Hepatitis C Virus Nonstructural 5B Protein Regulates Tumor Necrosis Factor Alpha Signaling through Effects on Cellular IκB Kinase

REFERENCES

• Aach, R. D., C. E. Stevens, F. B. Hollinger, J. W. Mosley, D. A. Peterson, P. E. Taylor, R. G. Johnson, L. H. Barbosa, and G. J. Nemo. 1991. Hepatitis C virus infection in post-transfusion hepatitis. An analysis with first- and second-generation assays. N. Engl. J. Med. 325:1325–1329.
   PubMed Web of Science ®Google Scholar
• Albanese, C., K. Wu, M. D'Amico, C. Jarrett, D. Joyce, J. Hughes, J. Hulit, T. Sakamaki, M. Fu, A. Ben-Ze'ev, J. F. Bromberg, C. Lamberti, U. Verma, R. B. Gaynor, S. W. Byers, and R. G. Pestell. 2003. IKKalpha regulates mitogenic signaling through transcriptional induction of cyclin D1 via Tcf. Mol. Biol. Cell 14:585–599.
   PubMed Web of Science ®Google Scholar
• Arenzana-Seisdedos, F., P. Turpin, M. Rodriguez, D. Thomas, R. T. Hay, J. L. Virelizier, and C. Dargemont. 1997. Nuclear localization of IkappaB alpha promotes active transport of NF-kappa B from the nucleus to the cytoplasm. J. Cell Sci. 110:369–378.
   PubMedGoogle Scholar
• Baeuerle, P. A., and D. Baltimore. 1996. NF-kappa B: ten years after. Cell 87:13–20.
   PubMed Web of Science ®Google Scholar
• Baldwin, A. S., Jr. 1996. The NF-kappa B and IkappaB proteins: new discoveries and insights. Annu. Rev. Immunol. 14:649–683.
   PubMed Web of Science ®Google Scholar
• Barnes, P. J., and M. Karin. 1997. Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. N. Engl. J. Med. 336:1066–1071.
   PubMed Web of Science ®Google Scholar
• Bazzoni, F., and B. Beutler. 1996. The tumor necrosis factor ligand and receptor families. N. Engl. J. Med. 334:1717–1725.
   PubMed Web of Science ®Google Scholar
• Behrens, S. E., L. Tomei, and R. De Francesco. 1996. Identification and properties of the RNA-dependent RNA polymerase of hepatitis C virus. EMBO J. 15:12–22.
   PubMed Web of Science ®Google Scholar
• Brenner, D. A., M. O'Hara, P. Angel, M. Chojkier, and M. Karin. 1989. Prolonged activation of jun and collagenase genes by tumour necrosis factor-alpha. Nature 337:661–663.
   PubMed Web of Science ®Google Scholar
• Bressanelli, S., L. Tomei, F. A. Rey, and R. De Francesco. 2002. Structural analysis of the hepatitis C virus RNA polymerase in complex with ribonucleotides. J. Virol. 76:3482–3492.
   PubMed Web of Science ®Google Scholar
• Cho, Y. G., J. W. Yoon, K. L. Jang, C. M. Kim, and Y. C. Sung. 1993. Full genome cloning and nucleotide sequence analysis of hepatitis C virus from sera of chronic hepatitis patients in Korea. Mol. Cells 3:195–202.
   Google Scholar
• Chung, Y. M., K. J. Park, S. Y. Choi, S. B. Hwang, and S. Y. Lee. 2001. Hepatitis C virus core protein potentiates TNF-α-induced NF-κB activation through TRAF2-IKKβ-dependent pathway. Biochem. Biophys. Res. Commun. 284:15–19.
   PubMedGoogle Scholar
• Deak, J. C., and D. J. Templeton. 1997. Regulation of the activity of MEK kinase 1 (MEKK1) by autophosphorylation within the kinase activation domain. Biochem. J. 322:185–192.
   PubMedGoogle Scholar
• Di Bisceglie, A., M. L. H. Simpson, M. T. Lotze, and J. H. Hoofnagle. 1994. Development of hepatocellular carcinoma among patients with chronic liver disease due to hepatitis C viral infection. J. Clin. Gastroenterol. 19:222–226.
   PubMedGoogle Scholar
• DiDonato, J. A., M. Hayakawa, D. M. Rothwarf, E. Zandi, and M. Karin. 1997. A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB. Nature 388:548–554.
   PubMed Web of Science ®Google Scholar
• Ferrari, E., J. Wright-Minogue, J. W. Fang, B. M. Baroudy, J. Y. Lau, and Z. Hong. 1999. Characterization of soluble hepatitis C virus RNA-dependent RNA polymerase expressed in Escherichia coli. J. Virol. 73:1649–1654.
