Relocation of the t-SNARE SNAP-23 from lamellipodia-like cell surface projections regulates compound exocytosis in mast cells

Cell

Volumn 94, Issue 4, 1998, Pages 537-548

  Guo, Zhenheng ^a   Turner, Christopher ^a,b   Castle, David ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^b Incyte Pharmaceuticals Inc ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNTAXIN;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; CYTOSKELETON; EXOCYTOSIS; IMMUNOFLUORESCENCE MICROSCOPY; LAMELLIPODIUM; MAST CELL; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT;

ANIMALIA;

EID: 0032555722     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81594-9     Document Type: Article

References (59)

1. Abraham, S.N., and Malaviya, R. (1997). Mast cells in infection and immunity. Infect. Immun. 65, 3501-3508.
2. Alvarez de Toledo, G., and Fernandez, J.M. (1990). Compound versus multigranular exocytosis in peritoneal mast cells. J. Gen. Physiol. 95, 397-409.
3. Anderson, P., Slorach, S.A., and Uvnas, B. (1973). Sequential exocytosis of storage granules during antigen-induced histamine release from sensitized rat mast cells in vitro. An electron microscopic study. Acta Physiol. Scand. 88, 359-372.
4. Araki, S., Tamori, Y., Kawanishi, M., Shinoda, H., Masugi, J., Mori, H., Niki, T., Okazawa, H., Kubota, T., and Kasuga, M. (1997). Inhibition of the binding of SNAP-23 to syntaxin 4 by Munc18c. Biochem. Biophys. Res. Commun. 234, 257-262.
5. i3. Science 262, 1569-1572.
6. 2+-dependent exocytosis. J. Biol. Chem. 271, 20227-20230.
7. Bennett, M.K., García-Arrarás, J.E., 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.
8. Bock, J.B., and Scheller, R.H. (1997). Protein transport. A fusion of new ideas. Nature 387, 133-135.
9. Brand, S.H., and Castle, J.D. (1993). SCAMP 37, a new marker within the general cell surface recycling system. EMBO J. 12, 3753-3761.
10. Brown, A.M., O'Sullivan, A.J., and Gomperts, B.D. (1998). Induction of exocytosis from permeabilized mast cells by the guanosine triphosphatases Rac and Cdc42. Mol. Biol. Cell 9, 1053-1063.
11. Burry, R.W., Vandre, D.D., and Hayes, D.M. (1992). Silver enhancement of gold antibody probes in pre-embedding electron microscopic immunocytochemistry. J. Histochem. Cytochem. 40, 1849-1856.
12. Chen, F., Foran, P., Shone, C.C., Foster, K.A., Melling, J., and Dolly, J.O. (1997). Botulinum neurotoxin B inhibits insulin-stimulated glucose uptake into 3T3-I1 adipocytes and cleaves cellubrevin unlike type A toxin which failed to proteolyze the SNAP-23 present. Biochemistry 36, 5719-5728.
13. Chock, S.P., and Schmauder-Chock, E.A. (1989). Phospholipid storage in the secretory granule of the mast cell. J. Biol. Chem. 264, 2862-2868.
14. Fernandez, J.M., Villalon, M., and Verdugo, P. (1991). Reversible condensation of mast cell secretory products in vitro. Biophys. J. 59, 1022-1027.
15. Ferro-Novick, S., and Jahn, R. (1994). Vesicle fusion from yeast to man. Nature 370, 191-193.
16. Fox, J.E.B., Boyles, J.K., Berndt, M.C., Steffen, P.K., and Anderson, L.K. (1988). Identification of a membrane skeleton in platelets. J. Cell Biol. 106, 1525-1538.
17. Gaisano H.Y., Sheu, L., Wong, P.P., Klip, A., and Trimble, W.S. (1997). SNAP-23 is located in the basolateral plasma membrane of rat pancreatic acinar cells. FEBS Lett. 414, 298-302.
18. Galli, T., Zahraoui, A., Vaidyanathan, V.V., Raposo, G., Tian, J.M., Karin, M., Niemann, H., and Louvard, D. (1998). A novel tetanus neurotoxin-insensitive vesicle-associated membrane protein in SNARE complexes of the apical plasma membrane of epithelial cells. Mol. Biol. Cell 9, 1437-1448.
