Asymmetric requirements for a Rab GTPase and SNARE proteins in fusion of COPII vesicles with acceptor membranes

Journal of Cell Biology

Volumn 149, Issue 1, 2000, Pages 55-65

  Cao, Xiaochun ^a   Barlowe, Charles ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Endoplasmic reticulum; Golgi apparatus; Membrane fusion; Secretion; Trafficking

Indexed keywords

GENE PRODUCT; SNARE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FRACTIONATION; CELL VACUOLE; ENDOPLASMIC RETICULUM; EUKARYOTE; MEMBRANE FUSION; PRIORITY JOURNAL; PROTEIN ANALYSIS; YEAST;

ALLELES; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CYTOPLASMIC GRANULES; ENDOPLASMIC RETICULUM; FUNGAL PROTEINS; GENES, FUNGAL; GOLGI APPARATUS; INTRACELLULAR MEMBRANES; MEMBRANE FUSION; MEMBRANE PROTEINS; MUTATION; RAB GTP-BINDING PROTEINS; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SNARE PROTEINS; TEMPERATURE; VESICULAR TRANSPORT PROTEINS;

EUKARYOTA;

EID: 0034599993     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.149.1.55     Document Type: Article

References (90)

1. 2+ -ATPase homologue, PMRI, is required for normal Golgi function and localizes in a novel Golgi-like distribution. Mol. Biol. Cell. 3:633-654.
2. Baker, D., L. Hicke, M. Rexach, M. Schleyer, and R. Schekman. 1988. Reconstitution of SEC gene product-dependent intercompartmental protein transport. Cell. 54:335-344.
3. Banfield, D.K., M.J. Lewis, and H.R. Pelham. 1995. A SNARE-like protein required for traffic through the Golgi complex. Nature. 375:806-809.
4. Bannykh, S.I., T. Rowe, and W.E. Balch. 1996. The organization of endoplasmic reticulum export complexes. J. Cell Biol. 135:19-35.
5. Barlowe, C. 1997. Coupled ER to Golgi transport reconstituted with purified cytosolic proteins. J. Cell Biol. 139:1097-1108.
6. Barlowe, C., L. Orci, T. Yeung, M. Hosobuchi, S. Hamamoto, N. Salama, M.F. Rexach, M. Ravazzola, M. Amherdt, and R. Schekman. 1994. COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell. 77:895-907.
7. Baudin, A., O. Ozier-Kalogeropoulos, A. Denouel, F. Lacroute, and C.A. Cullin. 1993. A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res. 21:3329-3330.
8. Bednarek, S.Y., M. Ravazzola, M. Hosobuchi, M. Amherdt, A. Perrelet, R. Schekman, and L. Orci. 1995. COPI- and COPII-coated vesicles bud directly from the cndoplasmic reticulum in yeast. Cell. 83:1183-1196.
9. Bennett, M.K., N. Calakos, T. Kreiner, and R.H. Sheller. 1992. Synaptic vesicle membrane proteins interact to form a multimeric complex. J. Cell Biol. 116: 761-775.
10. Berninsone, P., Z.Y. Lin, E. Kempner, and C.B. Hirschberg. 1995. Regulation of yeast Golgi glycosylation. J. Biol. Chem. 270:14564-14567.
11. Bonfanti, L., A.A. Mironov Jr., J.A. Martinez-Menarguez, O. Martella, A. Fusella, M. Baldassarre, R. Buccione, H.J. Geuze, A.A. Mironov, and A. Luini. 1998. Procollagen traverses the Golgi stack without leaving the lumen of cisternae: evidence for cisternal maturation. Cell. 95:993-1003.
12. Cao, X., N. Ballew, and C. Barlowe. 1998. Initial docking of ER-derived vesicles requires Usolp and Ypt1p but is independent of SNARE proteins. EMBO (Eur. Mol. Biol. Organ.) J. 17:2156-2165.
13. Chamberlain, L.H., D. Roth, A. Morgan, and R.D. Burgoyne. 1995. Distinct effects of alpha-SNAP, 14-3-3 proteins, and calmodulin on priming and triggering of regulated exocytosis. J. Cell Biol. 130:1063-1070.
