Retrograde transport from the pre-Golgi intermediate compartment and the Golgi complex is affected by the vacuolar H+ -ATPase inhibitor Bafilomycin A1

Molecular Biology of the Cell

Volumn 9, Issue 12, 1998, Pages 3561-3578

  Palokangas, Harri ^a,b   Ying, Ming ^a   Väänänen, Kalervo ^b   Saraste, Jaakko ^a  

^a UNIVERSITY OF BERGEN   (Norway)

^b UNIVERSITY OF OULU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BAFILOMYCIN A1; ENZYME INHIBITOR; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL FRACTIONATION; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME INHIBITION; GOLGI COMPLEX; HUMAN; HUMAN CELL; IMMUNOELECTRON MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; VESICULAR STOMATITIS VIRUS;

ANIMALIA; VESICULAR STOMATITIS VIRUS;

EID: 0031772176     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.9.12.3561     Document Type: Article

References (88)

1. Anderson, R.G.W., Falck, J.R., Goldstein, J.L. and Brown, M.S. (1984). Visualization of acidic organelles in intact cells by electron microscopy. Proc. Natl. Acad. Sci. USA 81, 4838-4842.
2. Anderson, R.G.W., and Pathak, R.K. (1985). Vesicles and cisternae in the trans Golgi apparatus of human fibroblasts are acidic compartments. Cell 40, 635-643.
3. Aniento, F., Gu, F., Parton, R.G., Gruenberg, J. (1996). An endosomal β-COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J. Cell Biol. 133, 29-41.
4. Arar, C., Carpentier, V., Le Caer, J.-P., Monsigny, M., Legrand, A., and Roche, A.-A. (1995). ERGIC-53, a membrane protein of the endoplasmic reticulum-Golgi intermediate compartment, is identical to MR60, an intracellular mannose-specific lectin of myelomonocytic cells. J. Biol. Chem. 270, 3551-3553.
5. Aridor, M., and Balch, W.E. (1996). Principles of selective transport: coat complexes hold the key. Trends Cell Biol. 96, 315-320.
6. Bannykh, S.I., Rowe, T., and Balch, W.E. (1996). The organization of the endoplasmic reticulum export complexes. J. Cell Biol. 135, 19-35.
7. Barlowe, C., et al. (1994). COPII: A membrane coat formed by sec proteins that drives vesicle budding from the endoplasmic reticulum. Cell 77, 895-907.
8. Bergman, J.E. (1989). Using temperature-sensitive mutants of VSV to study membrane protein biogenesis. Methods Cell Biol. 32, 85-110.
9. Bonifacino, J.S., Lippincott-Schwartz, J., Chen, C., Antusch, D., Samelson, L.E., and Klausner, R.D. (1988). Association and dissociation of the murine T cell receptor-associated protein (TRAP). Early events in the biosynthesis of a multi-subunit receptor. J. Biol. Chem. 263, 8965-8971.
10. Boulay, F., Doms, R., Wilson, I., and Helenius, A. (1987). The influenza hemagglutinin as an acid sensitive probe of the biosynthetic pathway. EMBO J. 6, 2643-2650.
11. Bowman, E.J., Siebers, A., and Altendorf, K. (1988). Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. USA 85, 7972-7976.
12. Clague, M., Urbe, S., Aniento, F., and Gruenberg, J. (1994). Vacuolar ATPase activity is required for endosomal carrier vesicle formation. J. Biol. Chem. 269, 21-24.
13. Cluett, E.B., Wood, S.A., Banta, M., and Brown, W.J. (1993). Tubulation of Golgi membranes in vivo and in vitro in the absence of brefeldin A. J. Cell Biol. 120, 15-24.
14. Cole, N.B., Sciaky, N., Marotta, A., Song, J., and Lippincott-Schwartz, J. (1996). Golgi dispersal during microtubule disruption: regeneration of Golgi stacks at peripheral endoplasmic reticulum exit sites. Mol. Biol. Cell 7, 631-650.
15. D'Arrigo, A., Bucci, C., Toh, B.-H., and Stenmark, H. (1997). Microtubules are involved in bafilomycin A1-induced tubulation and Rab5-dependent vacuolization of early endosomes. Eur. J. Cell Biol. 72, 95-103.
16. Doms, R.W., Keller, D.S., Helenius, A., and Balch, W.E. (1987). Role of adenosine triphosphate in the assembly and transport of vesicular stomatitis virus G protein trimers. J. Cell Biol. 105, 1957-1969.
