Defective Jak-Stat activation in hepatoma cells is associated with hepatitis C viral IFN-α resistance

Journal of Interferon and Cytokine Research

Volumn 25, Issue 9, 2005, Pages 528-539

  Zhu, Haizhen ^b   Nelson, David R ^b   Crawford, James M ^b   Liu, Chen ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ALPHA2B INTERFERON; INTERFERON; JANUS KINASE; RECOMBINANT INTERLEUKIN 6; RIBAVIRIN; STAT PROTEIN; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3;

ARTICLE; CANCER; CELL CULTURE; CELL LINE; CELL SELECTION; CONTROLLED STUDY; DRUG RESPONSE; ENZYME ACTIVATION; GENE MUTATION; HEPATITIS C; HEPATITIS C VIRUS; HEPATOMA CELL; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; IN VITRO STUDY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPLICON; SIGNAL TRANSDUCTION; VIRUS GENOME; VIRUS INFECTION; VIRUS MUTATION;

ANTIVIRAL AGENTS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; DNA-BINDING PROTEINS; DRUG RESISTANCE, VIRAL; HEPACIVIRUS; HUMANS; INTERFERON-ALPHA; LIVER; LIVER NEOPLASMS; MUTATION; PROTEIN-TYROSINE KINASES; REPLICON; REPRESSOR PROTEINS; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; VIRAL NONSTRUCTURAL PROTEINS;

HEPATITIS C VIRUS;

EID: 25844465627     PISSN: 10799907     EISSN: None     Source Type: Journal    
DOI: 10.1089/jir.2005.25.528     Document Type: Article

References (44)