   PubMedGoogle Scholar
• Fuerst, T. A., E. G. Niles, F. W. Studier, and B. Moss. 1986. Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc. Natl. Acad. Sci. USA 83:8122–8126.
   PubMed Web of Science ®Google Scholar
• Geleziunas, R., S. Ferrell, X. Lin, Y. Mu, E. T. Cunningham, Jr., M. Grant, M. A. Connelly, J. E. Hambor, K. B. Marcu, and W. C. Greene. 1998. Human T-cell leukemia virus type 1 Tax induction of NF-kappaB involves activation of the IkappaB kinase alpha (IKKalpha) and IKKbeta cellular kinases. Mol. Cell. Biol. 18:5157–5165.
   PubMed Web of Science ®Google Scholar
• Grakoui, A., C. Wychowski, C. Lin, S. M. Feinstone, and C. M. Rice. 1993. Expression and identification of hepatitis C virus polyprotein cleavage products. J. Virol. 67:1385–1395.
   PubMed Web of Science ®Google Scholar
• Hideo, Y., N. Kato, Y. Shiratori, M. Otsuka, S. Maeda, J. Kato, and M. Omata. 2001. Hepatitis C virus core protein activates nuclear factor kappa B-dependent signaling through tumor necrosis factor receptor-associated factor. J. Biol. Chem. 276:16399–16405.
   PubMedGoogle Scholar
• Hijikata, M., N. Kato, Y. Ootsuyama, M. Nakagawa, and K. Shimotohno. 1991. Gene mapping of the putative structural region of the hepatitis C virus genome by in vitro processing analysis. Proc. Natl. Acad. Sci. USA 88:5547–5551.
   PubMed Web of Science ®Google Scholar
• Hiscott, J., H. Kwon, and P. Genin. 2001. Hostile takeovers: viral appropriation of the NF-kappaB pathway. J. Clin. Investig. 107:143–151.
   PubMed Web of Science ®Google Scholar
• Hu, Y., V. Baud, M. Delhase, P. Zhang, T. Deerinck, M. Ellisman, R. Johnson, and M. Karin. 1999. Abnormal morphogenesis but intact IKK activation in mice lacking the IKKalpha subunit of IkappaB kinase. Science 284:316–320.
   PubMed Web of Science ®Google Scholar
• Hwang, S. B., K. J. Park, Y. S. Kim, Y. C. Sung, and M. M. C. Lai. 1997. Hepatitis C virus NS5B protein is a membrane-associated phosphoprotein with a predominantly perinuclear localization. Virology 227:439–446.
   PubMed Web of Science ®Google Scholar
• Karin, M. 1999. How NF-kappaB is activated: the role of the IkappaB kinase (IKK) complex. Oncogene 18:6867–6874.
   PubMed Web of Science ®Google Scholar
• Krappmann, D., and C. Scheidereit. 1997. Regulation of NF-kappaB activity by IkappaB alpha and IkappaB beta stability. Immunobiology 198:3–13.
   PubMedGoogle Scholar
• Lee, F. S., R. T. Peters, L. C. Dang, and T. Maniatis. 1998. MEKK1 activates both IκB kinase α and IκB kinase β. Proc. Natl. Acad. Sci. USA 95:9319–9324.
   PubMed Web of Science ®Google Scholar
• Lee, S. Y., A. Reichlin, A. Santana, K. A. Sokol, M. C. Nussenzweig, and Y. Choi. 1997. TRAF2 is essential for JNK but not NF-kappaB activation and regulates lymphocyte proliferation and survival. Immunity 7:703–713.
   PubMed Web of Science ®Google Scholar
• Lee, S. Y., S. Y. Lee, G. Kandala, M.-L. Liou, H. C. Liou, and Y. Choi. 1997. CD30/TNF receptor-associated factor interaction: NF-kappaB activation and binding specificity. Proc. Natl. Acad. Sci. USA 93:9699–9703.
   Google Scholar
• Lesburg, C. A., M. B. Cable, E. Ferrari, Z. Hong, A. F. Mannarino, and P. C. Weber. 1999. Crystal structure of the RNA-dependent RNA polymerase from hepatitis C virus reveals a fully encircled active site. Nat. Struct. Biol. 6:937–943.
   PubMedGoogle Scholar
• Li, Q., G. Estepa, S. Memet, A. Israel, and I. M. Verma. 2000. Complete lack of NF-kappaB activity in IKK1 and IKK2 double-deficient mice: additional defect in neurulation. Genes Dev. 14:1729–1733.
   PubMed Web of Science ®Google Scholar
• Li, Q., D. Van Antwerp, F. Mercurio, K. F. Lee, and I. M. Verma. 1999. Severe liver degeneration in mice lacking the IkappaB kinase 2 gene. Science 284:321–325.
