The protein machinery of vesicle budding and fusion

Protein Science

Volumn 5, Issue 2, 1996, Pages 185-194

  Rothman, James E ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

budding and fusion mechanisms; endoplasmic reticulum; Golgi stack; soluble NSF attachment proteins, NSF protein, ARF proteins, coat proteins, SNARE proteins

Indexed keywords

ADENOSINE TRIPHOSPHATASE; COAT PROTEIN; HYBRID PROTEIN;

CELL VACUOLE; ENDOPLASMIC RETICULUM; INTRACELLULAR TRANSPORT; MEMBRANE FUSION; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW;

EID: 0030020733     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1002/pro.5560050201     Document Type: Review

References (92)

1. Aalto MK, Ronne H, Keranen S. 1992. Yeast syntaxins Ssolp and Sso2p belong to a family of related membrane proteins that function in vesicular transport. EMBO J 12:4095-4104.
2. Acharya U, Jacobs R, Peters JM, Watson N, Farquhar MG, Malhotra V. 1995. The formation of Golgi stacks from vesiculated Golgi membranes requires two distinct fusion events. Cell 82:895-904.
3. Ahle S, Mann A, Eichelsbacher U, Ungewickell E. 1988. Structural relationship between clathrin assembly proteins from the Golgi and plasma membrane. EMBO J 7:919-929.
4. Balch WE, Dunphy WG, Braell WA, Rothman JE. 1984a. Reconstitution of the transport of protein between successive compartments of the Golgi measured by the coupled incorporation of N-acetylglucosamine. Cell 3:405-416.
5. Balch WE, Glick BS, Rothman JE. 1984b. Sequential intermediates in the pathway of intercompartmental transport in a cell-free system. Cell 39: 525-536.
6. Barlowe C, Orci L, Yeung T, Hosobuchi M, Hamamoto S. 1994. COPII: A membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77:895-907.
7. Baumert M, Maycox PR, Navone F, De Camilli P, Jahn R. 1989. Synaptobrevin: An integral membrane protein of 18,000 daltons present in small synaptic vesicles of rat brain. EMBO 8:379-384.
8. Bennett MK, Calakos N, Scheller RH. 1992. Syntaxin: A synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257:255-259.
9. Bennett MK, Scheller RH. 1993. The molecular machinery for secretion is conserved from yeast to neurons. Proc Natl Acad Sci USA 90:2559-2563.
10. Bennett MK, Scheller RH. 1994. Molecular description of synaptic vesicle trafficking. Annu Rev Biochem 63:63-100.
11. Bittner MA, Holz RW. 1992. A temperature-sensitive step in exocytosis. J Biol Chem 267:16619-16626.
12. Block MR, Glick BS, Wilcox CA, Wieland FT, Rothman JE. 1988. Purification of an N-ethylmaleimide-sensitive protein catalyzing vesicular transport. Proc Natl Acad Sci USA 85:7852-7856.
13. Braell WA, Balch WE, Dobbenin DC, Rothman JE. 1984. The glycoprotein that is transported between successive compartments of the Golgi in a cell-free system resides in stacks of cisternae. Cell 39:511-524.
14. Calakos N, Bennett MK, Peterson KE, Scheller RH. 1994. Protein-protein interactions contributing to the specificity of intracellular vesicular trafficking. Science 263:1146-1149.
15. Clary DO, Griff IC, Rothman JE. 1990, SNAPs, a family of NSF attachment proteins involved in intracellular membrane fusion in animals and yeast. Ceil 61:709-721.
16. Clary DO, Rothman JE. 1990. Purification of three related peripheral membrane proteins needed for vesicular transport. J Biol Chem 265:10109-10117.
17. DeBello WM, O'Connor V, Dresbach T, Whiteheart SW, Wang SS, Schweizer FE, Betz H, Rothman JE, Augustine GJ. 1995 SNAP-mediated protein-protein interactions essential for neurotransmitter release. Nature 373: 626-630.
18. DeBello WM, Betz H, Augustine GJ. 1993. Synaptotagmin and neurotransmitter release. Cell 74:947-950.
19. Donaldson JG, Cassel D, Kahn RA, Klausner RD. 1992a. ADP-ribosylation factor, a small GTP-binding protein, is required for binding of the coatomer protein beta-COP to Golgi membranes. Proc Natl Acad Sci USA 89:6408-6412.
