A mutant impaired in SNARE complex dissociation identifies the plasma membrane as first target of synaptobrevin 2

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Volumn 5, Issue 5, 2004, Pages 371-382

  Martinez Arca, Sonia ^a,c   Arold, Stefan ^b   Rudge, Rachel ^a   Laroche, Fabrice ^a   Galli, Thierry ^a  

^a INSTITUT DU FER À MOULIN   (France)

^b UNIV MONTPELLIER   (France)

^c HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

Author keywords

Membrane fusion; Neurons; SNARE; Synaptobrevin; Target membrane

Indexed keywords

ARGININE; DYNAMIN; MUTANT PROTEIN; PROLINE; SNARE PROTEIN; SYNAPTOBREVIN;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL SURFACE; COMPLEX FORMATION; CONTROLLED STUDY; DENDRITIC CELL; DISSOCIATION; GENE MUTATION; GENETIC CONSERVATION; HUMAN; HUMAN CELL; INTERNALIZATION; NERVE CELL MEMBRANE; NERVE FIBER MEMBRANE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TARGETING; RAT;

ANIMALS; ARGININE; AXONS; CELL MEMBRANE; CELLS, CULTURED; DENDRITES; HEAT; HELA CELLS; HIPPOCAMPUS; HUMANS; IONS; KINETICS; MEMBRANE PROTEINS; MICE; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; MUTATION; PROLINE; PROTEIN BINDING; R-SNARE PROTEINS; RABBITS; RATS; SNARE PROTEINS; THERMODYNAMICS; VESICULAR TRANSPORT PROTEINS;

EID: 2442710275     PISSN: 13989219     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1398-9219.2004.00180.x     Document Type: Article

References (46)

