Replication of hepatitis C virus RNA occurs in a membrane-bound replication complex containing nonstructural viral proteins and RNA

Journal of General Virology

Volumn 84, Issue 10, 2003, Pages 2761-2769

  El Hage, Nazira ^a   Luo, Guangxiang ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; CALNEXIN; DETERGENT; MEMBRANE PROTEIN; RIBONUCLEASE; URIDINE DERIVATIVE; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; CANCER CELL CULTURE; CELL FRACTIONATION; CELL MEMBRANE; CELL NUCLEUS; COMPLEX FORMATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HEPATITIS C VIRUS; HEPATOMA CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INTRACELLULAR SPACE; ISOTOPE LABELING; MEMBRANE BINDING; MEMBRANE DAMAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RNA REPLICATION; RNA SYNTHESIS; VIRUS GENOME; VIRUS IDENTIFICATION; WESTERN BLOTTING;

CELL MEMBRANE; ENDOPLASMIC RETICULUM; HEPACIVIRUS; HUMANS; REPLICON; RNA, VIRAL; TUMOR CELLS, CULTURED; VIRAL NONSTRUCTURAL PROTEINS; VIRUS ASSEMBLY; VIRUS REPLICATION;

HEPATITIS C VIRUS; RNA VIRUSES;

EID: 0141507081     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.19305-0     Document Type: Article

References (53)

