Three distinct steps in transport of vesicular stomatitis virus glycoprotein from the ER to the cell surface in vivo with differential sensitivities to GTPγS

Journal of Cell Science

Volumn 111, Issue 13, 1998, Pages 1877-1888

  Pepperkok, Rainer ^a,c   Lowe, Martin ^a,c   Burke, Brian ^b   Kreis, Thomas E ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF CALGARY   (Canada)

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Coat protein; Exocytic membrane traffic; GTP analog; GTP binding protein; Microinjection

Indexed keywords

BREFELDIN A; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); VIRUS GLYCOPROTEIN;

ANIMAL CELL; ARTICLE; CELL SURFACE; ENDOPLASMIC RETICULUM; GOLGI COMPLEX; INTRACELLULAR TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; VERO CELL; VESICULAR STOMATITIS VIRUS;

ANIMALS; BIOLOGICAL TRANSPORT; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOPLASMIC RETICULUM; GLYCOPROTEINS; GOLGI APPARATUS; GTP-BINDING PROTEINS; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); HYDROLYSIS; MEMBRANE GLYCOPROTEINS; MICROINJECTIONS; MONOMERIC GTP-BINDING PROTEINS; MUTATION; SACCHAROMYCES CEREVISIAE PROTEINS; VERO CELLS; VESICULAR STOMATITIS-INDIANA VIRUS; VIRAL ENVELOPE PROTEINS;

ANIMALIA; MAMMALIA; VESICULAR STOMATITIS VIRUS;

EID: 0031826012     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (96)