20. Donaldson JG, Finazzi D, Klausner RD. 1992b Brefeldin A inhibits Golgi membrane-catalyzed exchange of guanine nucleotide onto ARF protein. Nature 360:350-352.
21. Dunphy WG, Fries E, Urbani LJ, Rothman JE. 1981. Early and late functions associated with the Golgi apparatus reside in distinct compartments. Proc Natl Acad Sci USA 78:7453-7457.
22. Elfrink LA, Peterson MR, Scheller RH. 1993. A role for synaptotagmin (p65) in regulated exocytosis. Cell 72:153-159.
23. Fries E, Rothman JE. 1980. Transport of vesicular stomatitis virus glycoprotein in a cell-free extract. Proc Natl Acad Sci USA 77:3870-3874.
24. 2+ sensor for transmitter release at a central synapse. Cell 79:717-727.
25. Glick BS, Rothman JE. 1987. Possible role for fatty acyl-coenzyme A in intracellular protein transport. Nature 326:309-312.
26. Goldstein JL, Anderson RGW, Brown MS. 1979. Coated pits, coated vesicles, and receptor-mediated endocytosis. Nature 279:679-685.
27. Hardwick KG, Pelham HRB. 1992. SED5 encodes a 39 kD integral membrane protein required for vesicular transport between the ER and the Golgi complex. J Cell Biol 119:513-521.
28. Hay JC, Martin TFJ. 1992. Resolution of regulated secretion into sequential MgATP-dependent and calcium-dependent stages mediated by distinct cytosolic proteins. J Cell Biol 119:139-151.
29. Helms JB, Palmer DJ, Rothman JE. 1993. Two distinct populations of ARF bound to Golgi membranes. J Cell Biol 121:751-760.
30. Helms JB, Rothman JE. 1992. Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF. Nature 360:352-354.
31. Hess DT, Slater TM, Wilson MC, Skene JHP. 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.
32. Hugueney P, Bouvier F, Bdillo A, d'Harlingue A, Kuntz M, Camara B. 1995. Identification of a plastid protein involved in vesicle fusion and/or membrane protein translocation. Proc Natl Acad Sci USA 92:5630-5634.
33. Huttner WB. 1993. Snappy exocytoxins. Nature 365:104-105.
34. Ikonen E, Tagaya M, Ulrich O, Montecucco C, Simons K. 1995. Different requirements for NSF, SNAP, and Rab proteins in apical and basolateral transport in MDCK cells. Cell 81:571-580.
35. Kahn RA, Gilman AG. 1986. The protein cofactor necessary for ADP-ribosylation of Gs by cholera toxin is itself a GTP binding protein. J Biol Chem 261:7906-7911.
36. Kahn RA, Goddard C, Newkirk. 1988. Chemical and immunological characterization of the 21-kDa ADP-ribosylation factor of adenylate cyclase. J Biol Chem 263:8282-8287.
37. Kahn RA, Kern FG, Clark J, Gelmann EP, Rulka C. 1991. Human ADP-ribosylation factors: A functionally conserved family of GTP-binding proteins. J Biol Chem 266:2606-2614.
38. Latterich M, Frohlich KU, Schekman R. 1995. Membrane fusion and the cell cycle: Cdc48p participates in the fusion of ER membranes. Cell 82:885-893.
39. Lian JP, Ferro-Novick S. 1993. Boslp, an integral membrane protein of the endoplasmic reticulum to Golgi transport vesicles, is required for their fusion competence. Cell 73:735-745.
40. Malhotra V, Orci L, Glick BS, Block MR, Rothman JE. 1988. Role of an N-ethylmaleimide-sensitive transport component in promoting fusion of transport vesicles with cisternae of the Golgi stack. Cell 54:221-227.
41. Malhotra V, Serafini T, Orci L, Shepherd JC, Rothman JE. 1989. Purification of a novel class of coated vesicles mediating biosynthetic protein transport through the Golgi stack. Cell 55:329-336.
42. McMahon HT, Ushkaryov YA, Edelmann L, Link E, Benz T, Niemann H, Jahn R, Südhof TC. 1993. Cellubrevin is a ubiquitous tetanus-toxin substrate homologous to a putative synaptic vesicle fusion protein. Nature 364:346-349.
43. Melançon P, Glick BS, Malhotra V, Weidman PJ, Serafini T, Gleason ML, Orci L, Rothman JE. 1987. Involvement of GTP-binding "G" proteins in transport through the Golgi stack. Cell 51:1053-1062.
44. Nakano A, Muramatsu M. 1989. A novel GTP-binding protein, Sar1p, is involved in transport from the endoplasmic reticulum to the Golgi apparatus. J Cell Biol 107:851-863.