1. Banerjee, R. & Dasgupta, A. (2001). Specific interaction of hepatitis C virus protease/helicase NS3 with the 3′-terminal sequences of viral positive- and negative-strand RNA. J Virol 75, 1708-1721.
2. Bartenschlager, R., Ahlborn-Laake, L., Mous, J. & Jacobsen, H. (1993). Nonstructural protein 3 of the hepatitis C virus encodes a serine-type proteinase required for cleavage at the NS3/4 and NS4/5 junctions. J Virol 67, 3835-3844.
3. Bartenschlager, R., Ahlborn-Laake, L., Mous, J. & Jacobsen, H. (1994). Kinetic and structural analyses of hepatitis C virus polyprotein processing. J Virol 68, 5045-5055.
4. Bartenschlager, R., Lohmann, V., Wilkinson, T. & Koch, J. O. (1995). Complex formation between the NS3 serine-type proteinase of the hepatitis C virus and NS4A and its importance for polyprotein maturation. J Virol 69, 7519-7528.
5. Behrens, S. E., Tomei, L. & De Francesco, R. (1996). Identification and properties of the RNA-dependent RNA polymerase of hepatitis C virus. EMBO J 15, 12-22.
6. Blight, K. J., Kolykhalov, A. A. & Rice, C. M. (2000). Efficient initiation of HCV RNA replication in cell culture. Science 290, 1972-1974.
7. Brass, V., Bieck, E., Montserret, R., Wolk, B., Hellings, J. A., Blum, H. E., Penin, F. & Moradpour, D. (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. Bukh, J., Pietschmann, T., Lohmann, V. & 7 other authors (2002). Mutations that permit efficient replication of hepatitis C virus RNA in Huh-7 cells prevent productive replication in chimpanzees. Proc Natl Acad Sci U S A 99, 14416-14421.
9. Choo, Q. L., Kuo, G., Weiner, A. J., Overby, L. R., Bradley, D. W. & Houghton, M. (1989). Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 244, 359-362.
10. De Francesco, R. & Steinkuhler, C. (2000). Structure and function of the hepatitis C virus NS3-NS4A serine proteinase. Curr Top Microbiol Immunol 242, 149-169.
11. Egger, D., Teterina, N., Ehrenfeld, E. & Bienz, K. (2000). Formation of the poliovirus replication complex requires coupled viral translation, vesicle production, and viral RNA synthesis. J Virol 74, 6570-6580.
12. Egger, D., Wolk, B., Gosert, R., Bianchi, L., Blum, H. E., Moradpour, D. & Bienz, K. (2002). Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J Virol 76, 5974-5984.
13. Froshauer, S., Kartenbeck, J. & Helenius, A. (1988). Alphavirus RNA replicase is located on the cytoplasmic surface of endosomes and lysosomes. J Cell Biol 107, 2075-2086.
14. Gontarek, R. R., Gutshall, L. L., Herold, K. M., Tsai, J., Sathe, G. M., Mao, J., Prescott, C. & Del Vecchio, A. M. (1999). hnRNP C and polypyrimidine tract-binding protein specifically interact with the pyrimidine-rich region within the 3′NTR of the HCV RNA genome. Nucleic Acids Res 27, 1457-1463.
15. Gosert, R., Egger, D., Lohmann, V., Bartenschlager, R., Blum, H. E., Bienz, K. & Moradpour, D. (2003). Identification of the hepatitis C virus RNA replication complex in Huh-7 cells harboring subgenomic replicons. J Virol 77, 5487-5492.
16. Grakoui, A., McCourt, D. W., Wychowski, C., Feinstone, S. M. & Rice, C. M. (1993). A second hepatitis C virus-encoded proteinase. Proc Natl Acad Sci U S A 90, 10583-10587.
17. Guo, J. T., Bichko, V. V. & Seeger, C. (2001). Effect of alpha interferon on the hepatitis C virus replicon. J Virol 75, 8516-8523.
18. Hardy, R. W., Marcotrigiano, J., Blight, K. J., Majors, J. E. & Rice, C. M. (2003). Hepatitis C virus RNA synthesis in a cell-free system isolated from replicon-containing hepatoma cells. J Virol 77, 2029-2037.
19. Haukenes, G. & Kalland, H.-H. (1998). Visualisation of ribosomal RNA (rRNA) synthesis in eukaryotic cells in culture. Methods Cell Sci 19, 295-302.
20. Hijikata, M., Kato, N., Ootsuyama, Y., Nakagawa, M. & Shimotohno, K. (1991). Gene mapping of the putative structural region of the hepatitis C virus genome by in vitro processing analysis. Proc Natl Acad Sci U S A 88, 5547-5551.
21. Hugle, T., Fehrmann, F., Bieck, E., Kohara, M., Krausslich, H. G., Rice, C. M., Blum, H. E. & Moradpour, D. (2001). The hepatitis C virus nonstructural protein 4B is an integral endoplasmic reticulum membrane protein. Virology 284, 70-81.
22. Hwang, S. B., Park, K. J., Kim, Y. S., Sung, Y. C. & Lai, M. M. (1997). Hepatitis C virus NS5B protein is a membrane-associated phosphoprotein with a predominantly perinuclear localization. Virology 227, 439-446.
23. Ikeda, M., Yi, M., Li, K. & Lemon, S. M. (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.
24. Ishido, S., Fujita, T. & Hotta, H. (1998). Complex formation of NS5B with NS3 and NS4A proteins of hepatitis C virus. Biochem Biophys Res Commun 244, 35-40.
25. Ito, T. & Lai, M. M. (1997). Determination of the secondary structure of and cellular protein binding to the 3′-untranslated region of the hepatitis C virus RNA genome. J Virol 71, 8698-8706.
26. Lai, V. C., Dempsey, S., Lau, J. Y., Hong, Z. & Zhong, W. (2003). In vitro RNA replication directed by replicase complexes isolated from the subgenomic replicon cells of hepatitis C virus. J Virol 77, 2295-2300.