1. Aniento, F., Gu, F., Parton, R. G. and Gruenberg, J. (1996). An endosomal beta COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J. Cell Biol. 133, 29-41.
2. Aridor, M., Bannykh, S. I., Rowe, T. and Balch, W. E. (1995) Sequential coupling between COPII and COPI vesicle coats in endoplasmic reticulum to Golgi transport. J. Cell Biol. 131, 875-893.
3. Bannykh, S. I., Rowe, T. and Balch, W. E. (1996). The organization of endoplasmic reticulum export complexes. J. Cell Biol. 135, 19-35.
4. Bannykh, S. I. and Balch, W. E. (1997). Membrane dynamics at the endoplasmic reticulum-Golgi interface. J. Cell Biol. 138, 1-4.
5. Barlowe, C., d'Enfert, C. and Schekman, R. (1993). Purification and characterization of SAR1p, a small GTP-binding protein required for transport vesicle formation from the endoplasmic reticulum. J. Biol. Chem. 268, 873-879.
6. Barlowe, C., Orci, L., Yeung, T., Hosobuchi, M., Hamamoto, S., Salama, N., Rexach, M. F., Ravazzola, M., Amherdt, M. and Schekman, R. (1994). COPII: A membrane coat formed by sec proteins that drive vesicle budding from the endoplasmic reticulum. Cell 77, 895-907.
7. Barr, F. A. and Huttner, W. B. (1996). A role for ADP-ribosylation factor 1. but not COP I, in secretory vesicle biogenesis from the trans-Golgi network. FEBS Lett. 384, 65-70.
8. Beckers, C. J. and Balch, W. E., (1989). Calcium and GTP: essential components in vesicular trafficking between the endoplasmic reticulum and Golgi apparatus. J. Cell Biol. 108, 1245-1256.
9. Bednarek, S. Y., Ravazzola, M., Hosobuchi, M., Amherdt, M., Perrelet, A. Schekman, R. and Orci, L. (1995). COPI- and COPII-coated vesicles bud directly from the endoplasmic reticulum in yeast. Cell 83, 1183-1196.
10. Bergmann, J. E., Tokuyasu, K. T. and Singer, S. J. (1981). Passage of an integral membrane protein, the vesicular stomatitis virus glycoprotein, through the Golgi apparatus en route to the plasma membrane. Proc. Nat. Acad. Sci. USA 78, 1746-1750.
11. Bloom, G. S. and Brashear, T. A. (1989). A novel 58-kDa protein associates with the Golgi apparatus and microtubules. J. Biol. Chem. 264, 16083-16092.
12. Bonatti, S., Migliaccio, G. and Simons, K. (1989). Palmitosylation of viral membrane glycoprotein takes place after exit from the endoplasmic retiulum. J. Biol. Chem. 264, 12590-12595.
13. Campbell, J. L. and Schekman, R. (1997). Selective packaging of cargo molecules into endoplasmic reticulum-derived COPII vesicles. Proc. Nat. Acad. Sci. USA 94, 837-842.
14. Chen, Y. G. and Shields, D. (1996). ADP-ribosylation factor-1 stimulates formation of nascent secretory vesicles from the trans-Golgi network of endocrine cells. J. Biol. Chem. 271, 5297-5300.
15. Cosson, P. and Letourneur, F. (1994). Coatomer interaction with di-lysine endoplasmic reticulum retention motifs. Science 263, 1629-1631.
16. Cosson, P., Démollière, C., Hennecke, S., Duden, R. and Letourneur, F. (1996). Delta- and zeta-COP, two coatomer subunits homologous to clathrin-associated proteins, are involved in ER retrieval. EMBO J. 15, 1792-1798.
17. Cowles, C. R., Odorizzi, G., Payne, G. S. and Emr, S. D. (1997). The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. Cell 91, 109-118.
18. Dascher, C. and Balch, W. E. (1994). Dominant inhibitory mutants of ARF1 block endoplasmic reticulum to Golgi transport and trigger disassembly of the Golgi apparatus. J. Biol. Chem. 269, 1437-1448.
19. Dell'Angelica, E. D., Ohno, H., Ooi, C. E., Rabinovich, E., Roche, W. K. and Bonifacino, J. S. (1997). AP-3: an adaptor like protein complex with ubiquitous expression. EMBO J. 16, 917-928.