45. Novick P, Ferro S, Schekman R. 1981. Order of events in the yeast secretory pathway. Cell 25:461-469.
46. Novick P, Field C, Schekman R. 1980. Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell 21:205-215.
47. Orci L, Glick BS, Rothman JE. 1986. A new type of coated vesicular carrier that appears not to contain clathrin: Its possible role in protein transport within the Golgi stack. Cell 46:171-184.
48. Orci L, Malhotra V, Amherdt M, Serafini T, Rothman JE. 1989. Dissection of a single round of vesicular transport: Sequential intermediates for intercisternal movement in the Golgi stack. Cell 56:357-368.
49. Orci L, Palmer DJ, Amherdt M, Rothman JE. 1993a. De novo assembly of coated vesicles from Golgi cisternae requires only coatomer and ARF proteins from the cytosol. Nature 364:732-734.
50. Orci L, Palmer DJ, Ravazzola M, Perrelet A, Amherdt M, Rothman JE. 1993b. Budding from Golgi membranes requires coatomer complex of non-clathrin coat proteins. Nature 362:648-652.
51. Ostermann J, Orci L, Tani K, Amherdt M, Ravazzola M, Rothman JE. 1993. Stepwise assembly of functionally active transport vesicles. Cell 75:1015-1025.
52. Oyler GA, Higgins GA, Hart RA, Battenberg E, Billingsley M, Bloom FE, Wilson MC. 1989. The identification of a novel synaptosomal-associated protein, SNAP-25, differentially expressed by neuronal subpopulations. J Cell Biol 109:3039-3052.
53. Palade G. 1959. Functional changes in the structure of cellcomponents. In: Hayashi T, ed. Subcellularparticles. Ronald Publishers, New York, pp 64-83.
54. Pallanack L, Ordway RW, Ganetzky B. 1995. A Drosophila NSF mutant. Nature 376:25.
55. Palmer DJ, Helms JB, Beckers CJM, Orci L, Rothman JE. 1993. Binding of coatomer to Golgi membranes requires ADP-ribosylation factor. J Biol Chem 268:12083-12089.
56. Pearse BMF. 1976. Clathrin: A unique protein associated with intracellular transfer of membrane by coated vesicles. Proc Natl Acad Sci USA 73:1255-1259.
57. Pearse BMF, Bretscher MS. 1981. Membrane recycling by coated vesicles. Annu Rev Biochem 50:85-101.
58. Pearse BMF, Robinson MS. 1990. Clathrin, adaptors, and sorting. Annu Rev Cell Biol 6:151-171.
59. Peters JM, Walsh MJ, Franke WW. 1990. An abundant and ubiquitous homo-oligomeric ring-shaped ATPase particle related to the putative vesicle fusion proteins Sec18p and NSF. EMBO J 9:1757-1767.
60. Pevsner J, Hsu SC, Braun JEA, Calakos N, Ting AE, Bennett MK, Scheller RH. 1994. Specificity and regulation of a synaptic vesicle docking complex. Neuron 13:353-361.
61. Protopopov V, Govindan B, Novick P, Gerst JE. 1993. Homologs of the synaptobrevin/VAMP family of synaptic vesicle proteins function on the late secretory pathway in S. cerevisiae. Cell 74:855-861.
62. Rabouille C, Levine TP, Peters JM, Warren G. 1995. An NSF-like ATPase, P97, and NSF mediate cisternal regrowth from mitotic Golgi fragments. Cell 82:905-914.
63. Robinson MS. 1992. Adaptins. Trends Cell Biol 2:293-297.
64. Rothman JE. 1992. Reconstitution of intracellular transport. Methods Enzymol Series, Volume 219. Academic Press, New York.
65. Rothman JE, Schmid SL. 1986. Enzymatic recycling of clathrin from coated vesicles. Cell 46:5-9.
66. Rothman JE, Urbani LJ, Brands R. 1984. Transport of protein between cytoplasmic membranes of fused cells: Correspondence to processes reconstituted in a cell-free system. J Cell Biol 99:260-271.
67. Rothman JE, Warren G. 1994. Implications of the SNARE hypothesis for intracellular membrane topology and dynamics. Curr Biol 4:220-233.
68. Salama NR, Yeung T, Schekman R. 1993. The Sec13p complex and reconstitution of vesicle budding from the ER with purified cytosolic proteins. EMBO J 12:4073-4082.
69. Schiavo G, Benfenati F, Poulain B, Rossetto O, Polverino de Laureto P, DasGupta BR, Montecucco C. 1992. Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359:832-835.
