Soluble NSF attachment protein receptors (SNAREs) in RBL-2H3 mast cells: Functional role of syntaxin 4 in exocytosis and identification of a vesicle- associated membrane protein 8-containing secretory compartment

Journal of Immunology

Volumn 164, Issue 11, 2000, Pages 5850-5857

  Paumet, Fabienne ^a   Le Mao, Joëlle ^a   Martin, Sophie ^a   Galli, Thierry ^b   David, Bernard ^a   Blank, Ulrich ^a   Roa, Michèle ^a  

^a INSTITUT PASTEUR   (France)

^b INSTITUT CURIE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELLUBREVIN; IMMUNOGLOBULIN E RECEPTOR; SNARE PROTEIN; SYNAPTOBREVIN; SYNTAXIN; SYNTAXIN 4; UNCLASSIFIED DRUG; VESICLE ASSOCIATED MEMBRANE PROTEIN 8;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOSOME; EXOCYTOSIS; INFLAMMATION; MAST CELL; MEMBRANE VESICLE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN PROTEIN INTERACTION; RAT; SECRETORY GRANULE;

EID: 0034081439     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.164.11.5850     Document Type: Article

References (62)

1. Abraham, S. N., and R. Malaviya. 1997. Mast cells in infection and immunity. Infect. Immun. 65:3501.
2. Galli, S. J., and C. S. Lantz. 1999. Allergy. In Fundamental Immunology. W. E. Paul, ed. Lippincott-Raven, Philadelphia, p. 1127.
3. Raposo, G., D. Tenza, S. Mecheri, R. Peronet, C. Bonnerot, and C. Desaymard. 1997. Accumulation of major histocompatibility complex class II molecules in mast cell secretory granules and their release upon degranulation. Mol. Biol. Cell 8:2631.
4. Xu, K., R. M. Williams, D. Holowka, and B. Baird. 1998. Stimulated release of fluorescently labeled IgE fragments that efficiently accumulate in secretory granules after endocytosis in RBL-2H3 mast cells. J. Cell Sci. 111:2385.
5. Griffiths, G. M. 1996. Secretory lysosomes: a special mechanism of regulated secretion in haemopoietic cells. Trends Cell Biol. 6:329.
6. Raposo, G., M. Vidal, and H. Geuze. 1997. Secretory lysosomes and the production of exosomes. In Unusual Secretory Pathways: From Bacteria to Man. K. Kuchler, A. Rubartelli, and B. Holland, eds. R. G. Landes Company, Austin, p. 161.
7. Stinchcombe, J. C., and G. M. Griffiths. 1999. Regulated secretion from hemopoietic cells. J. Cell Biol. 147:1.
8. Kinet, J. P. 1999. The high-affinity IgE receptor (Fc∈RI): from physiology to pathology. Annu. Rev. Immunol. 17:931.
9. Söllner, T., S. W. Whiteheart, M. Brunner, H. Erdjument-Bromage, S. Geromanos, P. Tempst, and J. E. Rothman. 1993. SNAP receptors implicated in vesicle targeting and fusion. Nature 362:318.
10. Südhof, T. C. 1995. The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375:645.
11. Goda, Y. 1997. SNAREs and regulated vesicle exocytosis. Proc. Natl. Acad. Sci. USA 94:769.
12. Weber, T., B. V. Zemelman, J. A. McNew, B. Westermann, M. Gmachl, F. Parlati, T. H. Söllner, and T. H. Rothman. 1998. SNAREpins: minimal machinery for membrane fusion. Cell 92:759.
13. Poirier, M. A., W. Xiao, J. C. Macosko, C. Chan, Y. K. Shin, and M. K. Bennett. 1998. The synaptic SNARE complex is a parallel four-stranded helical bundle. Nat. Struct. Biol. 5:765.
14. Sutton, R. B., D. Fasshauer, R. Jahn, and A. T. Brunger. 1998. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution. Nature 395:347.
15. Canaves, J. M., and M. Montal. 1998. Assembly of a ternary complex by the predicted minimal coiled-coil-forming domains of syntaxin, SNAP-25, and synaptobrevin. J. Biol. Chem. 273:34214.
16. Hay, J. C., and R. H. Scheller. 1997. SNAREs and NSF in targeted membrane fusion. Curr. Opin. Cell Biol. 9:505.
17. Bock, J. B., and R. H. Scheller. 1997. A fusion of new ideas. Nature 387:133.
18. Ravichandran, V., A. Chawla, and P. A. Roche. 1996. Identification of a novel syntaxin-and synaptobrevin/VAMP-binding proteins, SNAP-23, expressed in non-neuronal tissues. J. Biol. Chem. 271:13300.
19. Wang, G., J. W. Witkin, G. Hao, V. A. Bankaitis, P. E. Scherer, and G. Baldini. 1997. Syndet is a novel SNAP-25 related protein expressed in many tissues. J. Cell Sci. 110:505.