   PubMed Web of Science ®Google Scholar
• Lin, C., B. D. Lindenbach, B. M. Pragai, D. W. McCourt, and C. M. Rice. 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.
   PubMed Web of Science ®Google Scholar
• Lohmann, V., F. Korner, U. Herian, and R. Bartenschlager. 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.
   PubMed Web of Science ®Google Scholar
• Manabe, S., I. Fuke, O. Tanishita, C. Kaji, Y. Gomi, S. Yoshida, C. Mori, A. Takamizawa, I. Yoshida, and H. Okayama. 1994. Production of nonstructural proteins of hepatitis C virus requires a putative viral protease encoded by NS3. Virology 198:636–644.
   PubMedGoogle Scholar
• May, M. J., and S. Ghosh. 1997. Rel/NF-kappaB and IkappaB proteins: an overview. Semin. Cancer Biol. 8:63–73.
   PubMed Web of Science ®Google Scholar
• Mercurio, F., H. Zhu, B. W. Murray, A. Shevchenko, B. L. Bennett, J. Li, D. B. Young, M. Barbosa, M. Mann, A. Manning, and A. Rao. 1997. IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation. Science 278:860–866.
   PubMed Web of Science ®Google Scholar
• Offringa, R., S. Gebel, H. van Dam, M. Timmers, A. Smits, R. Zwart, B. Stein, J. L. Bos, A. van der Eb, and P. Herrlich. 1990. A novel function of the transforming domain of E1a: repression of AP-1 activity. Cell 62:527–538.
   PubMedGoogle Scholar
• Oh, J. W., T. Ito, and M. M. C. Lai. 1999. A recombinant hepatitis C virus RNA-dependent RNA polymerase capable of copying the full-length viral RNA. J. Virol. 73:7694–7702.
   PubMed Web of Science ®Google Scholar
• Oh, J. W., G. T. Sheu, and M. M. C. Lai. 2000. Template requirement and initiation site selection by hepatitis C virus polymerase on a minimal viral RNA template. J. Biol. Chem. 275:17710–17717.
   PubMed Web of Science ®Google Scholar
• Osborn, L., S. Kunkel, and G. J. Nabel. 1989. Tumor necrosis factor alpha and interleukin 1 stimulate the human immunodeficiency virus enhancer by activation of the nuclear factor kappa B. Proc. Natl. Acad. Sci. USA 86:2336–2340.
   PubMed Web of Science ®Google Scholar
• Park, H. S., M. S. Kim, S. H. Huh, J. Park, J. Chung, S. S. Kang, and E. J. Choi. 2002. Akt (protein kinase B) negatively regulates SEK1 by means of protein phosphorylation. J. Biol. Chem. 277:2573–2578.
   PubMedGoogle Scholar
• Park, K. J., S. H. Choi, M. S. Koh, D. J. Kim, S. W. Yie, S. Y. Lee, and S. B. Hwang. 2001. Hepatitis C virus core protein potentiates c-Jun N-terminal kinase activation through a signaling complex involving TRADD and TRAF2. Virus Res. 74:89–98.
   PubMedGoogle Scholar
• Park, K. J., S. H. Choi, S. Y. Lee, S. B. Hwang, and M. M. C. Lai. 2002. Nonstructural 5A protein of hepatitis C virus modulates tumor necrosis factor α-stimulated nuclear factor κB activation. J. Biol. Chem. 277:13122–13128.
   PubMed Web of Science ®Google Scholar
• Park, K. J., S. H. Choi, D. H. Choi, J. M. Park, S. W. Yie, S. Y. Lee, and S. B. Hwang. 2003. Hepatitis C virus NS5A protein modulates c-Jun N-terminal kinase through interaction with tumor necrosis factor receptor-associated factor 2. J. Biol. Chem. 278:30711–30718.
   PubMedGoogle Scholar
• Penin, F., J. Dubuisson, F. A. Rey, D. Moradpour, and J. M. Pawlotsky. 2004. Structural biology of hepatitis C virus. Hepatology 39:5–19.
   PubMed Web of Science ®Google Scholar
• Regnier, C. H., H. Y. Song, X. Gao, D. V. Goeddel, Z. Cao, and M. Rothe. 1997. Identification and characterization of an IkappaB kinase. Cell 90:373–383.
   PubMed Web of Science ®Google Scholar
• Revilla, Y., M. Callejo, J. M. Rodriguez, E. Culebras, M. L. Nogal, M. L. Salas, E. Vinuela, and M. Fresno. 1998. Inhibition of nuclear factor kappaB activation by a virus-encoded IkappaB-like protein. J. Biol. Chem. 273:5405–5411.
   PubMedGoogle Scholar
• Rothwarf, D. M., E. Zandi, G. Natoli, and M. Karin. 1998. IKK-gamma is an essential regulatory subunit of the IkappaB kinase complex. Nature 395:297–300.