17. Doms, R.W., Russ, G., and Yewdell, J.W. (1989). Brefeldin A redistributes resident and itinerant Golgi proteins to the endoplasmic reticulum. J. Cell Biol. 109, 61-72.
18. Donaldson, J.G., Lippincott-Schwartz, J., Bloom, G., Kreis, T., 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.
19. Duden, R., Griffiths, G., Frank, R., Argos, P., and Kreis, T.E. (1991). β-COP, a 110 kD protein associated with non-clathrin coated vesicles and the Golgi complex, shows homology to β-adaptin. Cell 64, 649-665.
20. Echard, A., Jollivet, F., Martinez, O., Lacapère, J.-J., Rousselet, A., Janoueix-Lerosey, I., and Goud, B. (1998). Interaction of a Golgi-associated kinesin-like protein with rab6p. Science 279, 580-585.
21. Fiedler, K., and Simons, K. (1994). A putative novel class of animal lectins in the secretory pathway homologous to leguminous lectins. Cell 77, 625-626.
22. Gaynor, E.C., and Emr, S.D. (1997). COPI-independent anterograde transport: cargo-selective ER to Golgi protein transport in yeast COPI mutants. J. Cell Biol. 136, 789-802.
23. +-ATPase occurs in the endoplasmic reticulum and requires a vma12p/vma22p assembly complex. J. Cell Biol. 142, 39-49.
24. Griffiths, G., Ericsson, M., Krijnse Locker, J., Nilsson, T., Goud, B., Soling, H.-D., Tang, B.L., Wong, S.H., and Hong, W. (1994). Localization of the lys, asp, glu, leu tetrapeptide receptor to the Golgi complex and the intermediate compartment in mammalian cells. J. Cell. Biol. 127, 1557-1574.
25. Griffiths, G., Pepperkok, R., Krinjse Locker, J., and Kreis, T.E. (1995). Immunocytochemical localization of β-COP to the ER-Golgi boundary and the TGN. J. Cell Sci. 108, 2839-2856.
26. 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.
27. Hopkins, C.R., Gibson, A., Shipman, M., and Miller, K. (1990). Movement of internalized ligand-receptor complexes along a continuous endosomal reticulum. Nature 346, 335-339.
28. Itin, C., Roche, A.-C., Monsigny, M., and Hauri, H.P. (1996). ERGIC-53 is a functional mannose-selective and calcium-dependent human homologue of leguminous lectins. Mol. Biol. Cell 7, 483-493.
29. Jäntti, J., Saraste, J., and Kuismanen, E. (1997). Protein segregation in peripheral pre-Golgi intermediates in response to caffeine treatment at 20°C. Eur. J. Cell Biol. 74, 150-164.
30. Kappeler, F., Klopfenstein, D.R.C., Foquet, M., Paccaud, J.-P., and Hauri, H.-P. (1997). The recycling of ERGIC-53 in the early secretory pathway. J. Biol. Chem. 272, 31801-31808.
31. Kim, J.H., Lingwood, C.A., Williams, D.B., Furuya, W., Manolson, M.F., and Grinstein, S. (1996). Dynamic measurement of the pH of the Golgi complex in living cells using retrograde transport of the verotoxin receptor. J. Cell Biol. 134, 1387-1399.
32. Klausner, R.D., Donaldson, J.G., and Lippincott-Schwartz, J. (1992). Brefeldin A: insights into the control of membrane traffic and organelle structure. J. Cell Biol. 116, 1071-1080.
33. Klionsky, D.J., and Emr, S.D. (1989). Membrane protein sorting: biosynthesis, transport and processing of yeast vacuolar alkaline phosphatase. EMBO J. 8, 2241-2250.
34. Kreis, T.E., Lowe, M., and Pepperkok, R. (1995). COPs regulating membrane traffic. Annu. Rev. Cell Dev. Biol. 11, 677-706.
35. Lahtinen, U., Dahllöf, B., and Saraste, J. (1992). Characterization of a 58 kDa cis-Golgi protein in pancreatic exocrine cells. J. Cell Sci. 103, 321-333.
36. Lahtinen, U., Hellman, U., Wernstedt, C., Saraste, J., and Pettersson, R.F. (1996). Molecular cloning of the 58 kDa (p58) cis-Golgi and intermediate compartment protein. J. Biol. Chem. 271, 4031-4037.
37. Letourneur, F., Gaynor, E.C., Hennecke, S., Demolliere, 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.B. (1996). SNARE-mediated retrograde traffic from the Golgi complex to the endoplasmic reticulum. Cell 85, 205-215.
39. Liljeström, P., and Garoff, H. (1991). A new generation of animal cell expression vectors based on the Semliki Forest virus replicon. Biotechnology 9, 1356-1361.
