Hepatitis C virus RNA replication occurs on a detergent-resistant membrane that cofractionates with caveolin-2

Journal of Virology

Volumn 77, Issue 7, 2003, Pages 4160-4168

  Shi, Stephanie T ^a   Lee, Ki Jeong ^a   Aizaki, Hideki ^a   Hwang, Soon B ^b   Lai, Michael M C ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b Hallym University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; BROMINE; CAVEOLIN 2; CELL PROTEIN; CYCLOHEXIMIDE; DETERGENT; FAT DROPLET; MEMBRANE PROTEIN; PROTEIN SYNTHESIS INHIBITOR; PUROMYCIN; URIDINE TRIPHOSPHATE; VIRUS RNA;

ARTICLE; CELL FRACTIONATION; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; ENDOPLASMIC RETICULUM; FLOTATION; GENE EXPRESSION; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INTRACELLULAR MEMBRANE; MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REPLICON; RNA REPLICATION; RNA SYNTHESIS;

CAVEOLIN 2; CAVEOLINS; CELL LINE; DETERGENTS; ENDOPLASMIC RETICULUM; HEPACIVIRUS; HUMANS; INTRACELLULAR MEMBRANES; MEMBRANE LIPIDS; POLYETHYLENE GLYCOLS; PROTEIN SYNTHESIS INHIBITORS; RNA, VIRAL; SOLUBILITY; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 0037379425     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.7.4160-4168.2003     Document Type: Article

References (59)