1. Alter MJ, Kruszon-Moran D, Nainan OV, McQuillan GM, Gao F, Moyer LA, Kaslow RA, Margolis HS. The prevalence of hepatitis C virus infection in the United States, 1988 through 1994. N Engl J Med. 1999;341:556-562.
2. Manns MP, McHutchison JG, Gordon SC, Rustgi VK, Shiffman M, Reindollar R, Goodman ZD, Koury K, Ling M, Albrecht JK. Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for initial treatment of chronic hepatitis C: a randomised trial. Lancet. 2001;358:958-965.
3. Fried MW, Shiffman ML, Reddy KR, Smith C, Marino G, Goncales FL Jr, Haussinger D, Diago M, Carosi G, Dhumeaux D, Craxi A, Lin A, Hoffman J, Yu J. Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N Engl J Med. 2002;347:975-982.
4. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. How cells respond to interferons. Annu Rev Biochem. 1998;67:227-264.
5. Pawlotsky JM. Mechanisms of antiviral treatment efficacy and failure in chronic hepatitis C. Antiviral Res. 2003;59:1-11.
6. Samuel CE. Antiviral actions of interferons. Clin Microbiol Rev. 2001;14:778-809.
7. Levy DE, Darnell JE Jr. Stats: transcriptional control and biological impact. Nat Rev Mol Cell Biol. 2002;3:651-662.
8. Starr R, Willson TA, Viney EM, Murray LJ, Rayner JR, Jenkins BJ, Gonda TJ, Alexander WS, Metcalf D, Nicola NA, Hilton DJ. A family of cytokine-inducible inhibitors of signalling. Nature. 1997;387:917-921.
9. Yang CH, Murti A, Baker SJ, Frangou-Lazaridis M, Vartapetian AB, Murti KG, Pfeffer LM. Interferon induces the interaction of prothymosin-alpha with Stat3 and results in the nuclear translocation of the complex. Exp Cell Res. 2004;298:197-206.
10. Darnell JE Jr. Stats and gene regulation. Science. 1997;277:1630-1635.
11. Bigger CB, Brasky KM, Lanford RE. DNA microarray analysis of chimpanzee liver during acute resolving hepatitis C virus infection. J Virol. 2001;75:7059-7066.
12. Iizuka N, Oka M, Yamada-Okabe H, Mori N, Tamesa T, Okada T, Takemoto N, Tangoku A, Hamada K, Nakayama H, Miyamoto T, Uchimura S, Hamamoto Y. Comparison of gene expression profiles between hepatitis B virus- and hepatitis C virus-infected hepatocellular carcinoma by oligonucleotide microarray data on the basis of a supervised learning method. Cancer Res. 2002;62:3939-3944.
13. Hoofnagle JH. Course and outcome of hepatitis C. Hepatology. 2002;36(5 Suppl 1):S21-29.
14. Liang TJ, Rehermann B, Seeff LB, Hoofnagle JH. Pathogenesis, natural history, treatment, and prevention of hepatitis C. Ann Intern Med. 2000;132:296-305.
15. Katze MG, He Y, Gale M Jr. Viruses and interferon: a fight for supremacy. Nat Rev Immunol. 2002;2:675-687.
16. Taylor DR, Shi ST, Romano PR, Barber GN, Lai MM. Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein. Science. 1999;285:107-110.
17. Gale M Jr, Blakely CM, Kwieciszewski B, Kwieciszewski B, Tan SL, Dossett M, Tang NM, Korth MJ, Polyak SJ, Gretch DR, Katze MG. Control of PKR protein kinase by hepatitis C virus nonstructural 5A protein: molecular mechanisms of kinase regulation. Mol Cell Biol. 1998;18:5208-5218.
18. Foy E, Li K, Sumpter R Jr, Loo YM, Johnson CL, Wang C, Fish PM, Yoneyama M, Fujita T, Lemon SM, Gale M Jr. Control of antiviral defenses through hepatitis C virus disruption of retinoic acid-inducible gene-I signaling. Proc Natl Acad Sci USA. 2005;102:2986-2991.
19. Enomoto N, Sakuma I, Asahina Y, Kurosaki M, Murakami T, Yamamoto C, Izumi N, Marumo F, Sato C. Comparison of full-length sequences of interferon-sensitive and resistant hepatitis C virus 1b. Sensitivity to interferon is conferred by amino acid substitutions in the NS5A region. J Clin Invest. 1995;96:224-230.
20. Herion D, Hoofnagle JH. The Interferon sensitivity determining region: all hepatitis C virus isolates are not the same. Hepatology. 1997;25:769-771.
21. Gong G, Waris G, Tanveer R, Siddiqui A. Human hepatitis C virus NS5A protein alters intracellular calcium levels, induces oxidative stress, and activates Stat3 and NF-kappa B. Proc Natl Acad Sci USA. 2001;98:9599-9604.
22. Hosui A, Ohkawa K, Ishida H, Sato A, Nakanishi F, Ueda K, Takehara T, Kasahara A, Sasaki Y, Hori M, Hayashi N. Hepatitis C virus core protein differently regulates the Jak-Stat signaling pathway under interleukin-6 and interferon-gamma stimuli. J Biol Chem. 2003;278:28562-28571.
