Inhibition of RIG-I-dependent signaling to the interferon pathway during hepatitis C virus expression and restoration of signaling by IKKε

Journal of Virology

Volumn 79, Issue 7, 2005, Pages 3969-3978

  Breiman, Adrien ^a   Grandvaux, Nathalie ^b   Lin, Rongtuan ^b   Ottone, Catherine ^a   Akira, Shizuo ^c   Yoneyama, Mitsutoshi ^d   Fujita, Takashi ^d   Hiscott, John ^b   Meurs, Eliane F ^a  

^a INSTITUT PASTEUR   (France)

^b MCGILL UNIVERSITY   (Canada)

^c OSAKA UNIVERSITY   (Japan)

^d TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; I KAPPA B KINASE; I KAPPA B KINASE EPSILON; INTERFERON; INTERFERON REGULATORY FACTOR 3; NONSTRUCTURAL PROTEIN 3; PROTEIN KINASE; PROTEIN RIG I; PROTEINASE; TANK BINDING KINASE 1; TOLL LIKE RECEPTOR; TRIF PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; FIBROBLAST; GENE OVEREXPRESSION; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; INNATE IMMUNITY; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; PROTEINASE INHIBITION; REPLICON; SIGNAL TRANSDUCTION; TRANSACTIVATION; TRANSCRIPTION REGULATION; VIRUS CELL INTERACTION; VIRUS REPLICATION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CELL LINE; CELL LINE, TUMOR; DEAD-BOX RNA HELICASES; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; HEPACIVIRUS; HUMANS; I-KAPPA B KINASE; IMMUNITY, NATURAL; INTERFERON REGULATORY FACTOR-3; INTERFERON-BETA; MEMBRANE GLYCOPROTEINS; MICE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; REPLICON; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA HELICASES; RNA, MESSENGER; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; TRANSCRIPTION FACTORS;

EID: 15244346528     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.7.3969-3978.2005     Document Type: Article

References (68)