20. Donaldson, J. G., Lippincott-Schwartz, J., Bloom, G. S., Kreis, T. E. and Klausner, R. D. (1990). Dissociation of a 110-kD peripheral membrane protein from the Golgi apparatus is an early event in brefeldin A action. J. Cell Biol. 111, 2295-2306.
21. Donaldson, J. G., Lippincott-Schwartz, J., Bloom, G. S., Kreis, T. E. and Klausner, R. D. (1991). Binding of ARF and β-COP to Golgi membranes: possible regulation by trimeric G protein. Science 254, 1197-1199.
22. Duden, R., Griffiths, G., Frank, R., Argos, P. and Kreis, T. E. (1991). β-COP. a 110kd protein associated with non-clathrin-coated vesicles and the Golgi complex, shows homology to β-adaptin. Cell 64, 649-665.
23. Evan, G. I., Lewis, G. K., Ramsay, G. and Bishop, J. M. (1985) Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5, 3610-3616.
24. Fiedler, K., Veit, M., Stamnes, M. A. and Rothman, J. E. (1996). Bimodal interaction of coatomer with the p24 family of putative cargo receptors. Science 273, 1396-1399.
25. Griffiths, G., Pfeifler, S., Simons, K. and Matlin, K. (1985). Exit of newly synthesized membrane proteins from the trans cisterna of the Golgi complex to the plasma membrane. J. Cell Biol. 101, 949-964.
26. Griffiths, G., Ericsson, M., Krijnse-Locker, J., Nilsson, T., Goud, B., Soling, H. D., Tang, B. L. , Wong, S. H., Hong, W., et al. (1994). Localization of the Lys. Asp. Glu. Leu tetrepeptide receptor to the Golgi complex and the intermediate compartment in mammalian cells. J. Cell Biol. 127, 1557-1574.
27. Griffiths, G., Pepperkok, R., Locker, J. K. and Kreis, T. K. (1995). Immunocytochemical localization of beta-COP to the ER-Golgi boundary and the TGN. J. Cell Sci. 108, 2839-2856.
28. Hammond, C. and Helenius, A. (1994). Quality control in the secretory pathway: retention of a misfolded viral membrane glycoprotein involves cycling between the ER. intermediate compartment and Golgi apparatus. J. Cell Biol. 126, 41-52.
29. Harter, C., Pavel, J., Coccia, F., Draken, E., Wegehingel, S., Tschochner, H. and Wieland, F. (1996). Nonclathrin coat protein gamma, a subunit of coatomer, binds to the cytoplasmic dilysine motif of membrane proteins of the early secretory pathway. Proc. Nat. Acad. Sci. USA 93, 1902-1906.
30. Hosobuchi, M., Kreis, T. E., and Schekman, R. (1992). Sec21 is a gene required for ER to Golgi transport that encodes a subunit of a yeast coatomer. Nature 360, 603-605.
31. Ikonen, E., Parton, R. G., Lafont, F. and Simons, K. (1996). Analysis of the role of p200-containing vesicles in post-Golgi traffic. Mol. Biol. Cell 7, 961-974.
32. Ikonen, E., de Almeid, J. B., Fath, K. F., Burgess, D. R., Ashman, K., Simons, K. and Stow, J. L. (1997). Myosin II is associated with Golgi membranes: identification of p200 as nonmuscle myosin II on Golgi-derived vesicles. J. Cell Sci. 110, 2155-2164.
33. Kreis, T. E. (1986). Microinjected antibodies against the cytoplasmic domain of vesicular stomatitis virus glycoprotem block its transport to the cell surface EMBO J 5, 931-941.
34. Kreis, T. E. and Lodish, H. F. (1986). Oligomerization is essential for transport of vesicular stomatitis viral glycoprotein to the cell surface. Cell 46, 929-937.
35. Kreis, T. E., Lowe, M. and Pepperkok, R. (1995) COPs regulating membrane traffic. Annu. Rev. Cell Dev. Biol. 11, 677-706.
36. Kuge, O., Dascher, C., Orci, L., Rowe, T., Amherdt, M., Plutner, H., Ravazzola, M., Tanigawa, G., Rothman, J. E. and Balch, W. E. (1994). Sar1 promotes vesicle budding from the endoplasmic reticulum but not Golgi compartments. J. Cell Biol. 125, 51-65.
37. Letourneur, F., Gaynor, E. C., Hennecke, S., Uemolliere, C., Duden, R., Emr, S. D., Riezman, H. and Cosson, P. (1994). Coatomer is essential for retrieval of dilysine-tagged proteins to the endoplasmic reticulum. Cell 79, 1199-1207.