70. Schiavo G, Gmachl M, Stenbeck G, Söllner T, Rothman JE. 1995. A possible docking and fusion particle for synaptic transmission. Nature 378:733-136.
71. Serafini T, Orci L, Amherdt M, Brunner M, Kahn RA, Rothman JE. 1991a. ADP-ribosylation factor is a subunit of the coat of Golgi-derived COP-coated vesicles: A novel role for a GTP-binding protein. Cell 67: 239-253.
72. Serafini T, Stenbeck G, Brecht A, Lottspeich F, Orci L, Rothman JE, Wieland FT. 1991b. A coat subunit of Golgi-derived non-clathrin-coated vesicles with homology to the clathrin-coated vesicle coat protein beta-adaptin. Nature 349:215-220.
73. Søgaard M, Tani K, Ye RR, Geromanos S, Tempst P, Sollner T, Rothman JE. 1994. A rab protein is required for the assembly of SNARE complexes in the docking of transport vesicles. Cell 78:937-948.
74. Söllner T, Bennett MK, Whiteheart SW, Scheller RH, Rothman JE. 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.
75. Söllner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, Tempst P, Rothman JE. 1993b. SNAP receptors implicated in vesicle targeting and fusion. Nature 362:318-324.
76. Stamnes MA, Rothman JE. 1993. The binding of AP-1 clathrin adaptor particles to Golgi membranes requires ADP-ribosylation factor, a small GTP-binding protein. Cell 73:999-1005.
77. Südhof T. 1995. The synaptic vesicle cycle: A cascade of protein-protein interactions. Nature 375:645-653.
78. Südhof TC, Jahn R. 1991. Proteins of synaptic vesicles involved in exocytosis and membrane recycling. Neuron 6:665-677.
79. Tagaya M, Wilson DW, Brunner M, Arango N, Rothman JE. 1993. Domain structure of an N-ethylmaleimide-sensitive fusion protein involved in vesicular transport. J Biol Chem 268:2662-2666.
80. Tanigawa G, Orci L, Amherdt M, Helms JB, Rothman JE. 1993. Hydrolysis of bound GTP by ARF protein triggers uncoating of Golgi-derived COP-coated vesicles. J Cell Biol 125:1365-1371.
81. 2+ receptor controls the final steps in peptide secretion from pituitary melanotrophs. Neuron 11:83-104.
82. Traub LM, Ostrom JA, Kornfeld S. 1993. Biochemical dissection of AP-1 recruitment onto Golgi membranes. J Cell Biol 123:561-573.
83. Trimbie WS, Cowan DM, Scheller RH. 1988. VAMP-1: A synaptic vesicle-associated integral membrane protein. Proc Natl Acad Sci USA 85: 4538-4542.
84. WatersMG, Serafini T, Rothman JE. 1991. "Coatomer:" A cytosolic protein complex containing subunits of non-clathrin-coated Golgi transport vesicles. Nature 349:248-251.
85. Weidman PJ, Melançon P, Block MR, Rothman JE. 1989. Binding of an N-ethylmaleimide-sensitive fusion protein to Golgi membranes requires both a soluble protein(s) and an integral membrane receptor. J Cell Biol 108:1589-1596.
86. Whiteheart SW, Brunner M, Wilson DW, Wiedmann M, Rothman JE. 1992. NSF attachment proteins (SNAPs) to a multi-SNAP receptor complex in Golgi membranes. J Biol Chem 267:12239-12243.
87. Whiteheart SW, Griff IC, Brunner M, Clary DO, Mayer T, Buhrow SA, Rothman JE. 1993. SNAP family of NSF attachment proteins includes a brain-specific isoform. Nature 362:353-355.
88. Whitehean SW, Rossnagel K, Buhrow S, Brunner M, Jaenicke R, Rothman JE. 1994. NSF: A trimeric ATPase whose hydrolysis of ATP is required for membrane fusion. J Cell Biol 126:945-954.
89. Wilson DW, Whiteheart SW, Wiedmann M, Brunner M, Rothman JE. 1992. A multisubunit particle implicated in membrane fusion. J Cell Biol 117: 531-538.
90. Wilson DW, Wilcox CA, Flynn CG, Chen E, Kuang WJ, Henzel WJ, Block MR, Ullrich R, Rothman JE. 1989. A fusion protein required for vesiclemediated transport in both mammalian cells and yeast. Nature 339: 355-359.
91. Yoshihisa T, Barlowe C, Schekman R. 1993. Requirement for a GTPase-activating protein in vesicle budding from the endoptasmic reticulum. Science 259:1466-1468.
92. Zhang CJ, Rosenwald AG, Willingham MC, Skuntz S, Clark J, Kahn RA. 1994. Expression of a dominant allele of human ARF1 inhibits membrane traffic in vivo. J Cell Biol 124:289-300.