40. Lippincott-Schwartz, J. (1993). Bidirectional membrane traffic between the endoplasmic reticulum and Golgi apparatus. Trends Cell Biol. 3, 81-88.
41. Lippincott-Schwartz, J., Cole, N.B., Marotta, A., Conrad, P.A., and Bloom, G.S. (1995). Kinesin is the motor for microtubule-mediated Golgi-to-ER membrane traffic. J. Cell. Biol. 128, 293-306.
42. Lippincott-Schwartz, J., Donaldson, J.G., Schweitzer, A., Berger, E.G., Hauri, H.-P., Yuan, L.C., and Klausner, R.D. (1990). Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway. Cell 60, 821-836.
43. Lotti, L., Torrisi, M., Pascale, M., and Bonatti, S. (1992). Immunocytochemical analysis of the transfer of VSV G-protein from the intermediate compartment to the Golgi complex. J. Cell Biol. 118, 43-50.
44. Mellman, I., Fuchs, R., and Helenius, A. (1986). Acidification of the endocytic and exocytic pathways. Annu. Rev. Biochem. 55, 663-700.
45. Mukherjee, S., Ghosh, R.N., and Maxfield, F.C. (1997). Endocytosis. Physiol. Rev. 77, 759-803.
46. Muroi, M., Shiragami, N., Nagao, K., Yamasaki, M., and Takatsuki, A. (1993). Folimycin (concanamycin A), a specific inhibitor of V-ATPase, blocks intracellular translocation of the glycoprotein of vesicular stomatitis virus before arrival to the Golgi apparatus. Cell Struct. Funct. 18, 139-149.
47. +-adenosine triphosphatase. J. Cell Physiol. 156, 35-42.
48. Nichols, W.C., et al. (1998). Mutations in the ER-Golgi intermediate compartment protein ERGIC-53 cause combined deficiency of coagulation factors V and VIII. Cell 93, 61-70.
49. Nuoffer, C., and Balch, W.E. (1994). GTPases: multifunctional molecular switches regulating vesicular traffic. Annu. Rev. Biochem. 63, 949-990.
50. Oprins, A., Duden, R., Kreis, T.E., Geuze, H., and Slot, J.W. (1993). β-COP localizes mainly to the cis-Golgi in exocrine pancreas. J. Cell Biol. 121, 49-59.
51. Orci, L., Stamnes, M., Ravazzola, M., Amherdt, M., Perrelet, A., Söllner, T., and Rothman, J.E. (1997). Bidirectional transport by distinct populations of COPI-coated vesicles. Cell 90, 335-349.
52. Palade, G.E. (1975). Intracellular aspects of the process of protein secretion. Science 187, 347-358.
53. +-ATPase is required for both endocytic and exocytic processes during viral infection of BHK-21 cells. J. Biol. Chem. 269, 17577-17585.
54. Pelham, H.R.B. (1994). About turn for COPs. Cell 79, 1125-1127.
55. Pepperkok, R., Scheel, J., Horstmann, H., Hauri, H.-P., Griffiths, G., and Kreis, T.E. (1993). β-COP is essential for biosynthetic membrane transport from the endoplasmic reticulum to the Golgi complex in vivo. Cell 74, 71-82.
56. Plutner, H., Cox, A.D., Pind, S., Khosravi-Far, R., Bourne, J.R., Schwaninger, R., Der, C.J., and Balch, W.E. (1991). Rab1b regulates vesicular transport between the ER and successive Golgi compartments. J. Cell Biol. 115, 31-43.
57. Presley, J.F., Cole, N.B., Schroer, T.A., Hirschberg, K., Zaal, K.J.M., and Lippincott-Schwartz, J. (1997). ER-to-Golgi transport visualized in living cells. Nature 389, 81-85.
58. Rambourg, A., and Clermont, Y. (1997). Three-dimensional structure of the Golgi apparatus in mammalian cells. In: The Golgi Apparatus, ed. E.G. Berger and J. Roth, Basel: Birkhauser Verlag, 37-61.
59. Robinson, M.S. (1997). Coats and vesicle budding. Trends Cell Biol. 7, 99-102.
60. Rothman, J.E., and Wieland, F.T. (1996). Protein sorting by transport vesicles. Science 272, 227-234.
61. 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.
62. Saraste, J., and Kuismanen, E. (1992). Pathways of protein sorting and membrane traffic between the rough endoplasmic reticulum and the Golgi complex. Semin. Cell Biol. 3, 343-355.
63. Saraste, J., Lahtinen, U., and Goud, B. (1995). Localization of the small GTP-binding protein rab1p to early compartments of the secretory pathway. J. Cell Sci. 108, 1541-1552.
64. Saraste, J., Palade, G.E. and Farquhar, M.G. (1987). Antibodies to rat pancreas Golgi subfractions: identification of a 58-kDa cis-Golgi protein. J. Cell Biol. 105, 2021-2029.