1. Abbate, I., M. Romano, R. Longo, G. Cappiello, O. Lo Iacono, V. Di Marco, C. Paparella, A. Spano, and M. R. Capobianchi. 2003. Endogenous levels of mRNA for IFNs and IFN-rclated genes in hepatic biopsies of chronic HCV-infected and non-alcoholic steatohepatitis patients. J. Med. Virol. 70:581-587.
2. Alexopoulou, L., A. C. Holt, R. Medzhitov, and R. A. Flavell. 2001. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413:732-738.
3. Bain, C., A. Fatmi, Z. Zoulim, J. P. Zarski, C. Trepo, and G. Inschauspe. 2001. Impaired allostimulatory function of dendritic cells in chronic hepatitis C infection. Gastroenterology 120:512-524.
4. Bartenschlager, B. 1999. The NS3/4A proteinase of the hepatitis C virus: unravelling structure and function of an unusual enzyme and a prime target for antiviral therapy. J. Viral Hepatitis 6:165-181.
5. Bartenschlager, R., and V. Lohmann. 2001. Novel cell cultures systems for the hepatitis C virus. Antiviral Res. 52:1-17.
6. Barton, G. M., and R. Medzhitov. 2003. Toll-like receptors signaling pathways. Science 300:1524-1625.
7. Basler, C. F., A. Mikulasova, L. Martinez-Sobrido, J. Paragas, E. Muhlberger, M. Bray, H. D. Klenk, P. Palese, and A. Garcia-Sastre. 2003. The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J. Virol. 77:7945-7956.
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. Blight, K. J., J. A. McKeating, J. Marcotrigiano, and C. M. Rice. 2003. Efficient replication of hepatitis C virus genotype 1a RNAs in cell culture. J. Virol. 77:181-190.
10. Bonnard, M., C. Mirtsos, S. Suzuki, K. Graham, J. Huang, M. Ng, A. Itie, A. Wakeham, A. Shahinian, W. J. Henzel, A. J. Elia, W. Shillinglaw, T. W. Mak, Z. Cao, and W. C. Yeh. 2000. Deficiency of T2K leads to apoptotic liver degeneration and impaired NF-kappaB-dependent gene transcription. EMBO J. 19:4976-4985.
11. Briere, F., N. Bendriss-Vermare, T. Delale, S. Burg, C. Corbet, M. C. Rissoan, L. Chaperot, J. Plumas, M. C. Jacob, G. Trinchieri, and E. E. Bates. 2002. Origin and filiation of human plasmacytoid dendritic cells. Hum. Immunol. 63:1081-1093.
12. Cao, Z., J. Xiong, M. Takeuchi, T. Kurama, and D. V. Goeddel. 1996. TRAF6 is a signal transducer for interleukin-1. Nature 383:443-446.
13. Castet, V., C. Fournier, A. Soulier, R. Brillet, J. Coste, D. Larrey, D. Dhumeaux, P. Maurel, and J. M. Pawlotski. 2002. Alpha interferon Inhibits hepatitis C virus replication in primary human hepatocytes infected in vitro. J. Virology. 76:8189-8199.
14. Chariot, A., A. Leonardi, J. Müller, M. Bonif, K. Brown, and U. Siebenlist. 2002. Association of the adaptor TANK with th IkB kinase (IKK) regulator NEMO connects IKK complexes with IKKe and TBKI kinases. J. Biol. Chem. 277:37029-37036.
15. Choo, Q. L., G. Kuo, A. J. Weiner, L. R. Overby, D. W. Bradley, and M. Houghton. 1989. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 244:359-362.
16. Diebold, S., T. Kaisho, H. Hemmi, S. Akira, and C. Reis e Sousa. 2004. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 300:1529-1531.
17. Fitzgerald, K. A., D. C. Rowe, B. J. Barnes, D. R. Caffrey, A. Visintin, E. Latz, B. Monks, P. M. Pitha, and D. T. Golenbock. 2003. LPS-TLR4 signaling to IRF-3/7 and NF-B involves the Toll Adapters TRAM and TRIF. J. Exp. Med. 198:1043-1055.
18. Fitzgerald, K. A., M. S.M., K. L. Faia, D. C. Rowe, E. Latz, D. T. Golenbock, A. J. Coyle, S.-M. Liao, and T. Maniatis. 2003. IKKepsilon and TBK-1 are essential components of the IRF-3 signaling pathway. Nat. Immunol. 4:491-496.
