Effects of the hepatitis C virus core protein on innate cellular defense pathways

Journal of Interferon and Cytokine Research

Volumn 24, Issue 7, 2004, Pages 391-402

  Miller, Kristen ^a   McArdle, Susan ^a   Gale Jr , Michael J ^b   Geller, David A ^c   Tenoever, Benjamin ^d   Hiscott, John ^d   Gretch, David R ^a   Polyak, Stephen J ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CORE PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 3; INTERFERON STIMULATED GENE FACTOR 3; JANUS KINASE; MESSENGER RNA; NITRIC OXIDE SYNTHASE; PROTEIN; STAT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; HELA CELL; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; VIRUS PATHOGENESIS;

DNA-BINDING PROTEINS; HELA CELLS; HEPACIVIRUS; HUMANS; IMMUNITY, NATURAL; INTERFERON REGULATORY FACTOR-1; INTERFERON-ALPHA; INTERFERON-BETA; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; PHOSPHOPROTEINS; PROMOTER REGIONS (GENETICS); SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; VIRAL CORE PROTEINS;

HEPATITIS C VIRUS; JANUS; RNA VIRUSES;

EID: 3242891546     PISSN: 10799907     EISSN: None     Source Type: Journal    
DOI: 10.1089/1079990041535647     Document Type: Article

References (77)

1. CDC. (1991). Public health service interagency guidelines for screening donors of blood, plasma, organs, tissues, and semen for evidence of hepatitis B and hepatitis C. MMWR 40(RR-4), 6-17.
2. DAVIS, G.L., ALBRIGHT, J.E., COOK, S., and ROSENBERG, D. (1998). Projecting the future healthcare burden from hepatitis C in the United States. Hepatology 28, 390A.
3. DI BISCEGLIE, A.M. (1995). Liver transplantation for hepatitis C: the promise and the challenge. Hepatology 22, 660-662.
4. FERRELL, L.D., WRIGHT, T.L., ROBERTS, J., ASCHER, N., and LAKE, J. (1992). Hepatitis C viral infection in liver transplant recipients. Hepatology 16, 865-876.
5. PURCELL, R. (1997). The hepatitis C virus: overview. Hepatology 26, 11S-14S.
6. WALEWSKI, J.L., KELLER, T.R., STUMP, D.D., and BRANCH, A.D. (2001). Evidence for a new hepatitis C virus antigen encoded in an overlapping reading frame. RNA 7, 710-721.
7. XU, Z., CHOI, J., YEN, T.S., LU, W., STROHECKER, A., GOVINDARAJAN, S., CHIEN, D., SELBY, M.J., and OU, J. (2001). Synthesis of a novel hepatitis C virus protein by ribosomal frameshift. EMBO J. 20, 3840-3848.
8. VARAKLIOTI, A., VASSILAKI, N., GEORGOPOULOU, U., and MAVROMARA, P. (2002). Alternate translation occurs within the core coding region of the hepatitis C viral genome. J. Biol. Chem. 277, 17713-17721.
9. VENTER, J.C., ADAMS, M.D., MYERS, E.W., LI, P.W., MURAL, R.J., SUTTON, G.G., SMITH, H.O., YANDELL, M., et al. (2001). The sequence of the human genome. Science 291, 1304-1351.
10. LANDER, E.S., LINTON, L.M., BIRREN, B., NUSBAUM, C., ZODY, M.C., BALDWIN, J., DEVON, K., DEWAR, K., et al. (2001). Initial sequencing and analysis of the human genome. Nature 409, 860-921.
11. POLYAK, S.J., PASCHAL, D., McARDLE, S., GALE, M., MORADPOUR, D., and GRETCH, D.R. (1999). Characterization of the effects of hepatitis C virus non-structural 5A protein expression in human cell lines and on interferon-sensitive virus replication. Hepatology 29, 1262-1271.
12. POLYAK, S.J., KHABAR, K.S., PASCHAL, D.M., EZELLE, H.J., DUVERLIE, G., BARBER, G.N., LEVY, D.E., MUKAIDA, N., and GRETCH, D.R. (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.
13. MORIYA, K., YOTSUYANAGI, H., SHINTANI, Y., FUJIE, H., ISHIBASHI, K., MATSUURA, Y., MIYAMURA, T., and KOIKE, K. (1997). Hepatitic C virus core protein induces hepatic steatosis in transgenic mice. J. Gen. Virol. 78, 1527-1531.