27. Lin, C., Lindenbach, B. D., Pragai, B. M., McCourt, D. W. & Rice, C. M. (1994). Processing in the hepatitis C virus E2-NS2 region: identification of p7 and two distinct E2-specific products with different C termini. J Virol 68, 5063-5073.
28. Lin, C., Wu, J. W., Hsiao, K. & Su, M. S. (1997). The hepatitis C virus NS4A protein: interactions with the NS4B and NS5A proteins. J Virol 71, 6465-6471.
29. Lohmann, V., Korner, F., Herian, U. & Bartenschlager, R. (1997). Biochemical properties of hepatitis C virus NS5B RNA-dependent RNA polymerase and identification of amino acid sequence motifs essential for enzymatic activity. J Virol 71, 8416-8428.
30. Lohmann, V., Korner, F., Koch, J., Herian, U., Theilmann, L. & Bartenschlager, R. (1999a). Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285, 110-113.
31. Lohmann, V., Overton, H. & Bartenschlager, R. (1999b). Selective stimulation of hepatitis C virus and pestivirus NS5B RNA polymerase activity by GTP. J Biol Chem 274, 10807-10815.
32. Lohmann, V., Korner, F., Dobierzewska, A. & Bartenschlager, R. (2001). Mutations in hepatitis C virus RNAs conferring cell culture adaptation. J Virol 75, 1437-1449.
33. Luo, G. (1999). Cellular proteins bind to the poly(U) tract of the 3′ untranslated region of hepatitis C virus RNA genome. Virology 256, 105-118.
34. Luo, G., Hamatake, R. K., Mathis, D. M., Racela, J., Rigat, K. L., Lemm, J. & Colonno, R. J. (2000). De novo initiation of RNA synthesis by the RNA-dependent RNA polymerase (NS5B) of hepatitis C virus. J Virol 74, 851-863.
35. Luo, G., Xin, S. & Cai, Z. (2003). Role of the 5′-proximal stem-loop structure of the 5′ untranslated region in replication and translation of hepatitis C virus RNA. J Virol 77, 3312-3318.
36. Mackenzie, J. M., Jones, M. K. & Young, P. R. (1996). Immunolocalization of the dengue virus nonstructural glycoprotein NS1 suggests a role in viral RNA replication. Virology 220, 232-240.
37. Mottola, G., Cardinali, G., Ceccacci, A., Trozzi, C., Bartholomew, L., Torrisi, M. R., Pedrazzini, E., Bonatti, S. & Migliaccio, G. (2002). Hepatitis C virus nonstructural proteins are localized in a modified endoplasmic reticulum of cells expressing viral subgenomic replicons. Virology 293, 31-43.
38. Oh, J. W., Ito, T. & Lai, M. M. (1999). A recombinant hepatitis C virus RNA-dependent RNA polymerase capable of copying the full-length viral RNA. J Virol 73, 7694-7702.
39. Petrik, J., Parker, H. & Alexander, G. J. (1999). Human hepatic glyceraldehyde-3-phosphate dehydrogenase binds to the poly(U) tract of the 3′ non-coding region of hepatitis C virus genomic RNA. J Gen Virol 80, 3109-3113.
40. Reed, K. E. & Rice, C. M. (2000). Overview of hepatitis C virus genome structure, polyprotein processing, and protein properties. Curr Top Microbiol Immunol 242, 55-84.
41. Restrepo-Hartwig, M. A. & Ahlquist, P. (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.
42. Restrepo-Hartwig, M. & Ahlquist, P. (1999). Brome mosaic virus RNA replication proteins 1a and 2a colocalize and 1a independently localizes on the yeast endoplasmic reticulum. J Virol 73, 10303-10309.
43. Rice, C. M. (1996). Flaviviridae: the viruses and their replication. In Fields Virology, 3rd edn, pp. 931-956. Edited by B. N. Fields, D. M. Knipe & P. M. Howley. Philadelphia: Lippincott-Raven.
44. Schmidt-Mende, J., Bieck, E., Hugle, T., Penin, F., Rice, C. M., Blum, H. E. & Moradpour, D. (2001). Determinants for membrane association of the hepatitis C virus RNA-dependent RNA polymerase. J Biol Chem 276, 44052-44063.
45. Schwartz, M., Chen, J., Janda, M., Sullivan, M., den Boon, J. & Ahlquist, P. (2002). A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. Mol Cell 9, 505-514.
46. Selby, M. J., Glazer, E., Masiarz, F. & Houghton, M. (1994). Complex processing and protein: protein interactions in the E2: NS2 region of HCV. Virology 204, 114-122.
47. Shi, S. T., Lee, K. J., Aizaki, H., Hwang, S. B. & Lai, M. M. (2003). Hepatitis C virus RNA replication occurs on a detergent-resistant membrane that cofractionates with caveolin-2. J Virol 77, 4160-4168.
48. Suhy, D. A., Giddings, T. H., Jr & Kirkegaard, K. (2000). Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles. J Virol 74, 8953-8965.
49. Tsuchihara, K., Tanaka, T., Hijikata, M., Kuge, S., Toyoda, H., Nomoto, A., Yamamoto, N. & Shimotohno, K. (1997). Specific interaction of polypyrimidine tract-binding protein with the extreme 3′-terminal structure of the hepatitis C virus genome, the 3′X. J Virol 71, 6720-6726.
50. Tu, H., Gao, L., Shi, S. T. & 7 other authors (1999). Hepatitis C virus RNA polymerase and NS5A complex with a SNARE-like protein. Virology 263, 30-41.
51. Wessel, D. & Flugge, U. I. (1984). A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 138, 141-143.
52. Westaway, E. G., Mackenzie, J. M., Kenney, M. T., Jones, M. K. & Khromykh, A. A. (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.
53. Westaway, E. G., Khromykh, A. A. & Mackenzie, J. M. (1999). Nascent flavivirus RNA colocalized in situ with double-stranded RNA in stable replication complexes. Virology 258, 108-117.