19. Fournier, C., C. Sureau, J. Coste, J. Ducos, G. Pageaux, D. Larrey, J. Domergue, and P. Maurel. 1998. In vitro infection of adult normal human hepatocytes in primary culture by hepatitis C virus. J. Gen. Virol. 79:2367-2374.
20. Foy, E., K. Li, C. Y. Wang, R. J. Sumpter, M. Ikeda, S. M. Lemon, and M. Gale. 2003. regulation of Interferon regulatory Factor-3 by the Hepatitis C virus Serine Protease. Science 300:1145-1148.
21. François, C., G. Duverlie, D. Rebouillat, H. Khorsi, S. Castelain, H. E. Blum, A. Gatignol, C. Wychowski, D. Moradpour, and E. F. Meurs. 2000. Expression of hepatitis C virus proteins interferes with the antiviral action of interferon independently of PKR-mediated control of protein synthesis. J. Virol. 74:5587-5596.
22. Fredericksen, B., G. R. Akkaraju, E. Foy, C. Wang, J. Pflugheber, Z. J. Chen, and M. Gale, Jr. 2002. Activation of the interferon-beta promoter during hepatitis C virus RNA replication. Viral Immunol. 15:29-40.
23. Gallè, M. B., M. S. De Franco, D. Kerjaschki, R. G. Romanelli, P. Montalto, P. Gentilini, M. Pinzani, and P. Romagnoli. 2001. Ordered array of dendritic cells and CD8+ lymphocytes in portal infiltrates in chronic hepatitis C. Histopathology 39:373 .
24. Gowans, E. J., K. L. Jones, M. Bharadwaj, and D. C. Jackson. 2004. Prospects for dendritic cell vaccination in persistent infection with hepatitis C virus. J. Clin. Virol. 30:283-290.
25. Guo, J. T., V. V. Bichko, and C. Seeger. 2001. Effect of alpha interferon on the hepatitis C virus replicon. J. Virol. 75:8516-8523.
26. Honda, K., S. Sakaguchi, C. Nakajima, A. Watanabe, H. Yanai, M. Matsumoto, T. Ohteki, T. Kaisho, A. Takaoka, S. Akira, T. Seya, and T. Taniguchi. 2003. Selective contribution of IFN-alpha/beta signaling to the maturation of dendritic cells induced by double-stranded RNA or viral infection. Proc. Natl. Acad. Sci. USA 100:10872-10877.
27. Ikeda, M., M. Yi, K. Li, and S. M. 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.
28. Kawai, T., O. Takeuchi, T. Fujita, J. Inoue, P. F. Muhlradt, S. Sato, K. Hoshino, and S. Akira. 2001. Lipopolysaccharide stimulates the MyD88-independent pathway and results in activation of IFN-regulatory factor 3 and the expression of a subset of lipopolysaccharide-inducible genes. J. Immunol. 167:5887-5894.
29. Keskinen, P., M. Nyqvist, T. Sareneva, J. Pirhonen, K. Melen, and I. Julkunen. 1999. Impaired antiviral response in human hepatoma cells. Virology 263:364-375.
30. Kravchenko, V. V., J. C. Mathison, K. Schwamborn, F. Mercurio, and R. J. Ulevitch. 2003. IKKi/IKKepsilon plays a key role in integrating signals induced by pro-inflammatory stimuli. J. Biol. Chem. 278:26612-26619.
31. Lanford, R. E., B. Guerra, H. Lee, D. R. Averett, B. Pfeifler, D. Chavez, L. Notvall, and C. Bigger. 2003. 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. J. Virol. 77:1092-1104.
32. Lanford, R. E., C. Sureau, J. R. Jacob, R. White, and T. R. Fuerst. 1994. Demonstration of in vitro infection of chimpanzee hepatocytes with hepatitis C virus using strand-specific RT/PCR. Virology 202:606-614.
33. Le Bon, A, A., and D. F. Tough. 2002. Links between innate and adaptive immunity via type I interferon. Curr. Opin. Immunol. 14:432-436.
34. Lin, R., P. Genin, Y. Mamane, M. Sgarbanti, A. Battístí ní, W. J. J. Harrington, G. N. Barber, and J. Hiscott. 2001. HHV-8 encoded vIRF-1 represses the intcrferon antiviral response by blocking IRF-3 recruitment of the CBP/p300 coactivators. Oncogene 15:800-811.
35. Lin, R., Y. Mamane, and J. Hiscott. 2000. Multiple regulatory domains control IRF-7 activity in response to virus infection. J. Biol. Chem. 275: 34320-34327.
