Résumés
Résumé
Les cellules eucaryotes possèdent un réseau complexe de membranes intracellulaires. Les différents compartiments (réticulum endoplasmique, appareil de Golgi, endosomes, lysosomes, membrane plasmique) communiquent entre eux grâce à des vésicules qui bourgeonnent d’un compartiment donneur et fusionnent avec un compartiment accepteur. Au cours de ces transports vectoriels qui définissent le trafic membranaire, les protéines SNARE ont un rôle clé. Dans cet article, nous évoquerons les protéines qui interviennent dans les différentes étapes de la fusion membranaire: l’arrimage des vésicules à la membrane cible, l’amorçage de la réaction, la fusion membranaire elle-même et, enfin, le recyclage des protéines SNARE.
Summary
Eukaryotic cells have a complex network of intracellular membranes. The different compartments (endoplasmic reticulum, Golgi apparatus, endosomes, lysosomes, plasma membrane) are connected by vesicles that bud from a donor compartment and fuse with an acceptor compartment thus defining membrane trafficking as a dynamic phenomenon. Membrane fusion depends on the SNARE family of proteins, the function of which can be recapitulated in vitro. In addition, a large number of proteins, that is discussed in the present paper, control the tethering of the membranes, the priming of the reaction, the regulation of fusion itself and the recycling of SNARE proteins.
Parties annexes
Références
- 1. Galli T, Haucke V. Cycling of synaptic vesicles: how far? How fast! Sci STKE 2001; 88: RE1.
- 2. Söllner T, Whiteheart SW, Brunner M, et al. SNAP receptors implicated in vesicle targeting and fusion. Nature 1993; 362: 318-24.
- 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: 347-53.
- 4. Hayashi T, McMahon H, Yamasaki S, et al. Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly. EMBO J 1994; 13: 5051-61.
- 5. Antonin W, Fasshauer D, Becker S, Jahn R, Schneider TR. Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs. Nat Struct Biol 2002; 9: 107-11.
- 6. Jahn R, Sudhof TC. Membrane fusion and exocytosis. Annu Rev Biochem 1999; 68: 863-911.
- 7. Niemann H, Blasi J, Jahn R. Clostridial neurotoxins: new tools for dissecting exocytosis. Trends Cell Biol 1994; 4: 179-85.
- 8. Montecucco C, Schiavo G. Mechanism of action of tetanus and botulinum neurotoxins. Mol Microbiol 1994; 13 : 1-8.
- 9. Galli T, Chilcote T, Mundigl O, Binz T, Niemann H, De Camilli P. Tetanus toxin-mediated cleavage of cellubrevin impairs exocytosis of transferrin receptor-containing vesicles in CHO cells. J Cell Biol 1994; 125: 1015-24.
- 10. Leung SM, Chen D, DasGupta BR, Whiteheart SW, Apodaca G. SNAP-23 requirement for transferrin recycling in streptolysin-O-permeabilized Madin-Darby canine kidney cells. J Biol Chem 1998; 273: 17732-41.
- 11. Ferro-Novick S, Jahn R. Vesicle fusion from yeast to man. Nature 1994; 370: 191-3.
- 12. Littleton JT. A genomic analysis of membrane trafficking and neurotransmitter release in Drosophila. J Cell Biol 2000; 150: F77-82.
- 13. Schoch S, Deak F, Konigstorfer A, et al. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 2001; 294: 1117-22.
- 14. Washbourne P, Thompson PM, Carta M, et al. Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat Neurosci 2002; 5 : 19-26.
- 15. Martinez-Arca S, Coco S, Mainguy G, et al. A common exocytotic mechanism mediates axonal and dendritic outgrowth. J Neurosci 2001; 21: 3830-8.
- 16. Bock JB, Matern HT, Peden AA, Scheller RH. A genomic perspective on membrane compartment organization. Nature 2001; 409: 839-41.
- 17. Weber T, Zemelman BV, McNew JA, et al. SNAREpins: minimal machinery for membrane fusion. Cell 1998; 92: 759-72.
- 18. McNew JA, Parlati F, Fukuda R, et al. Compartmental specificity of cellular membrane fusion encoded in SNARE proteins. Nature 2000; 407: 153-9.
- 19. Nickel W, Weber T, McNew JA, Parlati F, Sollner TH, Rothman JE. Content mixing and membrane integrity during membrane fusion driven by pairing of isolated v-SNAREs and t-SNAREs. Proc Natl Acad Sci USA 1999; 96: 12571-6.
- 20. Peters C, Bayer MJ, Buhler S, Andersen JS, Mann M, Mayer A. Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion. Nature 2001; 409: 581-8.