14. MORIYA, K., FUJIE, H., SHINTANI, Y., YOTSUYANAGI, H., TSUTSUMI, T., ISHIBASHI, K., MATSUURA, Y., KIMURA, S., MIYAMURA, T., and KOIKE, K. (1998). The core protein of hepatitis C virus induces hepatocellular carcinoma in transgenic mice. Nat. Med. 4, 1065-1067.
15. LERAT, H., HONDA, M., BEARD, M.R., LOESCH, K., SUN, J., YANG, Y., OKUDA, M., GOSERT, R., XIAO, S.Y., WEINMAN, S.A., and LEMON, S.M. (2002). Steatosis and liver cancer in transgenic mice expressing the structural and nonstructural proteins of hepatitis C virus. Gastroenterology 122, 352-365.
16. BARBA, G., HARPER, F., HARADA, T., KOHARA, M., GOULINET, S., MATSUURA, Y., EDER, G., SCHAFF, Z., CHAPMAN, M.J., MIYAMURA, T., and BRECHOT, C. (1997). Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. Proc. Natl. Acad. Sci. USA 175, 740-744.
17. PERLEMUTER, G., SABILE, A., LETTERON, P., VONA, G., TOPILCO, A., CHRETIEN, Y., KOIKE, K., PESSAYRE, D., CHAPMAN, J., BARBA, G., and BRECHOT, C. (2002). Hepatitis C virus core protein inhibits microsomal triglyceride transfer protein activity and very low density lipoprotein secretion: a model of viral-related steatosis. FASEB J. 16, 185-194.
18. OKUDA, M., LI, K., BEARD, M.R., SHOWALTER, L.A., SCHOLLE, F., LEMON, S.M., and WEINMAN, S.A. (2002). Mitochondrial injury, oxidative stress, and antioxidant gene expression are induced by hepatitis C virus core protein. Gastroenterology 122, 366-375.
19. MATSUMOTO, M., HSIEH, T.Y., ZHU, N.L., VANARSDALE, T., HWANG, S.B., JENG, K.S., GORBALENYA, A.E., LO, S.Y., OU, J.H., WARE, C.F., and LAI, M.M.C. (1997). Hepatitis C virus core protein interacts with the cytoplasmic tail of lymphotoxin-beta receptor. J. Virol. 71, 1301-1309.
20. ZHU, N.L., KHOSHNAN, A., SCHNEIDER, R., MATSUMOTO, M., DENNERT, G., WARE, C., and LAI, M.M.C. (1998). Hepatitis C virus core protein binds to the cytoplasmic domain of tumor necrosis factor (TNF) receptor 1 and enhances TNF-induced apoptosis. J. Virol. 72, 3691-3697.
21. RAY, R.B., MEYER, K., and RAY, R. (1996). Suppression of apoptotic cell death by hepatitis C virus core protein. Virology 226, 176-182.
22. RAY, R.B., MEYER, K., STEELE, R., SHRIVASTAVA, A., AGGARWAL, B.B., and RAY, R. (1998). Inhibition of tumor necrosis factor (TNF-alpha)-mediated apoptosis by hepatitis C virus core protein. J. Biol. Chem. 273, 2256-2259.
23. MARUSAWA, H., HIJIKATA, M., CHIBA, T., and SHIMOTOHNO, K. (1999). Hepatitis C virus core protein inhibits Fas-and tumor necrosis factor alpha-mediated apoptosis via NF-kappa B activation. J Virol. 73, 4713-4720.
24. POLYAK, S.J. (2003). Hepatitis C virus-cell interactions and their role in pathogenesis. Clin. Liver Dis. 7, 67-88.
25. FOY, E., LI, K., WANG, C., SUMPTER, R., JR., IKEDA, M., LEMON, S.M., and GALE, M., JR. (2003). Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease. Science 300, 1145-1148.
26. HEIM, M.H., MORADPOUR, D., and BLUM, H.E. (1999). Expression of hepatitis C virus proteins inhibits signal transduction through the Jak-Stat pathway. J. Virol. 73, 8469-8475.
27. DUONG, F.H., FILIPOWICZ, M., TRIPODI, M., LA MONICA, N., and HEIM, M.H. (2004). Hepatitis C virus inhibits interferon signaling through up-regulation of protein phosphatase 2A. Gastroenterology 126, 263-277.
28. 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. (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.
29. TAYLOR, D.R., SHI, S.T., ROMANO, P.R., BARBER, G.N., and LAI, M.M.C. (1999). Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein. Science 285, 107-110.
30. GIRARD, S., SHALHOUB, P., LESCURE, P., SABILE, A., MISEK, D.E., HANASH, S., BRECHOT, C., and BERETTA, L. (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.