38. Lewis, M. J. and Pelham, H. R. (1992). Ligand-induced redistribution of a human KDEL receptor from the Golgi complex to the endoplasmic reticulum. Cell 68, 353-364.
39. Leyte, A., Barr, F. A., Kehlenbach, R. H. and Huttner, W. B. (1992) Multiple trimeric G-proteins on the trans-Golgi network exert stimulatory and inhibitory effects on secretory vesicle formation. EMBO J. 11.
40. Lowe, M. and Kreis, T. E. (1995). In vitro assembly and disassembly of coatomer. J. Biol. Chem. 270, 31364-31371.
41. Malhotra, V., Serafini, T., Orci, L., Shepherd, J. C. and Rothman, J. E. (1989). Purification of a novel class of coated vesicles mediating biosynthetic protein transport through the Golgi stack. Cell 58, 329-336.
42. Matlin, K. S. and Simons, K. (1983). Reduced temperature prevents transfer of a membrane glycoprotein to the cell surface but does not prevent terminal glycosylation. Cell 34, 233-243.
43. Melançon, P., Glick, B. S., Malhotra, V., Weidmann, P. J., Serafini, T., Gleason, M. L., Orci, L. and Rothman, J. E. (1987) Involvement of GTP-binding 'G' proteins in transport through the Golgi stack. Cell 51, 1053-1062.
44. Miller, S. G., Carnell, L. and Moore, H. H. (1992). Post-Golgi membrane traffic: brefeldin A inhibits export from distal Golgi compartments to the cell surface but not recycling. J. Cell Biol. 118, 267-283.
45. Miller, S. G. and Moore, H. P. (1991). Reconstitution of constitutive secretion using semi-intact cells: regulation by GTP but not calcium. J. Cell Biol. 112, 39-54.
46. Müsch, A., Cohen, D. and Rodriguez-Boulan, E. (1997). Myosin II is involved in the production of constitutive transport vesicles from the TGN. J. Cell Biol. 138, 291-306.
47. Narula, N., McMorrow, I., Plopper, G., Doherty, J., Matlin, K. S., Burke, B. and Stow, J. L. (1992). Identification of a 200-kD. brefeldin-sensitive protein on Golgi membranes. J. Cell Biol. 117, 27-38.
48. Narula, N. and Stow, J. L. (1995). Distinct coated vesicles labeled for p200 bud from trans-Golgi network membranes. Proc. Nat. Acad. Sci. USA 92, 2874-2878.
49. Newman, L. S., McKeever, M. O., Okano, H. J. and Darnell, R. B. (1995) b-NAP, a cebrellar degeneration antigen, is a neuron-specific vesicle coat protein. Cell 82, 773-783.
50. Novick, P. and Brennwald, P. (1993). Friends and family: the role of the Rab GTPases in vesicular traffic. Cell 75, 597-601.
51. Nuoffer, C. and Balch, W. E. (1994). GTPases: multifunctional molecular switches regulating vesicular traffic. Annu. Rev. Biochem. 63, 949-990.
52. Oka, T. and Nakano, A. (1994). Inhibition of GTP hydrolysis by Sar1 p causes accumulation of vesicles that are a functional intermediate of the ER to Golgi transport in yeast. J. Cell Biol. 124, 425-434.
53. Oka, T., Nishikawa, S. and Nakano, A. (1991). Reconstitution of GTP-binding Sar1 protein function in ER to Golgi transport. J. Cell Biol. 114, 671-679.
54. Orci, L., Stamnes, M., Ravazzola, M., Amherdt, M., Perrelet, A., Söllner, T. H. and Rothman, J. E. (1997). Bidirectional transport by distinct populations of COPI-coated vesicles. Cell 90, 335-349.
55. Paccaud, J. P., Reith, W., Carpentier, J.-L., Ravazzola, M., Amherdt, M., Schekman, R. and Orci, L. (1996). Cloning and characterization of mammalian homologues of the COPII component Sec23. Mol. Biol. Cell 7, 1535-1546.
56. Palade, G. (1975). Intracellular aspects of the process of protein synthesis. Science 187, 347-358.
57. Palmer, D. J., Helms, J. B., Beckers, C. J. L. Orci and J. E. Rothman, (1993). Binding of coatomer to Golgi membranes requires ADP-ribosylation factor. J. Biol. Chem. 268, 12083-12089.