14. Conchon, S., X. Cao, C. Barlowe, and H.R. Pelham. 1999. Got1p and Sft2p: membrane proteins involved in traffic to the Golgi. EMBO (Eur. Mol. Biol. Organ.) J. 18:3934-3946.
15. 2+ sensitivity. J. Cell Biol. 143:1845-1857.
16. Dascher, C., R. Ossig, D. Gallwitz, and H.D. Schmitt. 1991. Identification and structure of four yeast genes (SLY) that are able to suppress the functional loss of YPT1, a member of the RAS superfamily. Mol. Cell. Biol. 11:872-885.
17. Dascher, C., J. Matteson, and W. Balch. 1994. Syntaxin 5 regulates endoplasmic reticulum to Golgi transport. J. Biol. Chem. 269:29363-29366.
18. Evan, G.I., G.K. Lewis, G. Ramsay, and J.M. Bishop. 1985. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5:3610-3616.
19. Fischer von Mollard, G.F., S.F. Nothwehr, and T.H. Stevens. 1997. The yeast v-SNARE Vtilp mediates two vesicle transport pathways through interactions with the t-SNAREs Sed5p and Pep12p. J. Cell Biol. 137:1511-1524.
20. Fischer von Mollard, G.F., and T.H. Stevens. 1999. The Saccharomyces cerevisiae v-SNARE Vtilp is required for multiple membrane transport pathways to the vacuole. Mol. Biol. Cell. 10:1719-1732.
21. Garrett, M.D., J.E. Zahner, C.M. Cheney, and P.J. Novick. 1994. GDII encodes a GDP dissociation inhibitor that plays an essential role in the yeast secretory pathway. EMBO (Eur. Mol. Biol. Organ.) J. 13:1718-1728.
22. Gotte, M., and G.F. Fischer von Mollard. 1998. A new heat for the SNARE drum. Trends Cell Biol. 8:215-218.
23. Haas, A., D. Scheglmann, T. Lazar, D. Gallwitz, and W. Wickner. 1995. The GTPase Ypt7p of Saccharomyces cerevisiae is required on both partner vacuoles for the homotypic fusion step of vacuole inheritance. EMBO (Eur. Mol. Biol. Organ.) J. 14:5258-5270.
24. Hardwick, K.G., and H.R. Pelham. 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.
25. Hay, J.C., D.S. Chao, C.S. Kuo, and R.H. Scheller. 1997. Protein interactions regulating vesicle transport between the endoplasmic reticulum and Golgi apparatus in mammalian cells. Cell. 89:149-158.
26. Hay, J.C., J. Klumperman, V. Oorschot, M. Steegmaier, C.S. Kuo, and R.H. Scheller. 1998. Localization, dynamics, and protein interactions reveal distinct roles for ER and Golgi SNAREs. J. Cell Biol. 141:1489-1507.
27. Hicke, L., and R. Schekman. 1989. Yeast See23p acts in the cytoplasm to promote protein transport from the endoplasmic reticulum to the Golgi complex in vivo and in vitro. EMBO (Eur. Mol. Biol. Organ.) J. 8:1677-1684.
28. Kaiser, C.A., and R. Schekman. 1990. Distinct sets of SEC genes govern transport vesicle formation and fusion early in the secretory pathway. Cell. 61: 723-733.
29. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
30. Latterich, M., K.U. Frohlich, and R. Schekman. 1995. Membrane fusion and the cell cycle: Cdc48p participates in the fusion of ER membranes. Cell. 82:885-893.
31. Lewis, M.J., and H.R. Pelham. 1996. SNARE-mediated retrograde traffic from the Golgi complex to the endoplasmic reticulum. Cell. 85:205-215.
32. Lewis, M.J., J.C. Rayner, and H.R.B. Pelham. 1997. A novel SNARE complex implicated in vesicle fusion with the endoplasmic reticulum. EMBO (Eur. Mol. Biol. Organ.) J. 16:3017-3024.
33. Lian, J.P., and S. Ferro-Novick. 1993. Bos1p, an integral membrane protein of the endoplasmic reticulum to Golgi transport vesicles, is required for their fusion competence. Cell. 73:735-745.
34. Lian, J.P., S. Stone, Y. Jiang, P. Lyons, and S. Ferro-Novick. 1994. Ypt1p implicated in v-SNARE activation. Nature. 372:698-701.