23. Kirkwood JM, Farkas DL, Chakraborty A, Chakraborty A, Dyer KF, Tweardy DJ, Abernethy JL, Edington HD, Donnelly SS, Becker D. Systemic interferon-alpha (IFN-alpha) treatment leads to Stat3 inactivation in melanoma precursor lesions. Mol Med. 1999;5:11-20.
24. Yang CH, Murti A, Pfeffer LM. Stat3 complements defects in an interferon-resistant cell line: evidence for an essential role for Stat3 in interferon signaling and biological activities. Proc Natl Acad Sci USA. 1998;95:5568-5572.
25. Wong LH, Krauer KG, Hatzinisiriou I, Estcourt MJ, Hersey P, Tam ND, Edmondson S, Devenish RJ, Ralph SJ. Interferon-resistant human melanoma cells are deficient in ISGF3 components, Stal1, Stat2, and p48-ISGF3 gamma. J Biol Chem. 1997;272:28779-28785.
26. Lohmann V, Korner F, Koch J, Herian U, Theilmann L, Bartenschlager R. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science. 1999;285:110-113.
27. Blight KJ, Kolykhalov AA, Rice CM. Efficient initiation of HCV RNA replication in cell culture. Science. 2000;290:1972-1974.
28. Zhu H, Zhao H, Collins CD, Eckenrode SE, Run Q, McIndoe RA, Crawford JM, Nelson DR, She JX, Liu C. Gene expression associated with interferon alfa antiviral activity in an HCV replicon cell line. Hepatology. 2003;37:1180-1188.
29. Guo JT, Zhu Q, Seeger C. Cytopathic and noncytopathic interferon responses in cells expressing hepatitis C virus subgenomic replicons. J Virol. 2003;77:10769-10779.
30. Guo JT, Bichko VV, Seeger C. Effect of alpha interferon on the hepatitis C virus replicon. J Virol. 2001;75:8516-8523.
31. Matsuda T, Nakamura T, Nakao K, Arai T, Katsuki M, Heike T, Yokota T. Stat3 activation is sufficient to maintain an undifferentiated state of mouse embryonic stem cells. EMBO J. 1999;18:4261-4269.
32. + T-cell interaction with HCV replicon cells: evidence for both cytokine- and cell-mediated antiviral activity. Hepatology. 2003;37:1335-1342.
33. Niu G, Heller R, Catlett-Falcone R, Coppola D, Jaroszeski M, Dalton W, Jove R, Yu H. Gene therapy with dominant-negative Stat3 suppresses growth of the murine melanoma B16 tumor in vivo. Cancer Res. 1999;59:5059-5063.
34. Zhu H, Liu C. Interleukin-1 inhibits hepatitis C virus subgenomic RNA replication by activation of extracellular regulated kinase pathway. J Virol. 2003;77:5493-5498.
35. Sumpter R, Jr, Wang C, Foy E, Loo YM, Gale M Jr. Viral evolution and interferon resistance of hepatitis C virus RNA replication in a cell culture model. J Virol. 2004;78:11591-11604.
36. Namba K, Naka K, Dansako H, Nozaki A, Ikeda M, Shiratori Y, Shimotohno K, Kato N. Establishment of hepatitis C virus replicon cell lines possessing interferon-resistant phenotype. Biochem Biophys Res Commun. 2004;323:299-309.
37. Reddy KR, Hoofnagle JH, Tong MJ, Lee WM, Pockros P, Heathcote EJ, Albert D, Joh T. Racial differences in responses to therapy with interferon in chronic hepatitis C. Consensus Interferon Study Group. Hepatology. 1999;30:787-793.
38. Layden-Almer JE, Ribeiro RM, Wiley T, Perelson AS, Layden TJ. Viral dynamics and response differences in HCV-infected African American and white patients treated with IFN and ribavirin. Hepatology. 2003;37:1343-1350.
39. Gao B, Hong F, Radaeva S. Host factors and failure of interferon alpha treatment in hepatitis C virus. Hepatology. 2004;39:880-890.
40. Taylor DR, Shi ST, Lai MM. Hepatitis C virus and interferon resistance. Microbes Infect. 2000;2:1743-1756.
41. Yoshida T, Hanada T, Tokuhisa T, Kosai K, Sata M, Kohara M, Yoshimura A. Activation of Stat3 by the hepatitis C virus core protein leads to cellular transformation. J Exp Med. 2002;196:641-653.
42. Zhu H, Shang X, Terada N, Liu C. Stat3 induces anti-hepatitis C viral activity in liver cells. Biochem Biophys Res Commun. 2004;324:518-528.
43. Song MM, Shuai K. The suppressor of cytokine signaling (SOCS) 1 and SOCS3 but not SOCS2 proteins inhibit interferon-mediated antiviral and antiproliferative activities. J Biol Chem. 1998;273:35056-35062.
44. Sakai I, Takeuchi K, Yamauchi H, Narumi H, Fujita S. Constitutive expression of SOCS3 confers resistance to IFN-alpha in chronic myelogenous leukemia cells. Blood. 2002;100:2926-2931.