31. POLYAK, S.J., KHABAR, K.S., REZEIQ, M., and GRETCH, D.R. (2001). Elevated levels of interleukin-8 in serum are associated with hepatitis C virus infection and resistance to interferon therapy. J. Virol. 75, 6209-6211.
32. NAGANUMA, A., NOZAKI, A., TANAKA, T., SUGIYAMA, K., TAKAGI, H., MORI, M., SHIMOTOHNO, K., and KATO, N. (2000). Activation of the interferon-inducible 2′-5′-oligoadenylate synthetase gene by hepatitis C virus core protein. J Virol. 74, 8744-8750.
33. GONG, G., WARIS, G., TANVEER, R., and SIDDIQUI, A. (2001). Human hepatitis C virus NS5A protein alters intracellular calcium levels, induces oxidative stress, and activates Stat-3 and NF-kappa B. Proc. Natl. Acad. Sci. USA 98, 9599-9604.
34. LIN, R., GENIN, P., MAMANE, Y., and HISCOTT, J. (2000). Selective DNA binding and association with the CREB binding protein coactivator contribute to differential activation of alpha/beta interferon genes by interferon regulatory factors 3 and 7. Mol. Cell. Biol. 20, 6342-6353.
35. POLYAK, S.J., RAWLS, W.E., and HARNISH, D.G. (1991). Characterization of Pichinde virus infection of cells of the monocytic lineage. J. Virol. 65, 3575-3582.
36. SERVANT, M.J., TEN OEVER, B., LEPAGE, C., CONTI, L., GESSANI, S., JULKUNEN, I., LIN, R., and HISCOTT, J. (2001). Identification of distinct signaling pathways leading to the phosphorylation of interferon regulatory factor 3. J. Biol. Chem. 276, 355-363.
37. LIN, R., HEYLBROECK, C., PITHA, P.M., and HISCOTT, J. (1998). Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation. Mol. Cell. Biol. 18, 2986-2996.
38. LEVY, D.E., LEW, D.J., DECKER, T., KESSLER, D.S., and DARNELL, J.E., JR. (1990). Synergistic interaction between interferon-alpha and interferon-gamma through induced synthesis of one subunit of the transcription factor ISGF3. EMBO J. 9, 1105-1111.
39. SHI, S.T., POLYAK, S.J., HONG, T., TAYLOR, D.R., GRETCH, D.R., and LAI, M.M.C. (2002). Hepatitis C virus NS5A colocalizes with the core protein on lipid droplets and interacts with apolipoproteins. Virology 292, 198-210.
40. BRIKEN, V., RUFFNER, H., SCHULTZ, U., SCHWARZ, A., REIS, L.F., STREHLOW, I., DECKER, T., and STAEHELI, P. (1995). Interferon regulatory factor 1 is required for mouse Gbp gene activation by gamma interferon. Mol. Cell. Biol. 15, 975-982.
41. HISCOTT, J., PITHA, P., GENIN, P., NGUYEN, H., HEYLBROECK, C., MAMANE, Y., ALGARTE, M., and LIN, R. (1999). Triggering the interferon response: the role of IRF-3 transcription factor. J. Interferon Cytokine Res. 19, 1-13.
42. JUANG, Y.T., LOWTHER, W., KELLUM, M., AU, W.C., LIN, R., HISCOTT, J., and PITHA, P.M. (1998). Primary activation of interferon A and interferon B gene transcription by interferon regulatory factor 3. Proc. Natl. Acad. Sci. USA 95, 9837-9842.
43. DARNELL, J.E., KERR, I.M., and STARK, G.R. (1994). Jak-Stat pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264, 1415-1421.
44. REES, D.D., PALMER, R.M., SCHULZ, R., HUDSON, H.F., and MONCADA, S. (1990). Characterization of three inhibitors of endothelial nitric oxide synthase in vitro and in vivo. Br. J. Pharmacol. 101, 746-752.
45. CHARTRAIN, N.A., GELLER, D.A., KOTY, P.P., SITRIN, N.F., NUSSLER, A.K., HOFFMAN, E.P., BILLIAR, T.R., HUTCHINSON, N.I., and MUDGETT, J.S. (1994). Molecular cloning, structure, and chromosomal localization of the human inducible nitric oxide synthase gene. J. Biol. Chem. 269, 6765-6772.
46. GANSTER, R.W., TAYLOR, B.S., SHAO, L., and GELLER, D.A. (2001). Complex regulation of human inducible nitric oxide synthase gene transcription by Stat1 and NF-kappa B. Proc. Natl. Acad. Sci. USA 98, 8638-8643.