1. Jahn R, Sudhof TC. Membrane fusion and exocytosis. Annu Rev Biochem 1999;68:863-911.
2. Galli T, Haucke V. Cycling of synaptic vesicles: how far? How fast! Sci STKE 2001 2001;88:RE1.
3. Sutton RB, Fasshauer D, Jahn R, Brunger AT. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 angstrom resolution. Nature 1998;395:347-353.
4. Antonin w, Fasshauer D, Becker S, Jahn R, Schneider TR. Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs. Nature Struct Biol 2002;9:107-111.
5. Fasshauer D, Sutton RB, Brunger AT, Jahn R. Conserved structural features of the synaptic fusion complex. SNARE proteins reclassified as Q- and R-SNAREs. Proc Natl Acad Sci U S A 1998;95:15781-15786.
6. Katz L, Brennwald P. Testing the 3Q: 1R "rule": Mutational analysis of the ionic "zero" layer in the yeast exocytic SNARE complex reveals no requirement for arginine. Mol Biol Cell 2000; 11:3849-3858.
7. Ossig R, Schmitt HD, deGroot B, Riedel D, Keranen S, Ronne H. Exocytosis requires asymmetry in the central layer of the SNARE complex. EMBO J 2000;19:6000-6010.
8. Scales SJ, Yoo BY, Scheller RH. The ionic layer is required for efficient dissociation of the SNARE complex by alpha-SNAP and NSF. Proc Natl Acad Sci U S A 2001;98:14262-14267.
9. Ernst JA, Brunger AT. High resolution structure, stability, and synaptotagmin binding of a truncated neuronal SNARE complex. J Biol Chem 2003;278:8630-8636.
10. 2+ and drives membrane fusion. Cell 1999;97:165-174.
11. Graham ME, Washbourne P, Wilson MC, Burgoyne RD. SNAP-25 with mutations in the zero layer supports normal membrane fusion kinetics. J Cell Sci 2001;114:4397-4405.
12. Martinez-Arca S, Proux-Gillardeaux V, Alberts P, Louvard D, Galli T. Ectopic expression of syntaxin 1 in the ER redirects TI-VAMP- and cellubrevin-containing vesicles. J Cell Sci 2003;116:2805-2816.
13. Söllner T, Bennett MK, Whiteheart SW, Scheller RH, Rothman JE. A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 1993;75:409-418.
14. Antonin W, Dulubova I, Arac D, Pabst S, Plitzner J, Rizo J, Jahn R. The N-terminal domains of syntaxin 7 and vti 1b form three-helix bundles that differ in their ability to regulate SNARE complex assembly. J Biol Chem 2002;11:11.
15. Yang B, Gonzalez L Jr, Prekeris R, Steegmaier M, Advani RJ, Scheller RH. SNARE interactions are not selective. Implications for membrane fusion specificity. J Biol Chem 1999;274:5649-5653.
16. Fasshauer D, Antonin W, Margittai M, Pabst S, Jahn R. Mixed and non-cognate SNARE complexes. Characterization of assembly and biophysical properties. J Biol Chem 1999;274:15440-15446.
17. Scales SJ, Chen YA, Yoo BY, Patel SM, Doung YC, Scheller RH. SNAREs contribute to the specificity of membrane fusion. Neuron 2000;26:457-464.
18. Knepper MA, Inoue T. Regulation of aquaporin-2 water channel trafficking by vasopressin. Curr Opin Cell Biol 1997;9:560-564.
19. Paumet F, Le Mao J, Martin S, Galli T, David B, Blank U, Roa M. 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. J Immunol 2000;164:5850-5857.
20. Muzerelle A, Alberts P, Martinez-Arca S, Jeannequin O, Lafaye P, Mazie J-C, Galli T, Gaspar P. Tetanus neurotoxin-insensitive vesicle-associated membrane protein localizes to a presynaptic membrane compartment in selected terminal subsets of the rat brain. Neuroscience 2003;122:59-75.
21. Chamberlain LH, Gould GW. The vesicle- and target-SNARE proteins that mediate Glut4 vesicle fusion are localized in detergent-insoluble lipid rafts present on distinct intracellular membranes. J Biol Chem 2002;277(51):49750-49754.
22. Martinez-Arca S, Rudge R, Vacca M, Raposo G, Camonis J, Proux-Gillardeaux V, Daviet L, Formstecher E, Hamburger A, Filippini F, D'Esposito M, Galli T. A dual mechanism controlling the localization and function of exocytic v-SNAREs. Proc Natl Acad Sci USA 2003;100(15):9011-9016.
23. Mollinedo F, Martin Martin B, Calafat J, Nabokina SM, Lazo PA. Role of vesicle-associated membrane protein-2, through Q-soluble N-ethyl-maleimide-sensitive factor attachment protein receptor/R-soluble N-ethylmaleimide-sensitive factor attachment protein receptor interaction, in the exocytosis of specific and tertiary granules of human neutrophils. J Immunol 2003;170(2):1034-1042.