   PubMed Web of Science ®Google Scholar
• Rudolph, D., W. C. Yeh, A. Wakeham, B. Rudolph, D. Nallainathan, J. Potter, A. J. Elia, and T. W. Mak. 2000. Severe liver degeneration and lack of NF-kappaB activation in NEMO/IKKgamma-deficient mice. Genes Dev. 14:854–862.
   PubMed Web of Science ®Google Scholar
• Shao, R., M. C. Hu, B. P. Zhou, S. Y. Lin, P. J. Chiao, R. H. von Lindern, B. Spohn, and M. C. Hung. 1999. E1A sensitizes cells to tumor necrosis factor-induced apoptosis through inhibition of IkappaB kinases and nuclear factor kappaB activities. J. Biol. Chem. 274:21495–21498.
   PubMed Web of Science ®Google Scholar
• Shirota, Y., H. Luo, W. Qin, S. Kaneko, T. Yamashita, K. Kobayashi, and S. Murakami. 2002. Hepatitis C virus NS5A binds RNA-dependent RNA polymerase (RdRp) NS5B and modulates RNA-dependent RNA polymerase activity. J. Biol. Chem. 277:11149–11155.
   PubMed Web of Science ®Google Scholar
• Shrivastava, A., S. K. Manna, R. Ray, and B. B. Aggarwal. 1998. Etopic expression of hepatitis C virus core protein differentially regulates nuclear transcription factors. J. Virol. 72:9722–9728.
   PubMedGoogle Scholar
• Tanaka, M., M. E. Fuentes, K. Yamaguchi, M. H. Durnin, S. A. Dalrymple, K. L. Hardy, and D. V. Goeddel. 1999. Embryonic lethality, liver degeneration, and impaired NF-kappaB activation in IKK-beta-deficient mice. Immunity 10:421–429.
   PubMed Web of Science ®Google Scholar
• Thanos, D., and T. Maniatis. 1995. NF-kappaB: a lesson in family values. Cell 80:529–532.
   PubMed Web of Science ®Google Scholar
• Weil, R., H. Sirma, C. Giannini, D. Kremsdorf, C. Bessia, C. Dargemont, C. Brechot, and A. Israel. 1999. Direct association and nuclear import of the hepatitis B virus X protein with the NF-κB inhibitor IκBα. Mol. Cell. Biol. 19:6345–6354.
   PubMedGoogle Scholar
• Whiteside, S. T., and A. Israel. 1997. IkappaB proteins: structure, function and regulation. Semin. Cancer Biol. 8:75–82.
   PubMed Web of Science ®Google Scholar
• Woronicz, J. D., X. Gao, Z. Cao, M. Rothe, and D. V. Goeddel. 1997. IkappaB kinase-beta: NF-kappaB activation and complex formation with IkappaB kinase-alpha and NIK. Science 278:866–869.
   PubMed Web of Science ®Google Scholar
• Yamaoka, S., G. Courtois, C. Bessia, S. T. Whiteside, R. Weil, F. Agou, H. E. Kirk, R. J. Kay, and A. Israel. 1998. Complementation cloning of NEMO, a component of the IkappaB kinase complex essential for NF-kappaB activation. Cell 93:1231–1240.
   PubMed Web of Science ®Google Scholar
• Yamashita, T., S. Kaneko, Y. Shirota, W. Qin, T. Nomura, K. Kobayashi, and S. Murakami. 1998. RNA-dependent RNA polymerase activity of the soluble recombinant hepatitis C virus NS5B protein truncated at the C-terminal region. J. Biol. Chem. 273:15479–15486.
   PubMed Web of Science ®Google Scholar
• Yan, M., T. Dai, J. C. Deak, J. M. Kyriakis, L. I. Zon, J. R. Woodgett, and D. J. Templeton. 1994. Activation of stress-activated protein kinase by MEKK1 phosphorylation of its activator SEK1. Nature 372:798–800.
   PubMed Web of Science ®Google Scholar
• Zandi, E., D. M. Rothwarf, M. Delhase, M. Hayakawa, and M. Karin. 1997. The IkappaB kinase complex (IKK) contains two kinase subunits, IKKalpha and IKKbeta, necessary for IkappaB phosphorylation and NF-kappaB activation. Cell 91:243–252.
   PubMed Web of Science ®Google Scholar
• Zandi, E., Y. Chen, and M. Karin. 1998. Direct phosphorylation of IkappaB by IKKalpha and IKKbeta: discrimination between free and NF-kappaB-bound substrate. Science 281:1360–1363.
   PubMed Web of Science ®Google Scholar
• Zhu, N., A. Khoshnan, R. Schneider, M. Matsumoto, G. Dennert, C. Ware, and M. M. C. Lai. 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.
   PubMed Web of Science ®Google Scholar