1. Anderson, R. G. 1998. The caveolae membrane system. Annu. Rev. Biochem. 67:199-225.
2. Barman, S., A. Ali, E. K. Hui, L. Adhikary, and D. P. Nayak. 2001. Transport of viral proteins to the apical membranes and interaction of matrix protein with glycoproteins in the assembly of influenza viruses. Virus Res. 77:61-69.
3. Bavari, S., C. M. Bosio, E. Wiegand, G. Ruthel, A. B. Will, T. W. Geisbert, M. Hevey, C. Schmaljohn, A. Schmaljohn, and M. J. Aman. 2002. Lipid raft microdomains: a gateway for compartmentalized trafficking of Ebola and Marburg viruses. J. Exp. Med. 195:593-602.
4. Bienz, K., D. Egger, and T. Pfister. 1994. Characteristics of the poliovirus replication complex. Arch. Virol. Suppl. 9:147-157.
5. Bienz, K., D. Egger, T. Pfister, and M. Troxler. 1992. Structural and functional characterization of the poliovirus replication complex. J. Virol. 66:2740-2747.
6. Blight, K. J., A. A. Kolykhalov, and C. M. Rice. 2000. Efficient initiation of HCV RNA replication in cell culture. Science 290:1972-1975.
7. Brass, V., E. Bieck, R. Montserret, B. Wolk, J. A. Hellings, H. E. Blum, F. Penin, and D. Moradpour. 2002. An amino-terminal amphipathic alpha-helix mediates membrane association of the hepatitis C virus nonstructural protein 5A. J. Biol. Chem. 277:8130-8139.
8. Brown, D. A. 2001. Lipid droplets: proteins floating on a pool of fat. Curr. Biol. 11:R446-R449.
9. Brown, D. A., and J. K. Rose. 1992. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68:533-544.
10. Campbell, S. M., S. M. Crowe, and J. Mak. 2001. Lipid rafts and HIV-1: from viral entry to assembly of progeny virions. J. Clin. Virol. 22:217-227.
11. Cauchi, M. R., E. A. Henchal, and P. J. Wright. 1991. The sensitivity of cell-associated dengue virus proteins to trypsin and the detection of trypsin-resistant fragments of the nonstructural glycoprotein NS1. Virology 180:659-667.
12. Chert, J., and P. Ahlquist. 2000. Brome mosaic virus polymerase-like protein 2a is directed to the endoplasmic reticulum by helicase-like viral protein 1a. J. Virol. 74:4310-4318.
13. Egger, D., B. Wolk, R. Gosert, L. Bianchi, H. E. Blum, D. Moradpour, and K. Bienz. 2002. Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J. Virol. 76:5974-5984.
14. Froshauer, S., J. Kartenbeck, and A. Helenius. 1988. Alphavirus RNA replicase is located on the cytoplasmic surface of endosomes and lysosomes. J. Cell Biol. 107:2075-2086.
15. Fujimoto, T., H. Kogo, K. Ishiguro, K. Tauchi, and R. Nomura. 2001. Caveolin-2 is targeted to lipid droplets, a new "membrane domain" in the cell. J. Cell Biol. 152:1079-1085.
16. Gkantiragas, I., B. Brugger, E. Stuven, D. Kaloyanova, X. Y. Li, K. Lohr, F. Lottspeich, F. T. Wieland, and J. B. Helms. 2001. Sphingomyelin-enriched microdomains at the Golgi complex. Mol. Biol. Cell 12:1819-1833.
17. Gosert, R., A. Kanjanahaluethai, D. Egger, K. Bienz, and S. C. Baker. 2002. RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J. Virol. 76:3697-3708.
18. Grakoui, A., C. Wychowski, C. Lin, S. M. Feinstone, and C. M. Rice. 1993. Expression and identification of hepatitis C virus polyprotein cleavage products. J. Virol. 67:1385-1395.
19. Guo, J. T., V. V. Bichko, and C. Seeger. 2001. Effect of alpha interferon on the hepatitis C virus replicon. J. Virol. 75:8516-8523.
20. Harder, T., and K. Simons. 1997. Caveolae, DIGs, and the dynamics of sphingolipid-cholesterol microdomains. Curr. Opin. Cell Biol. 9:534-542.
21. Higuchi, M., K. M. Izumi, and E. Kieff. 2001. Epstein-Barr virus latent-infection membrane proteins are palmitoylated and raft-associated: protein 1 binds to the cytoskeleton through TNF receptor cytoplasmic features. Proc. Natl. Acad. Sci. USA 98:4675-4680.
22. Hijikata, M., H. Mizushima, T. Akagi, S. Mori, N. Kakiuchi, N. Kato, T. Tanaka, K. Kimura, and K. Shimotohno. 1993. Two distinct proteinase activities required for the processing of a putative nonstructural precursor protein of hepatitis C virus. J. Virol. 67:4665-4675.
