Isolation and gene analysis of interferon α-resistant cell clones of the hepatitis C virus subgenome

Virology

Volumn 375, Issue 2, 2008, Pages 424-432

  Noguchi, Tohru ^a,b   Otsubaki, Tomoko ^a   Ando, Izuru ^a   Ogura, Naoki ^a   Ikeda, Satoru ^a   Shimotohno, Kunitada ^b  

^a JAPAN TOBACCO INC   (Japan)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

Hepatitis C virus; Interferon resistance; Nonstructural protein NS5A; Replicon; Stat 1

Indexed keywords

ALPHA INTERFERON; STAT1 PROTEIN;

ARTICLE; CELL CLONE; CONTROLLED STUDY; GENE MUTATION; GENE SEQUENCE; GENETIC ANALYSIS; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; VIRUS REPLICATION;

CELL LINE, TUMOR; CLONE CELLS; DRUG RESISTANCE, VIRAL; GENES, VIRAL; HEPACIVIRUS; HUMANS; INTERFERON-ALPHA; MUTATION; PHOSPHORYLATION; REPLICON; RNA, VIRAL; STAT1 TRANSCRIPTION FACTOR; TRANSFECTION; VIRAL NONSTRUCTURAL PROTEINS;

HEPATITIS C VIRUS;

EID: 43249114794     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2008.02.009     Document Type: Article

References (51)