65. Saraste, J., and Svensson, K. (1991). Distribution of the intermediate elements operating in ER to Golgi transport. J. Cell Sci. 100, 415-430.
66. 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.
67. Scheel, A.A., and Pelham, H.R.B. (1996). Purification and characterization of the human KDEL receptor. Biochemistry 35, 10203-10209.
68. Scheel, J., Pepperkok, R., Lowe, M., Griffiths, G., and Kreis, T.E. (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.
69. Schekman, R., and Mellman, I. (1997). Does COPI go both ways? Cell 90, 197-200.
70. Schekman, R., and Orci, L. (1996). Coat proteins and vesicle budding. Science 271, 1526-1533.
71. Schindler, R., Itin, C., Zerial, M., Lottspeich, F., and Hauri, H.-P. (1993). ERGIC-53, a membrane protein of the ERGIC, carries an ER retention motif. Eur. J. Cell Biol. 61, 1-9.
72. Schwartz, A.L., Strous, G.J.A.M., Slot, J.W., and Geuze, H. (1985). Immunoelectron microscopic localization of acidic intracellular compartments in hepatoma cells. EMBO J. 4, 899-904.
73. 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 tubulovesicular compartment at the cis-side of the Golgi apparatus. J. Cell Biol. 107, 1643-1653.
74. Schweizer, A., Fransen, J.A.M., Matter, K., Kreis, T.E., Ginsel, L., and Hauri, H.-P. (1990). Identification of an intermediate compartment involved in protein transport from endoplasmic reticulum to Golgi apparatus. Eur. J. Cell Biol. 53, 185-196.
75. Sciaky, N., Presley, J., Smith, C., Zaal, K.J.M., Cole, N., Moreira, J.E., Terasaki, M., Siggia, E., and Lippincott-Schwartz, J. (1997). Golgi tubule traffic and the effects of brefeldin A visualized in living cells. J. Cell Biol. 139, 1137-1155.
76. +)-ATPase. Annu. Rev. Cell Dev. Biol. 13, 779-808.
77. Stinchcombe, J.C., Nomoto, H., Cutler, D., and Hopkins, C.R. (1995). Anterograde and retrograde traffic between the rough endoplasmic reticulum and the Golgi complex. J. Cell Biol. 131, 1387-1401.
78. Sönnichsen, B., Watson, R., Clausen, H., Misteli, T., and Warren, G. (1996). Sorting by COPI-coated vesicles under interphase and mitotic conditions. J. Cell Biol. 134, 1411-1425.
79. Tang, B.L., Low, S.H., Hauri, H.-P., and Hong, W. (1995). Segregation of ERGIC-53 and the mammalian KDEL receptor upon exit from the 157°C compartment. Eur. J. Cell Biol. 68, 398-410.
80. Tisdale, E.J., Plutner, H., Matteson, J., and Balch, W.E. (1997). p53/58 binds COPI and is required for selective transport through the early secretory pathway. J. Cell Biol. 137, 581-593.
81. Tooze, J., and Hollinshead, M. (1991). Tubular early endosomal networks in AtT20 and other cells. J. Cell Biol. 115, 635-653.
82. +-ATPase with bafilomycin reduces delivery of internalized molecules from mature multivesicular endosomes to lysosomes in Hep-2 cells. Eur. J. Cell Biol. 69, 343-350.
83. Van Weert, A.W., Dunn, K.W., Geuze, H.J., Maxfield, F.R., and Stoorvogel, W. (1995). Transport from late endosomes to lysosomes, but not sorting of integral membrane proteins in endosomes, depends on the vacuolar proton pump. J. Cell Biol. 130, 821-834.
84. Weidman, P., Roth, R., and Heuser, J. (1993). Golgi membrane dynamics imaged by freeze-etch electron microscopy: views of different membrane coatings involved in tubulation versus vesiculation. Cell 75, 123-133.
85. Wilson, D.W., Lewis, M.J. and Pelham, H.R.B. (1993). pH-dependent binding of KDEL to its receptor in vitro. J. Biol. Chem. 268, 7465-7468.
86. +-ATPases in the secretory pathway of HepG2 Cells. J. Biol. Chem. 268, 19092-19100.
87. Zeuzem, S., Feick, P., Zimmerman, P., Haase, W., Kahn, R.A., and Schultz, I. (1992). Intravesicular acidification correlates with binding of ADP-ribosylation factor to microsomal membranes. Proc. Natl. Acad. Sci. USA 89, 6619-6623.
88. Zhao, H., Lindqvist, B., Garoff, H., von Bonsdorff, C.-H., and Liljeström, P. (1994). A tyrosine-based motif in the cytoplasmic domain of the alphavirus envelope protein is essential for budding. EMBO J. 13, 4204-4211.