19. Gomperts, B.D., and Tatham, P.E. (1992). Regulated exocytotic secretion from permeabilized cells. Methods Enzymol. 219, 178-189.
20. Hay, J.C., and Scheller, R.H. (1997). SNAREs and NSF in targeted membrane fusion. Curr. Opin. Cell Biol. 9, 505-512.
21. Heidelberger, R. (1998). Adenosine triphosphate and the late steps in calcium-dependent exocytosis at the ribbon synapse. J. Gen. Physiol. 111, 225-241.
22. Hess, D.T., Slater, T.M., Wilson, M.C., and Skene, J.H. (1992). The 25 kDa synaptosomal-associated protein SNAP-25 is the major methionine-rich polypeptide in rapid axonal transport and a major substrate for palmitoylation in adult CNS. J. Neurosci. 12, 4634-4641.
23. 2+ and guanine nucleotides: an all-or-none event. J. Cell Biol. 123, 585-593.
24. Hohne-Zell, B., and Gratzl, M. (1996). Adrenal chromaffin cells contain functionally different SNAP-25 monomers and SNAP-25/syntaxin heterodimers. FEBS Lett. 394, 109-116.
25. Jacobson, 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.
26. Kannan, R., Grant, N.J., Aunis, D., and Langley, K. (1996). SNAP-25 is differentially expressed by noradrenergic and adrenergic chromaffin cells. FEBS Lett. 385, 159-164.
27. Kemble, G.W., Danieli, T., and White, J.M. (1994). Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion. Cell 76, 383-391.
28. Koffer, A. (1993). Calcium-induced secretion from permeabilized rat mast cells: requirements for guanine nucleotides. Biochim. Biophys. Acta 1176, 231-239.
29. Koffer, A., and Churcher, Y. (1993). Calcium and GTP-gamma-S as single effectors of secretion from permeabilized rat mast cells: requirements for ATP. Biochim. Biophys. Acta 1176, 222-230.
30. Koffer, A., Tatham, P.E., and Gomperts, B.D. (1990). Changes in the state of actin during the exocytotic reaction of permeabilized rat mast cells. J. Cell Biol. 111, 919-927.
31. Kruger, P.G., Lagunoff, D., and Wan, H. (1980). Isolation of rat mast cell granules with intact membranes. Exp. Cell Res. 129, 83-93.
32. Mariot, P., O'Sullivan, A.J., Brown, A.M., and Tatham, P.E. (1996). Rho guanine nucleotide dissociation inhibitor protein (RhoGDI) inhibits exocytosis in mast cells. EMBO J. 15, 6476-6482.
33. 2+)-dependent triggering of neurotransmitter exocytosis. Proc. Natl. Acad. Sci. USA 93, 10471-10476.
34. Miller, S.G., and Moore, H.P. (1992). Movement from trans-Golgi network to cell surface in semiintact cells. Methods Enzymol. 219, 234-248.
35. Mollinedo, F., and Lazo, P.A. (1997). Identification of two isoforms of the vesicle-membranefusion protein SNAP-23 in human neutrophils and HL-60 cells. Biochem. Biophys. Res. Commun. 231, 808-812.
36. Nobes, C.D., and Hall, A. (1995). Rho, Rac, and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62.
37. Norman, J.C., Price, L.S., Ridley, A.J., and Koffer, A. (1996). The small GTP-binding proteins, Rac and Rho, regulate cytoskeletal organization and exocytosis in mast cells by parallel pathways. Mol. Biol. Cell 7, 1429-1442.
38. Oberhauser, A.F., Monck, J.R., Balch, W.E., and Fernandez, J.M. (1992). Exocytotic fusion is activated by Rab3a peptides. Nature 360, 270-273.
39. Oberhauser, A.F., Robinson, I.M.,and Fernandez, J.M. (1996). Simultaneous capacitance and amperometric measurements of exocytosis: a comparison. Biophys. J. 71, 1131-1139.