20. Sadoul, K., A. Berger, H. Niemann, U. Weller, P. A. Roche, A. Klip, W. S. Trimble, R. Regazzi, S. Catsicas, and P. A. Halban. 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.
21. Low, S. H., S. J. Chapin, C. Wimmer, S. W. Whiteheart, L. G. Kömüves, K. E. Mostov, and T. Weimbs. 1998. The SNARE machinery is involved in apical plasma membrane trafficking in MDCK cells. J. Cell Biol. 141:1503.
22. Lafont, F., P. Verkade, T. Galli, C. Wimmer, D. Louvard, and K. Simons. 1999. Raft association of SNAP receptors acting in apical trafficking in Madin-Darby canine kidney cells. Proc. Natl. Acad. Sci. USA 96:3734.
23. Bennett, M. K., J. E. Garcia-Arraras, 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.
24. Volchuk, A., Q. Wang, S. Ewart, Z. Liu, L. He, M. K. Bennett, and A. Klip. 1996. Syntaxin 4 in 3T3-L1 adipocytes: regulation by insulin and participation in insulin-dependent glucose transport. Mol. Biol. Cell 7:1075.
25. Tellam, J. T., S. L. Macaulay, S. McIntosh, D. R. Hewish, C. W. Ward, and D. E. James. 1997. Characterization of Munc-18c and syntaxin-4 in 3T3-L1 adipocytes. J. Biol. Chem. 272:6179.
26. Link, E., L. Edelman, J. H. Chou, T. Binz, S. Yamasaki, V. Eisel, M. Baumert, T. C. Südhof, H. Niemann, and R. Jahn. 1992. Tetanus toxin action: inhibition of neurotransmitter release linked to synaptobrevin proteolysis. Biochem. Biophys. Res. Commun. 189:1017.
27. Schiavo, G., F. Benfenati, B. Poulain, O. Rossetto, P. Polverino de Laureto, B. R. DasGupta, and C. Montecucco. 1992. Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359:832.
28. Chilcote, T. J., T. Galli, O. Mundigl, L. Edelmann, P. S. McPherson, K. Takei, and P. De Camilli. 1995. Cellubrevin and synaptobrevins: similar subcellular localization and biochemical properties in PC12 cells. J. Cell Biol. 129:219.
29. 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 364:346.
30. Galli, T., T. Chilcote, O. Mundigl, T. Binz, H. Niemann, and P. De Camilli. 1994. Tetanus toxin-mediated cleavage of Cellubrevin impairs exocytosis of transferrin receptor-containing vesicles in CHO cells. J. Cell Biol. 125:1015.
31. Teter, K., G. Chandy, B. Quinones, K. Pereyra, T. Machen, and H. P. H. Moore. 1998. Cellubrevin-targeted fluorescence uncovers heterogeneity in the recycling endosomes. J. Biol. Chem. 273:19625.
32. Galli, T., A. Zahraoui, V. V. Vaidyanathan, G. Raposo, J. M. Tian, M. Karin, H. Niemann, and D. Louvard. 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.
33. Advani, R. J., B. Yang, R. Prekeris, K. C. Lee, J. Klumperman, and R. H. Scheller. 1999. VAMP-7 mediates vesicular transport from endosomes to lysosomes. J. Cell Biol. 146:765.
34. Wong, S. H., T. Zhang, Y. Xu, N. Subramaniam, G. Griffiths, and W. Hong. 1998. Endobrevin, a novel synaptobrevin/VAMP-like protein preferentially associated with the early endosome. Mol. Biol. Cell 9:1549.
35. Advani, R. J., H. R. Bae, J. B. Bock, D. S. Chao, Y. C. Doung, R. Prekeris, J. S. Yoo, and R. H. Scheller. 1998. Seven novel mammalian SNARE proteins localize to distinct membrane compartments. J. Biol. Chem. 273:10317.
36. Gonzalez, L., and R. H Scheller. 1999. Regulation of membrane trafficking: structural insights from a rableffector complex. Cell 96:755.
37. Roa, M., F. Paumet, J. Le Mao, B. David, and U. Blank. 1997. Involvement of the ras-like GTPase rab3d in RBL-2H3 mast cell exocytosis following stimulation via high affinity IgE receptors (Fc∈RI). J. Immunol. 159:2815.
38. 2+-triggered exocytosis of lysosomes in mast cells. J. Exp. Med. 189:1649.
39. Flaumenhaft, R., K. Croce, E. Chen, B. Furie, and B. C. Furie. 1999. Proteins of the exocytotic core complex mediate platelet α-granule secretion. J. Biol. Chem. 274:2492.
40. Hackam, D. J., O. D. Rotstein, C. Sjolin, A. D. Schreiber, W. S. Trimble, and S. Grinstein. 1998. v-SNARE-dependent secretion is required for phagocytosis. Proc. Natl. Acad. Sci. USA 95:11691.