1. Alter M.J. Epidemiology of hepatitis C. Hepatology 26 (1997) 62S-65S
2. Appel N., Pietschmann T., and Bartenschlager R. Mutational analysis of hepatitis C virus nonstructural protein 5A: potential role of differential phosphorylation in RNA replication and identification of a genetically flexible domain. J. Virol. 79 (2005) 3187-3194
3. Asabe S., Tanji Y., Satoh S., Kaneko T., Kimura K., and Shimotohno K. The N-terminal region of hepatitis C virus-encoded NS5A is important for NS4A dependent phosphorylation. J. Virol. 71 (1997) 790-796
4. Bartenschlager R., and Lohmann V. Replication of hepatitis C virus. J. Gen. Virol. 81 (2000) 1631-1648
5. Bartenschlager R., and Lohmann V. Novel cell culture systems for the hepatitis C virus. Antivir. Res. 52 (2001) 1-17
6. Choo Q.I., Richman K.H., Han J.H., Berger K., Lee C., Dong C., Gallegos C., Coit D., Medina S.R., Barr P.J., Weiner A.J., Bradely D.W., Kuo G., and Houghton M. Genetic organization and diversity of the hepatitis C virus. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 2451-2455
7. Enomoto N., Sakuma I., Asahina Y., Kurosaki M., Murakami T., Yamamoto C., Ogura Y., Izumi N., Marumo F., and Sato C. Mutations in the nonstructural protein 5A gene and response to interferon I patients with chronic hepatitis C virus 1b infection. N. Engl. J. Med. 334 (1996) 77-81
8. Evans M.J., Rice C.M., and Goff S.P. Phosphorylation of hepatitis C virus nonstructural protein 5A modulates its protein interactions and viral RNA replication. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 13038-13043
9. Frese M., Schwärzle V., Barth K., Krieger N., Lohmann V., Mihm S., Haller O., and Bartenschlager R. Interferon-γ inhibits replication of subgenomic and genomic hepatitis C virus RNAs. Hepatology 35 (2002) 694-703
10. Gale M.J., Korth M.J., Tang N.M., Tan S.L., Hopkins D.A., Dever T.E., Polyak S.J., Gretch D.R., and Katze M.G. Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by nonstructural 5A protein. Virology 230 (1997) 217-227
11. Gong G.Z., Cao J., Jiang Y.F., Zhou Y., and Liu B. Hepatitis C virus non-structural 5A abrogates signal transducer and activator of transcription-1 nuclear translocation induced by IFN-alpha through dephosphorylation. World Gastroenterol. 13 (2007) 4080-4084
12. Guo J.T., Bichko V.V., and Seeger C. Effect of alpha interferon on the hepatitis C virus replicon. J. Virol. 75 (2001) 8516-8523
13. Guo J.T., Sohn J.A., Zhu Q., and Seeger C. Mechanism of the interferon alpha response against hepatitis C virus replicons. Virology 325 (2004) 71-81
14. Hijikata M., Kato N., Ootsuyama Y., Nakagawa M., and Shimotohno K. 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 (1991) 5547-5551
15. Hijikata M., Mizushima H., Tanji Y., Komoda Y., Hirowatari Y., Akagi N., Kato N., Kimura K., and Shimotohno K. Proteolytic processing and membrane association of putative nonstructural proteins of hepatitis C virus. Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 10773-10777
16. Hijikata M., Mizushima H., Tanji Y., Komoda Y., Hirowatari Y., Akagi N., Kato N., Kimura K., and Shimotohno K. Two distinct proteinase activities required for the processing of a putative nonstructural precursor protein of hepatitis C virus. J. Virol. 67 (1993) 4665-4675
17. Hirashima S., Suzuki T., Ishida T., Noji S., Yata S., Ando I., Komatsu M., Ikeda S., and Hashimoto H. Benzimidazole derivatives bearing substituted biphenyls as hepatitis C virus NS5B RNA-dependent RNA polymerase inhibitors: structure-activity relationship studies and identification of a potent and highly selective inhibitor JTK-109. J. Med. Chem. 49 (2006) 4721-4736
18. Houghton M. Hepatitis C viruses, p1035-1058. In: Fields B.N., Knipe D.M., and Howley P.M. (Eds). Fields Virology. 3rd ed (1996), Lippincott-Raven Co., Philadelphia
19. Huang Y., Chen X.C., Konduri M., Fomina N., Lu J., Jin L., Kolykhalov A., and Tan S.L. Mechanistic link between the anti-HCV effect of interferon gamma and control of viral replication by a Ras-MAPK signaling cascade. Hepatology 43 (2006) 81-90
20. Ide Y., Tanimoto A., Sasaguri Y., and Padmanabhan R. Hepatitis C virus NS5A protein is phosphorylated in vitro by a stably bound protein kinase from HeLa cells and by cAMP-dependent protein kinase A-a catalytic subunit. Gene 201 (1997) 151-158
21. Ishida T., Suzuki T., Hirashima S., Mizutani K., Yoshida A., Ando I., Ikeda S., Adachi T., and Hashimoto H. Benzimidazole inhibitors of hepatitis C virus NS5B polymerase: identification of 2-[(4-diarylmethoxy) phenyl]-benzimidazole. Bioorg. Med. Chem. Lett. 16 (2006) 1859-1863
22. Kaneko T., Tanji Y., Satoh S., Hijikata M., Asabe S., Kimura K., and Shimotohno K. Production of two phosphoproteins from the NS5A region of the hepatitis C virus genome. Biochem. Biophys. Res. Commun. 205 (1994) 320-326
23. Kato N., Hijikata M., Ootsuyama M., Nakagawa S., Ohkoshi S., Sugimura T., and Shimotohno K. Molecular cloning of the human hepatitis C virus genome from Japanese patients with non-A, non-B hepatitis. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 9524-9528
24. Kawai T., Takahashi K., Sato S., Coban C., Kumar H., Kato H., Ishii K.J., Takeuchi O., and Akira S. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 6 (2005) 1074-1076
25. Kim J., Lee D., and Choe J. Hepatitis C virus NS5A protein is phosphorylated by casein kinase II. Biochem. Biophys. Res. Commun. 257 (1999) 777-781
26. Lan K.H., Lan K.L., Lee W.P., Sheu M.L., Chen M.Y., Lee Y.L., Yen S.H., Chang F.Y., and Lee S.D. HCV NS5A inhibits interferon-alpha signaling through suppression of STAT1 phosphorylation in hepatocyte-derived cell lines. J. Hepatol. 46 (2007) 759-767