35. Lin, C.-C., H.D. Love, J.N. Gushe, J.J.M. Bergeron, and J. Ostermann. 1999. ER/Golgi intermediates acquire Golgi enzymes by brefeldin A-sensitive retrograde transport in vitro. J. Cell Biol. 147:1457-1472.
36. Lin, R.C., and R.H. Scheller. 1997. Structural organization of the synaptic exocytosis core complex. Neuron. 19:1087-1094.
37. Lupashin, V.V., and M.G. Waters. 1997. t-SNARE activation through transient interaction with a Rab-like guanosine triphophatase. Science. 276:1255-1258.
38. Mayer, A., W. Wickner, and A. Haas. 1996. Sec18p (NSF)-driven release of Sec17p (α-SNAP) can precede docking and fusion of yeast vacuoles. Cell. 85:83-94.
39. McNew, J.A., M. Sogaard, N.M. Lampen, S. Machida, R. R. Ye. L. Lacomis, P. Tempst, J.E. Rothman, and T.H. Sollner. 1997. Ykt6p, a prenylated SNARE essential for endoplasmic reticulum-Golgi transport. J. Biol. Chem. 272: 17776-17783.
40. Morin-Ganet, M.-N., A. Rambourg, S.B. Deitz, A. Franzusoff, and F. Kepes. 1999. Morphogenesis and dynamics of the yeast Golgi apparatus. Traffic. 1:56-68.
41. Nagahama, M., L. Orci, M. Ravazzola, M. Amherdt, L. Lacomis, P. Tempst, J.E. Rothman, and T.H. Sollner, 1996. A v-SNARE implicated in intra-Golgi transport. J. Cell Biol. 133:507-516.
42. 3H]mannose suicide selection. J. Cell Biol. 105:1587-1593.
43. Newman, A.P., J. Shim, and S. Ferro-Novick. 1990. BET1. BOS1 and SEC22 are members of a group of interacting yeast genes required for transport from the endoplasmic reticulum to the Golgi complex. Mol. Cell. Biol. 10: 3405-3414.
44. Newman, A.P., M.E. Groesch, and S. Ferro-Novick. 1992. Bos1p, a membrane protein required for ER to Golgi transport in yeast, co-purifies with the carrier vesicles and with Bet1p and the ER membrane. EMBO (Eur. Mol. Biol. Organ.) J. 11:3609-3617.
45. Nichols, B.J., and H.R.B. Pelham. 1998. SNAREs and membrane fusion in the Golgi apparatus. Biochim. Biohys. Acta. 1404:9-31.
46. Nichols, B.J., C. Ungermann, H.R. Pelham, W. Wickner, and A. Haas. 1997. Homotypic vacuolar fusion mediated by t- and v-SNAREs. Nature. 387:199-202.
47. Ossig, R., C. Dascher, H. Trepte, H.D. Schmitt, and D. Gallwitz. 1991. The yeast SLY gene products, suppressors of defects in the essential GTP-binding Ypt1 protein, may act in endoplasmic reticulum-to-Golgi transport. Mol. Cell. Biol. 11:2980-2993.
48. Ossig, R., W. Laufer, H.D. Schmitt, and D. Gallwitz. 1995. Functionality and specific membrane localization of transport GTPases carrying C-terminal membrane anchors of synaptobrevin-like proteins. EMBO (Eur. Mol. Biol. Organ.) J. 14:3645-3653.
49. Patel, S.K., F.E. Indig, N. Olivieri, N.D. Levine, and M. Latterich. 1998. Organelle membrane fusion: a novel function for the syntaxin homolog Ufe1p in ER membrane fusion. Cell. 92:611-620.
50. Pelham, H.R.B. 1998. Getting through the Golgi complex. Trends Cell Biol. 8:45-49.
51. Peng, R., R Grabowski, A. De Antoni, and D. Gallwitz. 1999. Specific interaction of the yeast cis-Golgi syntaxin Sed5p and the coat protein complex II component Sec24p of endoplasmic reticulum-derived transport vesicles. Proc. Natl. Acad. Sci. USA. 96:3751-3756.
52. Poirier, M.A., W. Xiao, J.C. Macosko, C. Chan, Y.-K. Shim, and M.K. Bennett. 1998. The synaptic SNARE complex is a parallel four-stranded helical bundle. Nat. Struct. Biol. 5:765-769.
