Antiviral effect and virus-host interactions in response to alpha interferon, gamma interferon, poly(I)-poly(C), tumor necrosis factor alpha, and ribavirin in hepatitis C virus subgenomic replicons

Journal of Virology

Volumn 77, Issue 2, 2003, Pages 1092-1104

  Lanford, Robert E ^a   Guerra, Bernadette ^a   Lee, Helen ^a   Averett, Devron R ^b   Pfeiffer, Brad ^a   Chavez, Deborah ^a   Notvall, Lena ^a   Bigger, Catherine ^a  

^a SOUTHWEST NATIONAL PRIMATE RESEARCH CENTER   (United States)

^b F HOFFMANN LA ROCHE LTD   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ANTIVIRUS AGENT; DOUBLE STRANDED RNA; GAMMA INTERFERON; RIBAVIRIN; TUMOR NECROSIS FACTOR ALPHA;

ANTIVIRAL ACTIVITY; ARTICLE; CELL LINE; CLONING; COLONY FORMATION; CONTROLLED STUDY; DRUG EFFECT; GENE ACTIVATION; GENE CONSTRUCT; GENE MUTATION; GENOTYPE; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; LIVER CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REPLICON; VIRUS CELL INTERACTION; VIRUS STRAIN;

AMINO ACID SEQUENCE; ANTIVIRAL AGENTS; CELL LINE; GENOME, VIRAL; GENOTYPE; HEPACIVIRUS; INTERFERON TYPE II; INTERFERON-ALPHA; MOLECULAR SEQUENCE DATA; MUTATION; POLY I-C; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBAVIRIN; RNA, VIRAL; SEQUENCE HOMOLOGY, AMINO ACID; TUMOR NECROSIS FACTOR-ALPHA; VIRAL NONSTRUCTURAL PROTEINS;

EID: 0037228023     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.2.1092-1104.2003     Document Type: Article

References (68)