24. 2+-activated exocytosis. J Biol Chem 1996; 271:20223-20226.
25. Galli T, Zahraoui A, Vaidyanathan W, Raposo G, Tian JM, Karin M, Niemann H, Louvard D. A novel tetanus neurotoxin-insensitive vesicle-associated membrane protein in SNARE complexes of the apical plasma membrane of epithelial cells. Mol Biol Cell 1998;9:1437-1448.
26. Davanger S, Bock JB, Klumperman J, Scheller RH. Syntaxin 6 functions in trans-Golgi network vesicle trafficking. Mol Biol Cell 1997;8:1261-1271.
27. Rice LM, Brunger AT. Crystal structure of the vesicular transport protein Sec17: Implications for SNAP function in SNARE complex disassembly. Mol Cell 1999;4:85-95.
28. Marz KE, Lauer JM, Hanson PI. Defining the SNARE complex binding surface of alpha-SNAP. Implications for SNARE complex disassembly. J Biol Chem 2003;278:27000-27008.
29. Pennuto M, Dunlap D, Contestabile A, Benfenati F, Valtorta F. Fluorescence resonance energy transfer detection of synaptophysin l and vesicle-associated membrane protein 2 interactions during exocytosis from single live synapses. Mol Biol Cell 2002;13: 2706-2717.
30. Edelmann L, Hanson PI, Chapman ER, Jahn R. Synaptobrevin binding to synaptophysin: a potential mechanism for controlling the exocytotic fusion machine. EMBO J 1995;14:224-231.
31. Washbourne P, Schiavo G, Montecucco C. Vesicle-associated membrane protein-2 (synaptobrevin-2) forms a complex with synaptophysin. Biochem J 1995;305:721-724.
32. Galli T, McPherson PS, De Camilli P. The V0 sector of the V-ATPase, synaptobrevin and synaptophysin are associated on synaptic vesicles in a triton X-100 resistant, freeze-thawing sensitive complex. J Biol Chem 1996;271:2193-2199.
33. Damke H, Baba T, Warnock DE, Schmid SL. Induction of mutant dynamin specifically blocks endocytic coated vesicle formation. J Cell Biol 1994;127:915-934.
34. Sampo B, Kaech S, Kunz S, Banker G. Two distinct mechanisms target membrane proteins to the axonal surface. Neuron 2003;37:611-624.
35. Lang T, Bruns D, Wenzel D, Riedel D, Holroyd P, Thiele C, Jahn R. SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J 2001;20: 2202-2213.
36. Winckler B, Mellman I. Neuronal polarity: controlling the sorting and diffusion of membrane components. Neuron 1999;23:637-640.
37. Winckler B, Forscher P, Mellman I. A diffusion barrier maintains distribution of membrane proteins in polarized neurons. Nature 1999; 397:698-701.
38. Regnier-Vigouroux A, Tooze SA, Huttner WB. Newly synthesized synaptophysin is transported to synaptic-like microvesicles via constitutive secretory vesicles and the plasma membrane. EMBO J 1991;10: 3589-3601.
39. Pennuto M, Bonanomi D, Benfenati F, Valtorta F. Synaptophysin I controls the targeting of VAMP2/synaptobrevin II to synaptic vesicles. Mol Biol Cell 2003;E03-06-0380.
40. Galli T, Garcia EP, Mundigl O, Chilcote TJ, DeCamilli P. v- and t-SNAREs in neuronal exocytosis: a need for additional components to define sites of release. Neuropharmacology 1995;34:1351-1360.
41. Martinez-Arca S, Coco S, Mainguy G, Schenk U, Alberts P, Bouille P, et al. A common exocytotic mechanism mediates axonal and dendritic outgrowth. J Neurosci 2001;21:3830-3838.
42. Martinez-Arca S, Alberts P, Zahraoui A, Louvard D, Galli T. Role of tetanus neurotoxin insensitive vesicle-associated membrane protein (TI-VAMP) in vesicular transport mediating neurite outgrowth. J Cell Biol 2000;149:889-899.
43. Chang S, De Camilli P. Glutamate regulates actin-based motility in axonal filopodia. Nat Neurosci 2001;4:787-793.
44. Coco S, Raposo G, Martinez S, Fontaine JJ, Takamori S, Zahraoui A, Jahn R, Matteoli M, Louvard D, Galli T. Subcellular localization of tetanus neurotoxin-insensitive vesicle-associated membrane protein (VAMP)/VAMP7 in neuronal cells: Evidence for a novel membrane compartment. J Neurosci 1999;19:9803-9812.
45. Peitsch MC. ProMod and Swiss-Model: Internet-based tools for automated comparative protein modelling. Biochem Soc Trans 1996;24: 274-279.
46. Jones TA, Zou JY, Cowan SW, Kjeldgaard M. Improved methods for building protein models in electron density maps and trhe location of errors in these models. Acta Crystallogr 1991;A 47: 110-119.