58. Pearse, B. M. F. and Robinson, M. S. (1990). Clathrin, adaptors and sorting. Annu. Rev. Cell Biol. 1, 151-171.
59. Pepperkok, R., Scheel, J., Horstmann, H., Hauri, H. P., Griffiths, G. and Kreis, T. E. (1993). Beta-COP is essential for biosynthetic membrane transport from the endoplasmic reticulum to the Golgi complex in vivo Cell 74, 71-82.
60. Peter, F., Plutner, H., Zhu, H., Kreis, T. E. and Balch, W. E. (1993). Beta-COP is essential for transport of protein from the endoplasmic reticulum to the Golgi in vitro. J. Cell Biol. 122, 1155-1167.
61. Pierre, P., Pepperkok, R. and Kreis, T. E. (1994). Molecular characterisation of two functional domains of CLIP-170 in vivo. J. Cell Sci. 107, 1909-1920.
62. Pevsner, J., Volknandt, W., Wong, B. R. and Scheller, R. H. (1994) Two rat homologs of clathrin-associated adaptor proteins. Gene 146, 279-283.
63. Pimplikar, S. W. and Simons, K. (1993). Regulation of apical transport in epithelial cells by a Gs class of heterotrimeric G protein. Nature 362, 456-458.
64. Ponnambalam, S., Rabouille, C., Luzio, J. P., Nilsson, T. and Warren, G. (1994). The TGN38 glycoprotein contains two non-overlapping signals that mediate localisation to the trans-Golgi network. J. Cell Biol. 125, 253-268.
65. Presley, J. F., Cole, N. B., Schroer, T. A., Hirschberg, K., Zaal, K. J. and Lippincott-Schwartz, J. (1997). ER-to-Golgi transport visualized in living cells. Nature 389, 81-85.
66. Rexach, M. F., Latterich, M. and Schekman, R. W. (1994). Characteristics of endoplasmic reticulum-derived transport vesicles. J. Cell Biol. 126, 1133-1148.
67. Robinson, M. S. (1994). The role of clathrin. adaptors and dynamin in endocytosis. Curr. Opin. Cell Biol. 6, 538-544.
68. Robinson, M. S. and Kreis, T. E. (1992). Recruitment of coat proteins onto Golgi membranes in intact and permeabilized cells: effects of brefeldin A and G protein activators. Cell 69, 129-138.
69. Rosa, P., Barr, F. A., Stinchcombe, J. C., Binacchi, C. and Huttner, W. B. (1992). Brefeldin A inhibits the formation of constitutive secretors vesicles and immature secretory granules from the trans-Golgi network. Eur. J. Cell Biol. 59, 265-274.
70. Rothman, J. E. and Orci, L. (1992). Molecular dissection of the secretory pathway. Nature 355, 409-415.
71. Saraste, J. and Kuismanen, E. (1984). Pre- and post-Golgi vacuoles operate in the transport of Semliki Forest virus membrane glycoproteins to the cell surface. Cell 38, 535-549.
72. Saraste, J., Lahtinen, U. and Goud, B. (1995). Localisation of the small GTP-binding protein rablp to early compartments of the secretory pathway. J. Cell Sci. 108, 1541-1552.
73. Satoh, A. K., Tokunaga, F., Kawamura, S. and Ozaki, K. (1997). In situ inhibition of vesicle transport and protein processing in the dominant negative Rabl mutant of Drosophila. J Cell Sci. 110, 2943-2953.
74. Scales, S. J., Pepperkok, R. and Kreis T. E. (1997). Visualization of ER-to-Golgi transport in living cells reveals a sequential mode of action for COPII and COPI. Cell 90, 1137-1148.
75. Scheel, J., Pepperkok, R., Lowe, M., Griffiths, G. and Kreis, T. (1997). Dissociation of coatomer from membranes is required for brefeldin A-induced transfer of Golgi enzymes to the endoplasmic reticulum. J. Cell Biol. 137, 319-333.
76. Schekman, R. and Orci, L. (1996) Coat proteins and vesicle budding Science 271, 1526-1533.
77. Schekman, R. and Mellman, I. (1997). Does COPI go both ways? Cell 90, 197-200.
78. Schweizer, A., Fransen, J. A. M., Bächi, T., Ginsel, L. and Hauri, H.-P. (1988). Identification, by a monoclonal antibody, of a 53-kD protein associated with a tubulo-vesicular compartment at the cis-side of the Golgi complex. J. Cell Biol. 107. 1643-1653.