23. Hugle, T., F. Fehrmann, E. Bieck, M. Kohara, H. G. Krausslich, C. M. Rice, H. E. Blum, and D. Moradpour. 2001. The hepatitis C virus nonstructural protein 4B is an integral endoplasmic reticulum membrane protein. Virology 284:70-81.
24. Hwang, S. B., K. J. Park, Y. S. Kim, Y. C. Sung, and M. M. Lai. 1997. Hepatitis C virus NS5B protein is a membrane-associated phosphoprotein with a predominantly perinuclear localization. Virology 227:439-446.
25. Ikeda, M., M. Yi, K. Li, and S. M. Lemon. 2002. Selectable subgenomic and genome-length dicistronic RNAs derived from an infectious molecular clone of the HCV-N strain of hepatitis C virus replicate efficiently in cultured Huh7 cells. J. Virol. 76:2997-3006.
26. Kim, J. E., W. K. Song, K. M. Chung, S. H. Back, and S. K. Jang. 1999. Subcellular localization of hepatitis C viral proteins in mammalian cells. Arch. Virol. 144:329-343.
27. Li, M., C. Yang, S. Tong, A. Weidmann, and R. W. Compans. 2002. Palmitoylation of the murine leukemia virus envelope protein is critical for lipid raft association and surface expression. J. Virol. 76:11845-11852.
28. Lohmann, V., J. O. Koch, and R. Bartenschlager. 1996. Processing pathways of the hepatitis C virus proteins. J. Hepatol. 24:11-19.
29. Lohmann, V., F. Korner, J. Koch, U. Herian, L. Theilmann, and R. Bartenschlager. 1999. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285:110-113.
30. Manie, S. N., S. Debreyne, S. Vincent, and D. Gerlier. 2000. Measles virus structural components are enriched into lipid raft microdomains: a potential cellular location for virus assembly. J. Virol. 74:305-311.
31. Mottola, G., G. Cardinali, A. Ceccacci, C. Trozzi, L. Bartholomew, M. R. Torrisi, E. Pedrazzini, S. Bonatti, and G. Migliaccio. 2002. Hepatitis C virus nonstructural proteins are localized in a modified endoplasmic reticulum of cells expressing viral subgenomic replicons. Virology 293:31-43.
32. Okamoto, H., S. Okada, Y. Sugiyama, T. Tanaka, Y. Sugai, Y. Akahane, A. Machida, S. Mishiro, H. Yoshizawa, Y. Miyakawa, et al. 1990. Detection of hepatitis C virus RNA by a two-stage polymerase chain reaction with two pairs of primers deduced from the 5′-noncoding region. Jpn. J. Exp. Med. 60:215-222.
33. Ostermeyer, A. G., J. M. Paci, Y. Zeng, D. M. Lublin, S. Munro, and D. A. Brown. 2001. Accumulation of caveolin in the endoplasmic reticulum redirects the protein to lipid storage droplets. J. Cell Biol. 152:1071-1078.
34. Park, J. S., J. M. Yang, and M. K. Min. 2000. Hepatitis C virus nonstructural protein NS4B transforms NIH 3T3 cells in cooperation with the Ha-ras oncogene. Biochem. Biophys. Res. Commun. 267:581-587.
35. Pedersen, K. W., Y. van der Meer, N. Roos, and E. J. Snijder. 1999. Open reading frame 1a-encoded subunits of the arterivirus replicase induce endoplasmic reticulum-derived double-membrane vesicles which carry the viral replication complex. J. Virol. 73:2016-2026.
36. Pfeifer, U., R. Thomssen, K. Legler, U. Bottcher, W. Gerlich, E. Weinmann, and O. Klinge. 1980. Experimental non-A, non-B hepatitis: four types of cytoplasmic alteration in hepatocytes of infected chimpanzees. Virchows Arch. B 33:233-243.
37. Pietschmann, T., V. Lohmann, G. Rutter, K. Kurpanek, and R. Bartenschlager. 2001. Characterization of cell lines carrying self-replicating hepatitis C virus RNAs. J. Virol. 75:1252-1264.
38. Pol, A., R. Luetterforst, M. Lindsay, S. Heino, E. Ikonen, and R. G. Parton. 2001. A caveolin dominant negative mutant associates with lipid bodies and induces intracellular cholesterol imbalance. J. Cell Biol. 152:1057-1070.
39. Polyak, S. J., D. M. Paschal, S. McArdle, M. J. Gale, Jr., D. Moradpour, and D. R. Gretch. 1999. Characterization of the effects of hepatitis C virus nonstructural 5A protein expression in human cell lines and on interferonsensitive virus replication. Hepatology 29:1262-1271.
40. Restrepo-Hartwig, M. A., and P. Ahlquist. 1996. Brome mosaic virus helicase- and polymerase-like proteins colocalize on the endoplasmic reticulum at sites of viral RNA synthesis. J. Virol. 70:8908-8916.