40. O'Sullivan, A., Brown, A.M., Freeman, H.N., and Gomperts, B.D. (1996). Purification and identification of FOAD-II, acytosolic protein that regulates secretion in streptolysin-O permeabilized mast cells, as a rac/rhoGDI complex. Mol. Biol. Cell 7, 397-408.
41. Otto, H., Hanson, P.I., and Jahn, R. (1997). Assembly and disassembly of a ternary complex of synaptobrevin, syntaxin, and SNAP-25 in the membrane of synaptic vesicles. Proc. Natl. Acad. Sci. USA 94, 6197-6201.
42. 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.
43. Palade, G.E. (1959). Functional changes in the structure of cell components. In Subcellular Particles, T. Hayashi, ed. (New York: Ronald Press), pp. 64-83.
44. Parsons, T.D., Coorssen, J.R., Horstmann, H., and Almers, W. (1995). Docked granules, the exocytic burst, and the need for ATP hydrolysis in endocrine cells. Neuron 15, 1085-1096.
45. Price, L.S., Norman, J.C., Ridley, A.J., and Koffer, A. (1995). The small GTPases Rac and Rho as regulators of secretion in mast cells. Curr. Biol. 5, 68-73.
46. Ravichandran, V., Chawla, A., and Roche, P.A. (1996). Identification of a novel syntaxin-and synaptobrevin/VAMP-binding protein, SNAP-23, expressed in non-neuronal tissues. J. Biol. Chem. 271, 13300-13303.
47. Rossi, G., Salminen, A., Rice, L.M., Brunger, A.T., and Brennwald, P. (1997). Analysis of a yeast SNARE complex reveals remarkable similarity to the neuronal SNARE complex and a novel function for the C terminus of the SNAP-25 homolog, Sec9. J. Biol. Chem. 272, 16610-16617.
48. Rothman, J.E. (1994). Mechanisms of intracellular protein transport. Nature 372, 55-63.
49. Sadoul, K.S., Berger, A., Niemann, H., Weller, L.J., Roche, P.A., Klip, A., Trimble, W.S., Regazzi, R., Catsicas, S., and Halban, P.A. (1997). SNAP-23 is not cleaved by botulinum neurotoxin E and can replace SNAP-25 in the process of insulin secretion. J. Biol. Chem. 272, 33023-33027.
50. Sargiacomo, M., Sudol, M., Tang, Z., and Lisanti, M.P. (1993). Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J. Cell Biol. 122, 789-807.
51. Sollner, T., Whiteheart, S.W., Brunner, M., Erdjument-Bromage, H., Geromanos, S., Tempst, P., and Rothman, J.E. (1993). SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318-324.
52. Sudhof, T.C. (1995). Thesynaptic vesicle cycle: acascade of protein-protein interactions. Nature 375, 645-653.
53. Tagaya, M., Genma, T., Yamamoto, A., Kozaki, S., and Mizushima, S. (1996). SNAP-25 is present on chromaffin granules and acts as a SNAP receptor. FEBS Lett. 394, 83-86.
54. Ungermann, C., and Wickner, W. (1998). Vam7p, a vacuolar SNAP-25 homolog, is required for SNARE complex integrity and vacuole docking and fusion. EMBO J. 17, 3269-3276.
55. Veit, M., Sollner, T.H., and Rothman, J.E. (1996). Multiple palmitoylation of synaptotagmin and the t-SNARE SNAP-25. FEBS Lett. 385, 119-123.
56. Walch-Solimena, C., Blasi, J., Edelmann, L., Chapman, E.R., von Mollard, G.F., 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.
57. Wang, G., Witkin, J.W., Hao, G., Bankaitis, V.A., Scherer, P.E., and Baldini, G. (1997). Syndet is a novel SNAP-25 related protein expressed in many tissues. J. Cell Sci. 110, 505-513.
58. Wong, P.P., Daneman, N., Volchuk, A., Lassam, N., Wilson, M.C., Klip, A., and Trimble, W.S. (1997). Tissue distribution of SNAP-23 and its subcellular localization in 3T3-L1 cells. Biochem. Biophys. Res. Commun. 230, 64-68.
59. Wu, T.T., and Castle, J.D. (1997). Evidence for colocalization and interaction between 37 and 39 kDa isoforms of secretory carrier membrane proteins (SCAMPs). J. Cell Sci. 110, 1533-1541.