- 21. Israel M, Morel N. Mediatophore: a nerve terminal membrane protein supporting the final step of the acetylcholine release process. Prog Brain Res 1990; 84: 101-10.
- 22. 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: 2193-9.
- 23. Finger FP, Novick P. Spatial regulation of exocytosis: lessons from yeast. J Cell Biol 1998; 142: 609-12.
- 24. Moskalenko S, Henry DO, Rosse C, Mirey G, Camonis JH, White MA. The exocyst is a Ral effector complex. Nat Cell Biol 2002; 4: 66-72.
- 25. Brymora A, Valova VA, Larsen MR, Roufogalis BD, Robinson PJ. The brain exocyst complex interacts with RalA in a GTP-dependent manner: identification of a novel mammalian Sec3 gene and a second Sec15 gene. J Biol Chem 2001; 276: 29792-7.
- 26. Hsu SC, Ting AE, Hazuka CD, et al. The mammalian brain rsec6/8 complex. Neuron 1996; 17: 1209-19.
- 27. Hazuka CD, Foletti DL, Hsu SC, Kee Y, Hopf FW, Scheller RH. The sec6/8 complex is located at neurite outgrowth and axonal synapse-assembly domains. J Neurosci 1999; 19: 1324-34.
- 28. Grindstaff KK, Yeaman C, Anandasabapathy N, et al. Sec6/8 complex is recruited to cell-cell contacts and specifies transport vesicle delivery to the basal-lateral membrane in epithelial cells. Cell 1998; 93: 731-40.
- 29. Whyte JR, Munro S. The Sec34/35 Golgi transport complex is related to the exocyst, defining a family of complexes involved in multiple steps of membrane traffic. Dev Cell 2001; 1: 527-37.
- 30. Sacher M, Barrowman J, Wang W, et al. TRAPP I implicated in the specificity of tethering in ER- to-Golgi transport. Mol Cell 2001; 7: 433-42.
- 31. Christoforidis S, McBride HM, Burgoyne RD, Zerial M. The Rab5 effector EEA1 is a core component of endosome docking. Nature 1999; 397: 621-5.
- 32. Seemann J, Jokitalo EJ, Warren G. The role of the tethering proteins p115 and GM130 in transport through the Golgi apparatus in vivo.Mol Biol Cell 2000; 11: 635-45.
- 33. Misura KMS, Scheller RH, Weis WI. Three-dimensional structure of the neuronal-Sec1-syntaxin 1a complex. Nature 2000; 404: 355-62.
- 34. Verhage M, Maia AS, Plomp JJ, et al. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 2000; 287: 864-9.
- 35. Ashery U, Varoqueaux F, Voets T, et al. Munc13-1 acts as a priming factor for large dense-core vesicles in bovine chromaffin cells. Embo J 2000; 19: 3586-96.
- 36. Schoch S, Castillo PE, Jo T, et al. RIM1alpha forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature 2002; 415: 321-6.
- 37. Davis AF, Bai JH, Fasshauer D, Wolowick MJ, Lewis JL, Chapman ER. Kinetics of synaptotagmin responses to Ca2+ and assembly with the core SNARE complex onto membranes. Neuron 1999; 24: 363-76.
- 38. Charvin N, Leveque C, Walker D, et al. Direct interaction of the calcium sensor protein synaptotagmin I with a cytoplasmic domain of the alpha (1) A subunit of the P/Q-type calcium channel. EMBO J 1997; 16: 4591-6.
- 39. Schivell AE, Batchelor RH, Bajjalieh SM. Isoform-specific, calcium-regulated interaction of the synaptic vesicle proteins SV2 and synaptotagmin. J Biol Chem 1996; 271: 27770-5.
- 40. Fernandez-Chacon R, Konigstorfer A, Gerber SH, et al. Synaptotagmin I functions as a calcium regulator of release probability. Nature 2001; 410: 41-9.
- 41. Wang CT, Grishanin R, Earles CA, et al. Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense-core vesicles. Science 2001; 294: 1111-5.
- 42. Mayer A, Wickner W, Haas A. Sec18p (NSF)-driven release of sec17p (alpha-SNAP) can precede docking and fusion of yeast vacuoles. Cell 1996; 85: 83-94.
- 43. Littleton JT, Barnard RJO, Titus SA, Slind J, Chapman ER, Ganetzky B. Snare-complex disassembly by nsf follows synaptic-vesicle fusion. Proc Nat Acad Sci USA 2001; 98: 12233-8.
- 44. Sankaranarayanan S, Ryan TA. Calcium accelerates endocytosis of vSNAREs at hippocampal synapses. Nat Neurosci 2001; 4: 129-36.