41. Sanderson, C. M., H. H. Wu, and D. P. Nayak. 1994. Sendai virus M protein binds independently to either the F or the HN glycoprotein in vivo. J. Virol. 68:69-76.
42. Schaad, M. C., P. E. Jensen, and J. C. Carrington. 1997. Formation of plant RNA virus replication complexes on membranes: role of an endoplasmic reticulum-targeted viral protein. EMBO J. 16:4049-4059.
43. Scherer, P. E., R. Y. Lewis, D. Volonte, J. A. Engelman, F. Galbiati, J. Couet, D. S. Kohtz, E. van Donselaar, P. Peters, and M. P. Lisanti. 1997. Cell-type and tissue-specific expression of caveolin-2. J. Biol. Chem. 272:29337-29346.
44. Schmidt-Mende, J., E. Bieck, T. Hugle, F. Penin, C. M. Rice, H. E. Blum, and D. Moradpour. 2001. Determinants for membrane association of the hepatitis C virus RNA-dependent RNA polymerase. J. Biol. Chem. 276:44052-44063.
45. Selby, M. J., Q. L. Choo, K. Berger, G. Kuo, E. Glazer, M. Eckart, C. Lee, D. Chien, C. Kuo, and M. Houghton. 1993. Expression, identification and subcellular localization of the proteins encoded by the hepatitis C viral genome. J. Gen. Virol. 74:1103-1113.
46. Shi, S. T., S. J. Polyak, H. Tu, D. R. Taylor, D. R. Gretch, and M. M. Lai. 2002. Hepatitis C virus NS5A colocalizes with the core protein on lipid droplets and interacts with apolipoproteins. Virology 292:198-210.
47. Shi, S. T., J. J. Schiller, A. Kanjanahaluethai, S. C. Baker, J. W. Oh, and M. M. Lai. 1999. Colocalization and membrane association of murine hepatitis virus gene 1 products and de novo-synthesized viral RNA in infected cells. J. Virol. 73:5957-5969.
48. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature 387:569-572.
49. Simons, K., and D. Toomre. 2000. Lipid rafts and signal transduction. Nat. Rev. Mol. Cell. Biol. 1:31-39.
50. Smart, E. J., G. A. Graf, M. A. McNiven, W. C. Sessa, J. A. Engelman, P. E. Scherer, T. Okamoto, and M. P. Lisanti. 1999. Caveolins, liquid-ordered domains, and signal transduction. Mol. Cell. Biol. 19:7289-7304.
51. 2+ stores during phagocytosis in human neutrophils. Science 265:1439-1441.
52. Tu, H., L. Gao, S. T. Shi, D. R. Taylor, T. Yang, A. K. Mitchell, Y. Wen, A. E. Gorbalenya, S. B. Hwang, and M. M. Lai. 1999. Hepatitis C virus RNA polymerase and NS5A complex with a SNARE-like protein. Virology 263:30-41.
53. van der Meer, Y., E. J. Snijder, J. C. Dobbe, S. Schleich, M. R. Denison, W. J. Spaan, and J. K. Locker. 1999. Localization of mouse hepatitis virus non-structural proteins and RNA synthesis indicates a role for late endosomes in viral replication. J. Virol. 73:7641-7657.
54. van der Meer, Y., H. van Tol, J. K. Locker, and E. J. Snijder. 1998. ORF1a-encoded replicase subunits are involved in the membrane association of the arterivirus replication complex. J. Virol. 72:6689-6698.
55. van Meer, G. 2001. Caveolin, cholesterol, and lipid droplets? J. Cell Biol. 152:F29-F34.
56. Wengler, G., T. Nowak, and E. Castle. 1990. Description of a procedure which allows isolation of viral nonstructural proteins from BHK vertebrate cells infected with the West Nile flavivirus in a state which allows their direct chemical characterization. Virology 177:795-801.
57. Westaway, E. G., A. A. Khromykh, and J. M. Mackenzie. 1999. Nascent flavivirus RNA colocalized in situ with double-stranded RNA in stable replication complexes. Virology 258:108-117.
58. Westaway, E. G., J. M. Mackenzie, M. T. Kenney, M. K. Jones, and A. A. Khromykh. 1997. Ultrastructure of Kunjin virus-infected cells: colocalization of NS1 and NS3 with double-stranded RNA, and of NS2B with NS3, in virus-induced membrane structures. J. Virol. 71:6650-6661.
59. Wolk, B., D. Sansonno, H. G. Krausslich, F. Dammacco, C. M. Rice, H. E. Blum, and D. Moradpour. 2000. Subcellular localization, stability, and transcleavage competence of the hepatitis C virus NS3-NS4A complex expressed in tetracycline-regulated cell lines. J. Virol. 74:2293-2304.