47. DELHEM, N., SABILE, A., GAJARDO, R., PODEVIN, P., ABADIE, A., BLATON, M.A., KREMSDORF, D., BERETTA, L., and BRECHOT, C. (2001). Activation of the interferon-inducible protein kinase PKR by hepatocellular carcinoma derived-hepatitis C virus core protein. Oncogene 20, 5836-5845.
48. PFLUGHEBER, J., FREDERICKSEN, B., SUMPTER, R., JR., WANG, C., WARE, F., SODORA, D.L., and GALE, M., JR. (2002). Regulation of PKR and IRF-1 during hepatitis C virus RNA replication. Proc. Natl. Acad. Sci. USA 99, 4650-4655.
49. KUMAR, A., YANG, Y.L., FLATI, V., DER, S., KADEREIT, S., DEB, A., HAQUE, J., REIS, L., WEISSMANN, C., and WILLIAMS, B.R. (1997). Deficient cytokine signaling in mouse embryo fibroblasts with a targeted deletion in the PKR gene: role of IRF-1 and NF-kappaB. EMBO J. 16, 406-416.
50. HOSUI, A., OHKAWA, K., ISHIDA, H., SATO, A., NAKANISHI, F., UEDA, K., TAKEHARA, T., KASAHARA, A., SASAKI, Y., HORI, M., and HAYASHI, N. (2003). Hepatitis C virus core protein differently regulates the Jak-Stat signaling pathway under interleukin-6 and interferon-gamma stimuli. J. Biol. Chem. 278, 28562-28571.
51. YOSHIDA, T., HANADA, T., TOKUHISA, T., KOSAI, K., SATA, M., KOHARA, M., and YOSHIMURA, A. (2002). Activation of Stat3 by the hepatitis C virus core protein leads to cellular transformation. J. Exp. Med. 196, 641-653.
52. DANSAKO, H., NAGANUMA, A., NAKAMURA, T., IKEDA, F., NOZAKI, A., and KATO, N. (2003). Differential activation of interferon-inducible genes by hepatitis C virus core protein mediated by the interferon-stimulated response element. Virus Res. 97, 17-30.
53. BASU, A., MEYER, K., RAY, R.B., and RAY, R. (2001). Hepatitis C virus core protein modulates the interferon-induced transacting factors of Jak/Stat signaling pathway but does not affect the activation of downstream IRF-1 or 561 gene. Virology 288, 379-390.
54. RAY, R.B., STEELE, R., BASU, A., MEYER, K., MAJUMDER, M., GHOSH, A.K., and RAY, R. (2002). Distinct functional role of hepatitis C virus core protein on NF-kappaB regulation is linked to genomic variation. Virus Res. 87, 21-29.
55. LOGUERCIO, C., and FEDERICO, A. (2003). Oxidative stress in viral and alcoholic hepatitis. Free Radic. Biol. Med. 34, 1-10.
56. ROCKEY, D.C., and SHAH, V. (2004). Nitric oxide biology and the liver: Report of an AASLD research workshop. Hepatology 39, 250-257.
57. HOFSETH, L.J., HUSSAIN, S.P., WOGAN, G.N., and HARRIS, C.C. (2003). Nitric oxide in cancer and chemoprevention. Free Radic. Biol. Med. 34, 955-968.
58. TORRE, D., PUGLIESE, A., and SPERANZA, F. (2002). Role of nitric oxide in HIV-1 infection: friend or foe? Lancet Infect. Dis. 2, 273-280.
59. LAI, M.M. (2002). Hepatitis C virus proteins: direct link to hepatic oxidative stress, steatosis, carcinogenesis and more. Gastroenterology 122, 568-571.
60. BAUTISTA, A.P. (2001). Free radicals, chemokines, and cell injury in HIV-1 and SIV infections and alcoholic hepatitis. Free Radic. Biol. Med. 31, 1527-1532.
61. AKAIKE, T. (2001). Role of free radicals in viral pathogenesis and mutation. Rev. Med. Virol. 11, 87-101.
62. AKAIKE, T., and MAEDA, H. (2000). Nitric oxide and virus infection. Immunology 101, 300-308.
63. BAUGH, M.A. (2000). HIV: reactive oxygen species, enveloped viruses and hyperbaric oxygen. Med. Hypotheses 55, 232-238.
64. DE LUCAS, S., BARTOLOME, J., AMARO, M.J., and CARRENO, V. (2003). Hepatitis C virus core protein transactivates the inducible nitric oxide synthase promoter via NF-kappaB activation. Antiviral Res. 60, 117-124.