53. Poon, P.P., D. Cassel, A. Spang, M. Rotman, E. Pick, R.A. Singer, and G.C. Johnston. 1999. Retrograde transport from the yeast Golgi is mediated by two ARF GAP proteins with overlapping function. EMBO (Eur. Mol. Biol. Organ.) J. 18:555-564.
54. Powers, J., and C. Barlowe. 1998. Transport of Ax12p depends on Erv14p, an ER-vesicle protein related to the Drosophila cornichon gene product. J. Cell Biol. 142:1209-1222.
55. Presley, J.F., N.B. Cole, T.A. Schroer, K. Hirschberg, K.J.M. Zaal, and J. Lippincott-Schwartz. 1997. ER to Golgi transport visualised in living cells. Nature. 389:81-85.
56. Preuss, D., J. Mulholland, A. Franzusoff, N. Segev, and D. Botstein. 1992. Characterization of the Saccharomyces Golgi complex through the cell cycle by immunoelectron microscopy. Mol. Biol. Cell. 3:789-803.
57. Rabouille, C., H. Kondo, R. Newman, M. Hui, P. Freemont, and G. Warren. 1998. Syntaxin 5 is a common component of the NSF- and p97-mediated reassembly pathways of Golgi cisternae from mitotic Golgi fragments in vitro. Cell. 92:603-610.
58. Rexach, M.F., and R.W. Schekman. 1991. Distinct biochemical requirements for the budding, targeting, and fusion of ER-derived transport vesicles. J. Cell Biol. 114:219-229.
59. Rexach, M.F., M. Latterich, and R.W. Schekman. 1994. Characteristics of endoplasmic reticulum-derived transport vesicles. J. Cell Biol. 126:1133-1148.
60. Robinson, L.J., and T. Martin. 1998. Docking and fusion in neuronsecretion. Curr. Opin. Cell Biol. 10:483-492.
61. Rothman, J.E., and F.T. Wieland. 1996. Protein sorting by transport vesicles. Science. 272:227-234.
62. Rowe, T., C. Dascher, S. Bannykh, H. Plutner, and W. Balch. 1998. Role of vesicle-associated syntaxin 5 in the assembly of pre-Golgi intermediates. Science. 279:696-700.
63. Sacher, M., S. Stone, and S. Ferro-Novick. 1997. The synaptobrevin-related domains of Bos1p and Sec22p bind to the syntaxin-like region of Sed5p. J. Biol. Chem. 272:17134-17138.
64. Scales, S.J., R. Pepperkok, and T.E. Kreis. 1997. Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COPII and COPI. Cell. 90:1137-1148.
65. Schekman, R., and L. Orci. 1996. Coat proteins and vesicle budding. Science. 271:1526-153.3.
66. Schroder, S., F. Schimmoller, B. Singer-Kruger, and H. Riezman. 1995. The Golgi-localization of yeast Emp47p depends on its di-lysine motif but is not affected by the ret1-1 mutation in alpha-COP. J. Cell Biol. 131:895-912.
67. Shim, J., A.P. Newman, and S. Ferro-Novick. 1991. The BOS1 gene encodes an essential 27-kD putative membrane protein that is required for vesicular transport from the ER to the Golgi complex in yeast. J. Cell Biol. 113:55-64.
68. Sikorski, R., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Sacchromyces cerevisiae. Genetics. 122:19-27.
69. Sogaard, M., K. Tani, R.R. Ye, S. Geromanos, P. Tempst, T. Kirchhausen, J.E. Rothman, and T. Sollner. 1994. A rab protein is required for the assembly of SNARE complexes in the docking of transport vesicles. Cell. 78:927-948.
70. Sollner, T., M.K. Bennett, S.W. Whiteheart, R.H. Scheller, and J.E. Rothman. 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.
71. Sollner, T., S.W. Whiteheart, M. Brunner, H. Erdjument-Bromage, S. Geromanos, P. Tempst, and J.E. Rothman. 1993b. SNAP receptors implicated in vesicle targeting and fusion. Nature. 362:318-324.
72. Spang, A., and R. Schekman. 1998. Reconstitution of retrograde transport from the Golgi to the ER in vitro. J. Cell Biol. 143:589-599.