27. Lindsay K.L. Therapy of hepatitis C: overview. Hepatology 26 (1997) 71S-77S
28. Lohmann V., Körner F., Koch J., Herian U., Theilman L., and Bartenschlager R. Replication of subgenomic Hepatitis C virus RNAs in a hepatoma cell line. Science 285 (1999) 110-113
29. McHutchison J.G., Gordon S.C., Schiff E.R., Shiffman M.L., Lee W.M., Rustgi V.K., Goodman Z.D., Ling M.H., Cort S., and Albrecht J.K. Interferon alfa-2b alone or in combination with ribavirin as initial treatment for chronic hepatitis C. Hepatitis Interventional Therapy Group. N. Engl. J. Med. 339 (1998) 1485-1492
30. Meylan E., Curran J., Hofmann K., Moradpour D., Binder M., Bartenschlager R., and Tschopp J. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437 (2005) 1167-1172
31. Naka K., Takemoto K., Abe K., Dansako H., Ikeda M., Shimotohno K., and Kato N. Interferon resistance of hepatitis C virus replicon-harboring cells is caused by functional disruption of type I interferon receptors. J. Gen. Virol. 86 (2005) 2787-2792
32. Namba K., Naka K., Dansako H., Nozaki A., Ikeda M., Shiratori Y., Shimotohno K., and Kato N. Establishment of hepatitis C virus replicon cell lines possessing interferon-resistant phenotype. Biochem. Biophys. Res. Commun. 323 (2004) 299-309
33. Neddermann P., Quintavalle M., Di Pietro C., Clementi A., Cerretani M., Altamura S., Bartholomew L., and De Francesco R. Reduction of hepatitis C virus NS5A hyperphosphorylation by selective inhibition of cellular kinases activates viral RNA replication in cell culture. J. Virol. 78 (2004) 13306-13314
34. Noguchi T., Satoh S., Noshi T., Hatada E., Fukuda R., Kawai A., Ikeda S., Hijikata M., and Shimotohno K. Effects of mutation in hepatitis C virus nonstructural protein 5A on interferon resistance mediated by inhibition of PKR kinase activity in mammalian cells. Microbiol. Immunol. 45 (2001) 829-840
35. Nousbaum J., Polyak S.J., Ray S.C., Sullivan D.G., Larson A.M., Caritherns R.L., and Gretch D.R. Prospective characterization of full-length hepatitis C virus NS5A quasispecies during induction and combination antiviral therapy. J. Virol. 74 (2000) 9028-9038
36. Okamoto H., Okada S., Sugiyama Y., Kurai K., Iizuka H., Machida A., Miyakawa Y., Tsuda F., and Mayumi M. Nucleotide sequence of the genomic of hepatitis C virus isolated from a human carrier: comparison with reported isolates for conserved and divergent regions. J. Gen. Virol. 72 (1991) 2697-2704
37. Okamoto H., Kurai K., Okada S., Yamamoto K., Iizuka H., Tanaka T., Fukuda S., Tsuda F., and Mishiro S. Full-length sequence of a hepatitis C virus genome having poor homology to reported isolates: comparative study of four distinct genotypes. Virology 188 (1992) 331-341
38. Puig-Basagoiti F., Forns X., Furcic I., Ampurdanes S., Gimenez-Barcons M., Franco S., Sanchez-Tapias J.M., and Saiz J.C. Dynamics of hepatitis C virus NS5A quasispecies during interferon and ribavirin therapy in responder and non-responder patients with genotype 1b chronic hepatitis C. J. Gen. Virol. 86 (2005) 1067-1075
39. Reed K.E., Xu J., and Rice C.M. Phosphorylation of the hepatitis C virus NS5A protein in vitro and in vivo: properties of the NS5A-associated kinase. J. Virol. 71 (1997) 7187-7197
40. Reed K.E., Gorbalenya A.E., and Rice C.M. The NS5A/NS5 proteins of viruses from three genera of the family Flaviviridae are phosphorylated by associated serine/threonine kinases. J. Virol. 72 (1998) 6199-6206
41. Sarcar B., Ghosh A.K., Steele R., Ray R., and Ray R.B. Hepatitis C virus NS5A mediated STAT3 activation requires co-operation of Jak1 kinase. Virology 322 (2004) 51-60
42. Seth R.B., Sun L., Ea C.K., and Chen Z.J. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122 (2005) 669-682
43. Sumpter Jr. R., Wang C., Foy E., Loo Y.M., and Gale Jr. M. Viral evolution and interferon resistance of hepatitis C virus RNA replication in a cell culture model. J. Virol. 78 (2004) 11591-11604
44. Taguchi T., Nagano-Fujii M., Akutsu M., Kadoya H., Ohgimoto S., Ishido S., and Hotta H. Hepatitis C virus NS5A protein interacts with 2′, 5'-oligoadenylate synthetase and inhibits antiviral activity of IFN in an IFN sensitivity-determining region-independent manner. J. Gen. Virol. 85 (2004) 959-969
45. Takamizawa A., Mori C., Fuke I., Manabe S., Murakami S., Fujita J., Onishi E., Andoh T., Yoshida I., and Okayama H. Structure and organization of the hepatitis C virus genome isolated from human carriers. J. Virol. 65 (1991) 1105-1113
46. Takeuchi T., Katsume A., Tanaka T., Abe A., Inoue K., Tsukiyama-Kohara K., Kawaguchi R., Tanaka S., and Kohara M. Real-time detection system for quantification of hepatitis C virus genome. Gastroenterology 116 (1999) 636-642
47. Tanji Y., Kaneko T., Satoh S., and Shimotohno K. Phosphorylation of hepatitis C virus-encoded nonstructural protein NS5A. J. Virol. 69 (1995) 3980-3986
48. Tong C.Y., Gilmore I.T., and Hart C.A. HCV-associated liver cancer. Lancet 345 (1995) 1058-1059
49. Xu L.G., Wang Y.Y., Han K.J., Li L.Y., Zhai Z., and Shu H.B. VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol. Cell 19 (2005) 727-740
50. Yoneyama M., Kikuchi M., Natsukawa T., Shinobu N., Imaizumi T., Miyagishi M., Taira K., Akira S., and Fujita T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5 (2004) 730-737
51. Zhu H.m., Nelson D.R., Crawford J.M., and Liu C. Defective Jak-Stat activation in hepatoma cells is associated with hepatitis C viral IFN-alpha resistance. J. Interferon Cytokine Res. 25 (2005) 528-539