41. Chen, H., M. Centola, S. F. Altschul, and H. Metzger. 1998. Characterization of gene expression in resting and activated mast cells. J. Exp. Med. 188:1657.
42. Guo, Z., C. Turner, and D. Castle. 1998. Relocation of the t-SNARE SNAP23 from lamellipodia-like cell surface projections regulates compound exocytosis in mast cells. Cell 94:537.
43. Volchuk, A., R. Sargeant, S. Sumitani, Z. Liu, L. He, and A. Klip. 1995. Cellubrevin is a resident protein of insulin-sensitive GLUT4 glucose transporter vesicles in 3T3-L1 adipocytes. J. Biol. Chem. 270:8233.
44. Bonifacino, J. S., P. Perez, R. D. Klausner, and I. V. Sandoval. 1986. Study of the transit of an integral membrane protein from secretory granules through the plasma membrane of secreting rat basophilic leukemia cells using a specific monoclonal antibody. J. Cell Biol. 105:516.
45. Mizoguchi, A., S. Kim, T. Ueda, and Y. Takai. 1989. Tissue distribution of smg p25A, a ras p21-like GTP-binding protein, studied by use of a specific monoclonal antibody. Biochem. Biophys. Res. Commun. 162:1438.
46. Schägger, H., and G. Von Jagow. 1987. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368.
47. Beckers, C. J. M., M. R. Block, B. S. Glick, J. E. Rothman, and W. E. Balch. 1989. Vesicular transport between the endoplasmic reticulum and the Golgi stack requires the NEM-sensitive fusion protein. Nature 339:397.
48. 2+-activated exocytosis. J. Biol. Chem. 271:20223.
49. Niemann, H., J. Blasi, and R. Jahn. 1994. Clostridial neurotoxins: new tools for dissecting exocytosis. Trends Cell Biol. 4:179.
50. Arora, N., L. C. Williamson, S. H. Leppla, and J. L. Halpern. 1994. Cytotoxic effects of a chimeric protein consisting of tetanus toxin light chain and anthrax toxin lethal factor in non-neuronal cells. J. Biol. Chem. 269:26165.
51. Bonifacino, J. S., L. Yuan, and I. V. Sandoval. 1989. Internalization and recycling to serotonin-conlaining granules of the 80K integral membrane protein exposed on the surface of secreting rat basophilic leukemia cells. J. Cell Sci. 92:701.
52. Hamawy, M. M., C. Oliver, S. E. Mergenhagen, and R. P. Siraganian. 1992. Adherence of rat basophilic leukemia (RBL-2H3) cells to fibronectin-coated surfaces enhances secretion. J. Immunol. 149:615.
53. Olson, A. L., J. B. Knight, and J. E. Pessin. 1997. Syntaxin 4, VAMP2, and/or VAMP3/cellubrevin are functional target membrane and vesicle SNAP receptors for insulin-stimulated GLUT4 translocation in adipocytes. Mol. Cell. Biol. 17: 2425.
54. Dascher, C., and W. E. Balch. 1996. Mammalian Sly1 regulates syntaxin 5 function in endoplasmic reticulum to Golgi transport. J. Biol. Chem. 271:15866.
55. Bittner, M. A., M. K. Bennett, and R. W. Holz. 1996. Evidence that syntaxin 1A is involved in storage in the secretory pathway. J. Biol. Chem. 271:11214.
56. Schimmöller, F., I. Simon, and S. R. Pfeffer. 1998. Rab GTPases, directors of vesicle docking. J. Biol. Chem. 273:22161.
57. Pfeffer, S. R. 1999. Transport vesicle targeting: tethers before SNAREs. Nat. Cell Biol. 1:E17.
58. Tuvim, M. J., R. Adachi, J. F. Chocano, R. H. Moore, R. M. Lampert, E. Zera, E. Romero, B. J. Knoll, and B. F. Dickey. 1999. Rab3d, a small GTPase, is localized on mast cell secretory granules and translocates to the plasma membrane upon exocytosis. Am. J. Respir. Cell Mol. Biol. 20:79.
59. Xu, T., T. Binz, H. Niemann, and E. Neher. 1998. Multiple kinetic components of exocytosis distinguished by neurotoxin sensitivity. Nat. Neurosci. 1:192.
60. McBride, H. M., V. Rybin, C. Murphy, A. Giner, R. Teasdale, and M. Zerial. 1999. Oligomeric complexes link Rab5 effectors with NSF and drive membrane fusion via interactions between EEA1 and syntaxin 13. Cell 98:377.
61. Röhlich, P., P. Anderson, and B. Uvnäs. 1971. Electron microscope observations on compound 48/80-induced degranulation in rat mast cells. J. Cell Biol. 51:465.
62. Alvarez de Toledo, G., and J. M. Fernandez. 1990. Compound versus multigranular exocytosis in peritoneal mast cells. J. Gen. Physiol. 95:397.