, an intermediate in granule biogenesis. J. Cell Biol. 115, 1491-1503.
61. Trimble W. S., Cowan D. M., and Scheller R. H. (1988) VAMP-1: a synaptic vesicle-associated integral membrane protein. Proc. Natl. Acad. Sci. USA 85, 4538-4542.
62. Walch-Solimena C., Blasi J., Edelmann L., Chapman E. R., Fischer von Mollard G., and Jahn R. (1995) The t-SNAREs syntaxin 1 and SNAP-25 are present on organelles that participate in synaptic vesicle recycling. J. Cell Biol. 128, 637-645.
63. Wick P. F., Senter R. A., Parsels L. A., Uhler M. D., and Holz R. W. (1993) Transient transfection studies of secretion in bovine chromaffin cells and PC12 cells. Generation of kainate-sensitive chromaffin cells. J. Biol. Chem. 268, 10983-10989.