36. Lohmann, V., J. O. Koch, U. Herian, L. Theilmann, and B. Bartenschlager. 1999. Replication of subgenomic hepatitis C virus RNAs in a Hepatoma Cell line. Science 285:110-113.
37. Lohmann, V., F. Korner, A. Dobierzawska, and R. Bartenschlager. 2001. Mutations in Hepatitis C virus RNAs conferring cell culture adaptation. J. Virol. 75:1437-1449.
38. Longman, R. S., A. H. Talal, I. M. Jacobson, M. L. Albert, and C. M. Rice. 2004. Presence of functional dendritic cells in patients chronically infected with hepatitis C virus. Blood 103:1026-1029.
39. Lozach, P. Y., H. Lortat-Jacob, A. de Lacroix de Lavalette, I. Staropoli, S. Foung, A. Amara, C. Houles, F. Fieschi, O. Schwartz, J. L. Virelizier, F. Arenzana-Seisdedos, and R. Altmeyer. 2003. DC-SIGN and L-SIGN are high affinity binding receptors for hepatitis C virus glycoprotein E2. J. Biol. Chem. 278:20358-20366.
40. Lund, J. M., L. Alexopoulou, A. Sato, M. Karow, N. C. Adams, N. W. Gale, A. Iwasaki, and R. A. Flavell. 2004. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. USA 101:5598-5603.
41. Marie, I., J. E. Durbin, and D. E. Levy. 1998. Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7. EMBO J. 17:6660-6669.
42. McCormick, C. J., L. Challinor, A. Macdonald, D. J. Rowlands, and M. Harris. 2004. Introduction of replication-competent hepatitis C virus transcripts using a tetracycline-regulable baculovirus delivery system. J. Gen. Virol. 85:429-439.
43. Navas, M. C., A. Fuchs, E. Schvoerer, A. Bohbot, A. M. Aubertin, and F. Stoll-Keller. 2002. Dendritic cell susceptibility to Hepatitis C Genotype 1 infection. J. Med. Virol. 67:152-161.
44. Oshiumi, H., M. Sasai, K. Shida, T. Fujita, M. Matsumoto, and T. Seya. 2003. TIR-containing adapter molecule (TICAM)-2, a bridging adapter recruiting to toll-like receptor 4 TICAM-1 that induces interferon-beta. J. Biol. Chem. 278:49751-49762.
45. Paste, M., G. Huez, and V. Kruys. Deadenylation of interferon-b mRNA is mediated by both the AU-rich element in the 3′-untranslated region and an instability sequence in the coding region. Eur. J. Biochem 270:1590-1597.
46. Peters, R. T., S.-M. Liao, and T. Maniatis. 2000. IKKe is part of a novel PMA-inducible IkB kinase complex. Mol. Cell 5:513-522.
47. 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.
48. Pietschmann, T., V. Lohmann, A. Kaul, N. Krieger, G. Rinck, G. TRutter, D. Strand, and B. Bartenschlager. 2002. Persistent and transient replication of full-length hepatitis C virus genomes in cell culture. J. Virol. 76:4008-4021.
49. Pohlmann, S., J. Zhang, F. Baribaud, Z. Chen, G. J. Leslie, G. Lin, A. Granelli-Piperno, R. W. Doms, C. M. Rice, and J. A. McKeating. 2003. Hepatitis C virus glycoproteins interact with DC-SIGN and DC-SIGNR. J. Virol. 77:4070-4080.
50. Pomerantz, J. L., and D. Baltimore. 1999. NF-kappaB activation by a signaling complex containing TRAF2, TANK and TBK-1, a novel IKK-related kinase. EMBO J. 18:6694-6704.
51. Ronco, L. V., A. Y. Karpova, M. Vidal, and P. M. Howley. 1998. Human papillomavirus 16 E6 oncoproein binds to interferon regulatory factor-3 and inhibits its transcriptional activity. Genes Dev. 12:2061-2072.
52. Rosenberg, S. 2001. Recent advances in the molecular biology of hepatitis C virus. J. Mol. Biol. 313:451-464.
53. Rumin, S., P. Berthillon, E. Tanaka, K. Kiyosawa, M. A. Trabaud, T. Bizollon, C. Gouillat, P. Gripon, C. Guguen-Guillouzo, G. Inchauspe, and C. Trepo. 1999. Dynamic analysis of hepatitis C virus replication and quasispecies selection in long-term cultures of adult human hepatocytes infected in vitro. J. Gen. Virol. 80:3007-3018.