1. Alter, H. J., and M. Houghton. 2000. Hepatitis C virus and eliminating post-transfusion hepatitis. Nat. Med. 6:1082-1086.
2. Alter, H. J., and L. B. Seeff. 2000. Recovery, persistence, and sequelae in hepatitis C virus infection: A perspective on long-term outcome. Semin. Liver Dis. 20:17-35.
3. Alter, M. J., D. Kruszon-Moran, O. V. Nainan, G. M. McQuillan, F. X. Gao, L. A. Moyer, R. A. Kaslow, and H. S. Margolis. 1999. The prevalence of hepatitis C virus infection in the United States, 1988 through 1994. N. Engl. J. Med. 341:556-562.
4. Bandyopadhyay, S. K., G. T. Leonard, Jr., T. Bandyopadhyay, G. R. Stark, and G. C. Sen. 1995. Transcriptional induction by double-stranded RNA is mediated by interferon-stimulated response elements without activation of interferon-stimulated gene factor 3. J. Biol. Chem. 270:19624-19629.
5. Bartenschlager, R., and V. Lohmann. 2000. Replication of hepatitis C virus. J. Gen. Virol. 81:1631-1648.
6. Beard, M. R., G. Abell, M. Honda, A. Carroll, M. Gartland, B. Clarke, K. Suzuki, R. Lanford, D. V. Sangar, and S. M. Lemon. 1999. An infectious molecular clone of a Japanese genotype 1b hepatitis C virus. Hepatology 30:316-324.
7. Bigger, C. B., K. M. Brasky, and R. E. Lanford. 2001. DNA microarray analysis of chimpanzee liver during acute resolving hepatitis C virus infection. J. Virol. 75:7059-7066.
8. Blight, K. J., A. A. Kolykhalov, and C. M. Rice. 2000. Efficient initiation of HCV RNA replication in cell culture. Science 290:1972-1974.
9. Bodenheimer, H. C., Jr., K. L. Lindsay, G. L. Davis, J. H. Lewis, S. N. Thung, and L. B. Seeff. 1997. Tolerance and efficacy of oral ribavirin treatment of chronic hepatitis C: A multicenter trial. Hepatology 26:473-477.
10. Boehm, U., T. Klamp, M. Groot, and J. Howard. 1997. Cellular responses to interferon-γ. Annu. Rev. Immunol. 15:749-795.
11. Choo, Q.-L., G. Kuo, A. J. Weiner, L. J. Overby, D. W. Bradley, and M. Houghton. 1989. Isolation of a cDNA clone derived from blood-borne non-A, non-B viral hepatitis genome. Science 244:359-362.
12. Conry-Cantilena, C., M. VanRaden, J. Gibble, J. Melpolder, A. O. Shakil, L. Viladomiu, L. Cheung, A. DiBisceglie, J. Hoofnagle, J. W. Shih, R. Kaslow, P. Ness, and H. J. Alter. 1996. Routes of infection, viremia, and liver disease in blood donors found to have hepatitis C virus infection. N. Engl. J. Med. 334:1691-1696.
13. Crotty, S., C. E. Cameron, and R. Andino. 2001. RNA virus error catastrophe: Direct molecular test by using ribavirin. Proc. Natl. Acad. Sci. USA 98:6895-6900.
14. De Clercq, E. 1993. Antiviral agents: characteristic activity spectrum depending on the molecular target with which they interact. Adv. Virus Res. 42:1-55.
15. Der, S. D., A. Zhou, B. R. Williams, and R. H. Silverman. 1998. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc. Natl. Acad. Sci. USA 95:15623-15628.
16. Dusheiko, G., J. Main, H. Thomas, O. Reichard, C. Lee, A. Dhillon, S. Rassam, A. Fryden, H. Reesink, M. Bassendine, G. Norkrans, T. Cuypers, N. Lelie, P. Telfer, J. Watson, C. Weegink, P. Sillikens, and O. Weiland. 1996. Ribavirin treatment for patients with chronic hepatitis C: Results of a placebo-controlled study. J. Hepatol. 25:591-598.
17. Enomoto, N., I. Sakuma, Y. Asahina, M. Kurosaki, T. Murakami, C. Yamamoto, and N. Izumi. 1996. Interferon sensitivity determining sequence of the hepatitis C virus genome. Hepatology 24:460-461.
18. Enria, D. A., and J. I. Maiztegui. 1994. Antiviral treatment of argentine hemorrhagic fever. Antiviral Res. 23:23-31.