73. Springer, S., and R. Schekman. 1998. Nucleation of COPII vesicular coat complex by endoplasmic reticulum to Golgi vesicle SNAREs. Science. 281:698-700.
74. Stirling, C.J., J. Rothblatt, M. Hosobuchi, R. Deshaies, and R. Schekman. 1992. Protein translocation mutants defective in the insertion of integral membrane proteins into the endoplasmic reticulum. Mol. Biol. Cell. 3:129-142.
75. Stone, S., M. Sacher, Y. Mao, C. Carr, P. Lyons, A.M. Ouinn, and S. Ferro-Novick. 1997. Bet1p activates the v-SNARE Bos1p. Mol. Biol. Cell. 8:1175-1181.
76. Subramaniam, V.N., F. Peter, R. Philp, S.H. Wong, and W. Hong, 1996. GS28, a 28-kilodalton Golgi SNARE that participates in ER-Golgi transport. Science. 272:1161-1163.
77. Sutton, R.B., D. Fasshauer, R. Jahn, and A.T. Brünger. 1998. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution. Nature. 395:347-353.
78. Towhin, H., T. Straelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA. 76:4350-4354.
79. Ungermann, C., K. Sato, and W. Wickner. 1998. Defining the functions of trans-SNARE pairs. Nature. 396:543-548.
80. Ungermann, C., G.F. von Mollard, O.N. Jensen, N. Margolis, T.H. Stevens, and W. Wickner. 1999. Three v-SNAREs and two t-SNAREs, present in a pentameric cis-SNARE complex on isolated vacuoles, are essential for homotypic fusion. J. Cell Biol. 145:1435-1442.
81. Walch-Solimena, C., J. Blasi, L. Edelmann, E.R. Chapman, G.F. von Mollard, and R. Jahn. 1995. t-SNAREs syntaxin 1 and SNAP-25 are present on organelles that participate in synaptic vesicle recycling. J. Cell Biol. 128:637-645.
82. Weber, T., B.V. Zelmelman, J.A. McNew, B. Westermann, M. Gmachl, F. Parlati, T.H. Sollner, and J.E. Rothman. 1998. SNAREpins: minimal machinery for membrane fusion. Cell. 92:759-772.
83. Weimbs, T., S.H. Low, S.J. Chapin, K.E. Mostov, P. Bucher, and K. Hofmann. 1997. A conserved domain is present in different families of vesicular fusion proteins: a new superfamily. Proc. Natl. Acad. Sci. USA. 94:3046-3051.
84. Weimbs, T., K. Mistov, S.H. Low, and K. Hofman. 1998. A model for structural similarity between different SNARE complexes based on sequence relationships. Trends Cell Biol. 8:260-262.
85. Wichmann, H., L. Hengst, and D. Gallwitz. 1992. Endocytosis in yeast: evidence for the involvement of a small GTP-binding protein (Ypt7p). Cell. 71: 1131-1142.
86. Wilson, D.W., S.W. Whiteheart, M. Wiedman, M. Brunner, and J.E. Rothman. 1992. A multisubunit particle implicated in membrane fusion. J. Cell Biol. 117:531-538.
87. Wooding, S., and H.R. Pelham. 1998 The dynamics of Golgi protein traffic visualized in living yeast cells. Mol. Biol. Cell. 9:2667-2680.
88. Xu, Y., S.H. Wong, T. Zhang, V.N. Subramaniam, and W. Hong. 1997. GS15, a 15-kilodalton Golgi soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) homologous to rbet1. J. Biol. Chem. 272:20162-20166.
89. Yanagisawa, K., D. Resnick, C. Abeijon, P.W. Robbins, and C.B. Hirschberg. 1990. A guanosine diphophatase enriched in Golgi vesicles of Saccharomyces cerevisiae: purification and characterization. J. Biol. Chem. 265:19351-19355.
90. Zhang, T., S.H. Wong, B.L. Tang, Y. Xu, F. Peter, V.N. Subramaniam, and W. Hong. 1997. The mammalian protein (rbet1) homologous to yeast Bet1p is primarily associated with the pre-Golgi intermediate compartment and is involved in vesicular transport from the endoplasmic reticulum to the Golgi apparatus. J. Cell Biol. 139:1157-1168.