54. Sato, S., M. Sugiyama, M. Yamamoto, Y. Watanabe, T. Kawai, K. Takeda, and S. Akira. 2003. Toll/IL-1 receptor domain-containing adaptor inducing IFN-beta (TRIF) associates with TNF receptor-associated factor 6 and TANK-binding kinase 1, and activates two distinct transcription factors, NF-kappa B and IFN-regulatory factor-3, in the Toll-like receptor signaling. J. Immunol. 171:4304-4310.
55. Serafino, A., M. B. Valli, F. Andreola, A. Crema, G. Ravagnan, L. Bertolini, and G. Carloni. 2003. Suggested role of th Golgi Apparatus and endoplasmic reticulum for crucial sites of Hepatitis C virus replication in Hum. Lymphoblastoid cells infected in vitro. J. Med. Virol. 70:31-41.
56. Servant, M. J., N. Grandvaux, B. R. tenOever, D. Duguay, R. Lin, and J. Hiscott. 2003. Identification of the minimal phosphoacceptor site required for in vivo activation of interferon regulatory factor 3 in response to virus and double-stranded RNA. J. Biol. Chem. 278:9441-9447.
57. Sharma, S., B. R. tenOever, N. Grandvaux, G.-P. Zhou, R. Lin, and J. Hiscott. 2003. Triggering the interferon antiviral response through an IKk-related pathway. Science 300:1148-1151.
58. Shimada, T., T. Kawai, K. Takeda, M. Matsumoto, J. Inoue, Y. Tatsumi, A. Kanamaru, and S. Akira. 1999. IKK-i, a novel lipopolysaccharide-inducible kinase that is related to IKappaB kinases. Int. Immunol. 11:1357-1362.
59. Smith, E., I. Marie, A. Prakash, A. Garcia-Sastre, and D. E. Levy. 2000. IRF-3 and IRF7 phosphorylation in virus-infected cells does not require double-stranded RNA-dependent protein kinase R or IkB kinase but is blocked by vaccinia virus E3L protein. J. Biol. Chem. 276:8951-8957.
60. Sung, V. M.-H., S. Shimodaira, A. L. Doughty, G. R. Picchio, H. Can, B. Y. T.S., K. L. Lindsay, A. M. Levine, and M. C. Lai. 2003. Establishment of B-cell lymphoma cell lines persistently infected with hepatitis C virus in vivo and in vitro: the apoptotic effects of virus infection. J. Virol. 77:2314-2146.
61. Talon, J., C. M. Horvath, R. Polley, C. F. Basler, T. Muster, P. Palese, and A. Garcia-Sastre. 2000. Activation of interferon regulatory factor 3 is inhibited by the influenza A virus NS1 protein. J. Virol. 74:7989-7996.
62. Tojima, Y., A. Fujimoto, M. Delhase, Y. Chen, S. Hatakeyama, K. Nakayama, Y. Kaneko, Y. Nimura, N. Motoyama, I. K., K. M., and M. Nakanishi. 2000. NAK is an IkappaB kinase-activating kinase. Nature 404:778-782.
63. Wang, W., F. C. Lahser, M. Yi, J. Wright-Minogue, E. Xia, P. C. Weber, S. M. Lemon, and B. A. Malcolm. 2004. Conserved C-terminal threonine of hepatitis C virus NS3 regulates autoproteolysis and prevents product inhibition. J. Virol. 78:700-709.
64. Yamamoto, M., S. Sato, H. Hemmi, K. Hoshina, T. Kaisho, H. Sanjo, O. Takeuchi, M. Sugiyama, M. Okabe, K. Takeda, and S. Akira. 2003. Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science 301:640-643.
65. Yamamoto, M., S. Sato, K. Mori, K. Hoshino, O. Takeuchi, K. Takeda, and S. Akira. 2002. Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-beta promoter in the Toll-like receptor signaling. J. Immunol. 169:6668-6672.
66. Yoneyama, M., M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, M. Miyagishi, K. Taira, S. Akira, and T. Fujita. 2004. The RNA helicase RIG-1 has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol. 5:730-737.
67. Zennou, V., C. Petit, D. Guetard, U. Nerhbass, L. Montagnier, and P. Charneau. 2000. HIV-1 Genome Nuclear Import is mediated by a Central DNA Flap. Cell 101:173-185.
68. Zhu, Q., J. T. Guo, and C. Seeger. 2003. Replication of hepatitis C virus subgenomes in nonhepatic epithelial and mouse hepatoma cells. J. Virol. 77:9204-9210.