19. Fang, S. H., L. H. Hwang, D. S. Chen, and B. L. Chiang. 2000. Ribavirin enhancement of hepatitis C virus core antigen-specific type 1 T helper cell response correlates with the increased IL-12 level. J. Hepatol. 33:791-798.
20. Frese, M., T. Pietschmann, D. Moradpour, O. Haller, and R. Bartenschlager. 2001. Interferon-α inhibits hepatitis C virus subgenomic RNA replication by an MxA-independent pathway. J. Gen. Virol. 82:723-733.
21. Frese, M., V. Schwarzle, K. Barth, N. Krieger, V. Lohmann, S. Mihm, O. Haller, and R. Bartenschlager. 2002. Interferon-gamma inhibits replication of subgenomic and genomic hepatitis C virus RNAs. Hepatology 35:694-703.
22. Gale, M., C. M. Blakely, B. Kwieciszewski, S. L. Tan, M. Dossett, N. M. Tang, M. J. Korth, S. J. Polyak, D. R. Gretch, and M. G. Katze. 1998. Control of PKR protein kinase by hepatitis C virus nonstructural 5A protein: Molecular mechanisms of kinase regulation. Mol. Cell. Biol. 18:5208-5218.
23. Gale, M. J., M. J. Korth, N. M. Tang, S. L. Tan, D. A. Hopkins, T. E. Dever, S. J. Polyak, D. R. Gretch, and M. G. Katze. 1997. Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by the nonstructural 5A protein. Virology 230:217-227.
24. Geiss, G., G. Jin, J. Guo, R. Bumgarner, M. G. Katze, and G. Sen. 2001. A comprehensive view of regulation of gene expression by double-stranded RNA-mediated cell signaling. J. Biol. Chem. 276:30178-30182.
25. Girard, S., P. Shalhoub, P. Lescure, A. Sabile, D. E. Misek, S. Hanash, C. Brechot, and L. Beretta. 2002. An altered cellular response to interferon and up-regulation of interleukin-8 induced by the hepatitis C viral protein NS5A uncovered by microarray analysis. Virology 295:272-283.
26. Guidotti, L. G., A. Morris, H. Mendez, R. Koch, R. H. Silverman, B. R. G. Williams, and F. V. Chisari. 2002. Interferon-regulated pathways that control hepatitis B virus replication in transgenic mice. J. Virol. 76:2617-2621.
27. Guo, J. T., V. Bichko, and C. Seeger. 2001. Effect of alpha interferon on the hepatitis C virus replicon. J. Virol. 75:8516-8523.
28. Honda, M., M. R. Beard, L. H. Ping, and S. M. Lemon. 1999. A phylogenetically conserved stem-loop structure at the 5′ border of the internal ribosome entry site of hepatitis C virus is required for cap-independent viral translation. J. Virol. 73:1165-1174.
29. Huggins, J. W., C. M. Hsiang, T. M. Cosgriff, J. Y. Guang, J. I. Smith, Z. O. Wu, J. W. DeDuc, Z. M. Zheng, J. M. Meegan, Q. N. Wang, D. D. Oland, X. E. Gui, P. H. Gibbs, G. H. Yuan, and T. M. Zhang. 1991. Prospective, double-blind, concurrent, placebo-controlled clinical trial of intravenous ribavirin therapy of hemorrhagic fever with renal syndrome. J. Infect. Dis. 164:1119-1127.
30. Hultgren, C., D. R. Milich, O. Weiland, and M. Siillberg. 1998. The antiviral compound ribavirin modulates the T helper (Th)1/Th2 subset balance in hepatitis B and C virus-specific immune responses. J. Gen. Virol. 79:2381-2391.
31. Hummer, B. T., X. L. Li, and B. A. Hassel. 2001. Role for p53 in gene induction by double-stranded RNA. J. Virol. 75:7774-7777.
32. Ikeda, M., M. K. Yi, K. Li, and S. A. 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.
33. Jaeckel, E., M. Cornberg, H. Wedemeyer, T. Santantonio, J. Mayer, M. Zankel, G. Pastore, M. Dietrich, C. Trautwein, and M. Manns. 2001. Treatment of acute hepatitis C with interferon alpha-2b. N. Engl. J. Med. 345:1-6.