79. Shaywitz, D. A., Orci, L., Ravazzola, M., Swaroop, A. and Kaiser, C. A. (1995). Human SFCI3Rp functions in yeast and is located on transport vesicles budding from the endoplasmic reticulum. J. Cell Biol. 128, 769-777.
80. Simon, J. P., Ivanov, I. E., Shopsin, B., Hersh, D., Adesnik, M. and Sabatini, D. D. (1996). The in vitro generation of post-Golgi vesicles carrying viral envelope glycoproteins requires an ARF-like GTP-binding protein and a protein kinase C associated with the Golgi apparatus. J. Biol. Chem. 271, 16952-16961.
81. Simpson, F., Bright, N. A., West, M. A., Newman, L. S., Darnell, R. B. and Robinson, M. S. (1996). A novel adaptor-related protein complex. J. Cell Biol. 133, 749-760.
82. Sönnichsen, B., Watson, R., Clausen, H., Misteli, T. and Warren, G. (1996). Sorting by COP I-coated vesicles under interphase and mitolic conditions. J. Cell Biol. 134, 1411-1425.
83. Sohn, K., Orci, L., Ravazzola, M., Amherdt, M., Bremser, M., Lottspeich, F., Fiedler, K., Helms, J. B. and Wieland, F. T. (1996) A major transmembrane protein of Golgi-derived COPI-coaied vesicles involved in coatomer binding. J. Cell Biol. 135, 1239-1248.
84. Stamnes, M. A. and Rothman, J. E. (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.
85. Tanigawa, G., Orci, L., Amherdt, M., Ravazzola, M., Helms, J. B. and Rothman, J. E. (1993). Hydrolysis of hound GTP by ARF protein triggers uncoating of Golgi-dcrived COP-coated vesicles. J. Cell Biol. 123, 1365-1371.
86. Tang, B. L., Peter, F., Krijnse-Locker, J., Low, S. H., Griffiths, G. and Hong, W. (1997). The mammalian homolog of yeast Sec13p is enriched in the intermediate compartment and is essential for protein transport from the endoplasmic reticulum to the Golgi apparatus. Mol. Cell Biol. 17, 256-266.
87. Teal, S. B., Hsu, V. W., Peters, P. J., Klausner, R. D. and Donaldson, J. G. (1994). An activating mutation in ARFI stabilizes coatomer binding to Golgi membranes. J. Biol. Chem. 269, 3135-3138.
88. Tisdale, E. J., Bourne, J. R., Khosravi-Far, R., Der, C. J. and Batch, W. E. (1992). GTP-binding mutants of rab1 and rab2 are potent inhibitors of vesicular transport from the endoplasmic reticulum to the Golgi complex. J. Cell Biol. 119, 749-761
89. Traub, L. M., Ostrom, J. A. and Kornfeld, S. (1993) Biochemical dissection of AP-1 recruitment onto Golgi membranes. J. Cell Biol. 123, 561-573.
90. Vaux, D., Tooze, J. and Fuller, S. (1990). Identification by anti-idiotype antibodies of an intracellular membrane protein that recognizes a mammalian endoplasmic reticulum retention signal. Nature 345, 495-502.
91. West, M. A., Bright, N. A. and Robinson, M. S. (1997). The role of ADP-ribosylation factor and phospholipase D in adaptor recruitment. J. Cell Biol. 138, 1239-1254.
92. Whitney, J. A., Gomez, M., Sheff, D., Kreis, T. K. and Mellman, I. (1995) Cytoplasmic coat proteins involved in endosome function. Cell 83, 703-713.
93. Xu, H. and Shields, D. (1993). Prohormone processing in the trans-Golgi network: endoprotcolytic cleavage of prosomalostatin and formation of nascent secretory vesicles in permeabilized cells. J. Cell Biol. 122, 1169-1184.
94. Zerial, M. and Stenmark, H. (1993). Rab GTPases in vesicular transport. Curr. Opin. Cell Biol. 5, 613-620.
95. Zerial, M. and Huber, L. A. (editors) (1995). Guidebook to the Small GTPases. Sambrook and Tooze Publication at Oxford University Press.
96. Zhang, C. J., Rosenwald, A. G., Willingham, M. C., Skuntz, S., Clark, J. and Kahn, R. A. (1994). Expression of a dominant allele of human ARF1 inhibits membrane traffic in vivo. J. Cell Biol. 124, 289-300.