65. KAMIJO, R., HARADA, H., MATSUYAMA, T., BOSLAND, M., GERECITANO, J., SHAPIRO, D., LE, J., KOH, S.I., KIMURA, T., GREEN, S.J., et al. (1994). Requirement for transcription factor IRF-1 in NO synthase induction in macrophages. Science 263, 1612-1615.
66. MARTIN, E., NATHAN, C., and XIE, Q.W. (1994). Role of interferon regulatory factor 1 in induction of nitric oxide synthase. J. Exp. Med. 180, 977-984.
67. TACCHINI, L., FUSAR-POLI, D., and BERNELLI-ZAZZERA, A. (2002). Activation of transcription factors by drugs inducing oxidative stress in rat liver. Biochem. Pharmacol. 63, 139-148.
68. WARIS, G., HUH, K.W., and SIDDIQUI, A. (2001). Mitochondrially associated hepatitis B virus X protein constitutively activates transcription factor Stat-3 and NF-kappa B via oxidative stress. Mol. Cell. Biol. 21, 7721-7730.
69. MADAMANCHI, N.R., LI, S., PATTERSON, C., and RUNGE, M.S. (2001). Reactive oxygen species regulate heat-shock protein 70 via the Jak/Stat pathway. Arterioscler Thromb. Vasc. Biol. 21, 321-326.
70. CARBALLO, M., CONDE, M., EL BEKAY, R., MARTIN-NIETO, J., CAMACHO, M.J., MONTESEIRIN, J., CONDE, J., BEDOYA, F.J., and SOBRINO, F. (1999). Oxidative stress triggers Stat3 tyrosine phosphorylation and nuclear translocation in human lymphocytes. J. Biol. Chem. 274, 17580-17586.
71. MAZIERE, C., ALIMARDANI, G., DANTIN, F., DUBOIS, F., CONTE, M.A., and MAZIERE, J.C. (1999). Oxidized LDL activates Stat1 and Stat3 transcription factors: possible involvement of reactive oxygen species. FEBS Lett. 448, 49-52.
72. HUI, D.J., BHASKER, C.R., MERRICK, K W.C., and SEN, G.C. (2003). Viral stress-inducible protein p56 inhibits translation by blocking the interaction of eIF3 with the ternary complex eIF2.GTP.Met-tRNAi. J. Biol. Chem. 278, 39477-39482.
73. GALE, M., BLAKELY, C.M., KWIECISZEWSKI, B., TAN, S.L., DOSSETT, M., TANG, N.M., KORTH, M.J., POLYAK, S.J., GRETCH, D.R., and KATZE, M.G. (1998). Control of PKR protein kinase by hepatitis C virus nonstructural 5A protein: molecular mechanisms of kinase regulation. Mol. Cell. Biol. 18, 5208-5218.
74. FERNANDEZ, M., QUIROGA, J.A., MARTIN, J., HERRERO, M., PARDO, M., HORISBERGER, M.A., and CARRENO, V. (1999). In vivo and in vitro induction of MxA protein in peripheral blood mononuclear cells from patients chronically infected with hepatitis C virus. J. Infect. Dis. 180, 262-267.
75. PAWLOTSKY, J.M., HOVANESSIAN, A.G., ROUDOT-THORAVAL, F., ROBERT, N., BOUVIER, M., BABANY, G., DUVAL, J., and DHUMEAUX, D. (1996). Effect of alpha interferon (IFN-alpha) on 2′-5′ oligoadenylate synthetase activity in peripheral blood mononuclear cells of patients with chronic hepatitis C: relationship to the antiviral effect of IFN-alpha. Antimicrob. Agents Chemother. 40, 320-324.
76. PAWLOTSKY, J.M., HOVANESSIAN, A., ROUDOT-THORAVAL, F., LEBON, P., ROBERT, N., BOUVIER, M., BABANY, G., DUVAL, J., and DHUMEAUX, D. (1995). Activity of the interferon-induced 2′,5′-oligoadenylate synthetase in patients with chronic hepatitis C. J. Interferon Cytokine Res. 15, 857-862.
77. YU, S.H., NAGAYAMA, K., ENOMOTO, N., IZUMI, N., MARUMO, F., and SATO, C. (2000). Intrahepatic mRNA expression of interferon-inducible antiviral genes in liver diseases: dsRNA-dependent protein kinase overexpression and RNase L inhibitor suppression in chronic hepatitis C. Hepatology 32, 1089-1095.