34. Kilgore, P. E., T. G. Ksiazek, P. E. Rollin, J. N. Mills, M. R. Villagra, M. J. Montenegro, M. A. Costales, L. C. Paredes, and C. J. Peters. 1997. Treatment of bolivian hemorrhagic fever with intravenous ribavirin. Clin. Infect. Dis. 24:718-722.
35. Krieger, N., V. Lohmann, and R. Bartenschlager. 2001. Enhancement of hepatitis C virus RNA replication by cell culture-adaptive mutations. J. Virol. 75:4614-4624.
36. Kumar, A., Y. L Yang, V. Flati, S. Der, S. Kadereit, A. Deb, J. Haque, L. Reis, C. Weissmann, and B. R. Williams. 1997. Deficient cytokine signaling in mouse embryo fibroblasts with a targeted deletion in the PKR gene: Role of IRF-1 and NF-κB. EMBO J. 16:406-416.
37. Lanford, R. E., and C. Bigger. 2002. Advances in model systems for hepatitis C virus research. Virology 293:1-9.
38. Lanford, R. E., D. Chavez, B. Guerra, J. Y. N. Lau, Z. Hong, K. M. Brasky, and B. Beames. 2001. Ribavirin induces error-prone replication of GB virus B in primary tamarin hepatocytes. J. Virol. 75:8074-8081.
39. Lanford, R. E., and L. E. Estlack. 1998. A cultivation method for highly differentiated primary chimpanzee hepatocytes permissive for hepatitis C virus replication. Methods Mol. Med. 19:501-516.
40. Lanford, R. E., H. Lee, D. Chavez, B. Guerra, and K. M. Brasky. 2001. Infectious cDNA clone of the hepatitis C virus genotype 1 prototype sequence. J. Gen. Virol. 82:1291-1297.
41. Lau, J. Y., R. C. Tam, T. J. Liang, and Z. Hong. 2002. Mechanism of action of ribavirin in the combination treatment of chronic HCV infection. Hepatology 35:1002-1009.
42. Lohmann, V., F. Korner, A. Dobierzewska, and R. Bartenschlager. 2001. Mutations in hepatitis C virus RNAs conferring cell culture adaptation. J. Virol. 75:1437-1449.
43. Lohmann, V., F. Körner, J. O. 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.
44. Maag, D., C. Castro, Z. Hong, and C. E. Cameron. 2001. Hepatitis C virus RNA-dependent RNA polymerase (NS5B) as a mediator of the antiviral activity of ribavirin. J. Biol. Chem. 276:46094-46098.
45. Manns, M. P., J. G. McHutchison, S. C. Gordon, V. K. Rustgi, M. Shiffman, R. Reindollar, Z. D. Goodman, M. H. Ling, and J. K. Albrecht. 2001. Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for initial treatment of chronic hepatitis C: A randomised trial. Lancet 358:958-965.
46. Marcus, P. I., and M. J. Sekellick. 2001. Combined sequential treatment with interferon and dsRNA abrogates virus resistance to interferon action. J. Interferon Cytokine Res. 21:423-429.
47. Markland, W., T. J. McQuaid, J. Jain, and A. D. Kwong. 2000. Broadspectrum antiviral activity of the IMP dehydrogenase inhibitor VX-497: a comparison with ribavirin and demonstration of antiviral additivity with alpha interferon. Antimicrob. Agents Chemother. 44:859-866.
48. McCormick, J. B., I. J. King, P. A. Webb, C. L. Scribner, R. B. Craven, K. M. Johnson, L. H. Elliott, and R. Belmont-Williams. 1986. Lassa fever/Effective therapy with ribavirin. N. Engl. J. Med. 314:20-26.
49. Melen, K., P. Keskinen, A. Lehtonen, and I. Julkunen. 2000. Interferon-induced gene expression and signaling in human hepatoma cell lines. J. Hepatol. 33:764-772.
50. Ning, Q., D. Brown, J. Parodo, M. Cattral, R. Gorczynski, E. Cole, L. Fung, J. W. Ding, M. F. Liu, O. Rotstein, M. J. Phillips, and G. Levy. 1998. Ribavirin inhibits viral-induced macrophage production of TNF, IL-1, the procoagulant fg12 prothrombinase and preserves Th1 cytokine production but inhibits Th2 cytokine response. J. Immunol. 160:3487-3493.
51. Pavio, N., D. R. Taylor, and M. M. C. Lai. 2002. Detection of a novel unglycosylated form of hepatitis C virus E2 envelope protein that is located in the cytosol and interacts with PKR. J. Virol. 76:1265-1272.
52. Pflugheber, J., B. Fredericksen, R. Sumpter, Jr., C. Wang, F. Ware, D. L. Sodora, and M. Gale, Jr. 2002. Regulation of PKR and IRF-1 during hepatitis C virus RNA replication. Proc. Natl. Acad. Sci. USA 99:4650-4655.
53. Pietschmann, T., V. Lohmann, A. Kaul, N. Krieger, G. Rinck, G. Rutter, D. Strand, and R. Bartenschlager. 2002. Persistent and transient replication of full-length hepatitis C virus genomes in cell culture. J. Virol. 76:4008-4021.
54. Podevin, P., A. Sabile, R. Gajardo, N. Delhem, A. Abadie, P. Y. Lozach, L. Beretta, and C. Brechot. 2001. Expression of hepatitis C virus NS5A natural mutants in a hepatocytic cell line inhibits the antiviral effect of interferon in a PKR-independent manner. Hepatology 33:1503-1511.
55. Polyak, S. J., K. S. A. Khabar, D. M. Paschal, H. J. Ezelle, G. Duverlie, G. N. Barber, D. E. Levy, N. Mukaida, and D. R. Gretch. 2001. Hepatitis C virus nonstructural 5A protein induces interleukin-8, leading to partial inhibition of the interferon-induced antiviral response. J. Virol. 75:6095-6106.
56. Reed, K. E., and C. M. Rice. 1998. Molecular characterization of hepatitis C virus. Curr. Stud. Hematol. Blood Transfus. 62:1-37.
57. Samuel, C. E. 2001. Antiviral actions of interferons. Clin. Microbiol. Rev. 14:778-809.
58. Sidwell, R. W., J. H. Huffman, G. P. Khare, L. B. Allen, J. T. Witkowski, and R. K. Robins. 1972. Broad-spectrum antiviral activity of virazole: 1-β-D-ribofuranosyl-1,2,4-triazole-3-carboxamide. Science 177:705-706.
59. Stark, G. R., I. M. Kerr, B. R. Williams, R. H. Silverman, and R. D. Schreiber. 1998. How cells respond to interferons. Annu. Rev. Biochem. 67:227-264.
60. Tam, R. C., B. Pai, J. Bard, C. Lim, D. R. Averett, U. T. Phan, and T. Milovanovic. 1999. Ribavirin polarizes human T cell responses towards a type 1 cytokine profile. J. Hepatol. 30:376-382.
61. Tan, S. L., and M. G. Katze. 2001. How hepatitis C virus counteracts the interferon response: The jury is still out on NS5A. Virology 284:1-12.
62. Tan, S. L, H. Nakao, Y. He, S. Vijaysri, P. Neddermann, B. L. Jacobs, B. J. Mayer, and M. G. Katze. 1999. NS5A, a nonstructural protein of hepatitis C virus, binds growth factor receptor-bound protein 2 adaptor protein in a Src homology 3 domain/ligand-dependent manner and perturbs mitogenic signaling. Proc. Natl. Acad. Sci. USA 96:5533-5538.
63. Taniguchi, T., and A. Takaoka. 2001. A weak signal for strong responses: Interferon-alpha/beta revisited. Nat. Rev. Mol. Cell Biol. 2:378-386.
64. Tanji, Y., T. Kaneko, S. Satoh, and K. Shimotohno. 1995. Phosphorylation of hepatitis C virus-encoded nonstructural protein NS5A. J. Virol. 69:3980-3986.
65. Taylor, D. R., S. T. Shi, P. R. Romano, G. N. Barber, and M. M. Lai. 1999. Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein. Science 285:107-110.
66. Tu, H., L. Gao, S. T. Shi, D. R. Taylor, T. Yang, A. K. Mircheff, Y. M. 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.
67. Weaver, B. K., K. P. Kumar, and N. C. Reich. 1998. Interferon regulatory factor 3 and CREB-binding protein/p300 are subunits of double-stranded RNA-activated transcription factor DRAF1. Mol. Cell, Biol. 18:1359-1368.
68. Yang, Y. L., L. F. Reis, J. Pavlovic, A. Aguzzi, R. Schafer, A. Kumar, B. R. Williams, M. Aguet, and C. Weissmann. 1995. Deficient signaling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO J. 14:6095-6106.