Hepatitis C virus proteins interfere with the activation of chemokine gene promoters and downregulate chemokine gene expression

Journal of General Virology

Volumn 89, Issue 2, 2008, Pages 432-443

  Sillanpää, Maarit ^a   Kaukinen, Pasi ^a   Melén, Krister ^a   Julkunen, Ilkka ^a  

^a NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; BETA INTERFERON; CARDIF PROTEIN; CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GLYCOPROTEIN E1; GLYCOPROTEIN E2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE KINASE; NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 4A; NONSTRUCTURAL PROTEIN 4B; POLYPROTEIN; PROTEIN C JUN; PROTEIN P50; PROTEIN P7; RANTES; SYNAPTOTAGMIN I; TRANSCRIPTION FACTOR AP 1; VIRUS PROTEIN; NS2 PROTEIN, HEPATITIS C VIRUS; NS3 PROTEIN, HEPATITIS C VIRUS; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENE EXPRESSION REGULATION; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; MITOCHONDRION; NONHUMAN; OSTEOSARCOMA CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SENDAI VIRUS; SIGNAL TRANSDUCTION; VIRUS INFECTION; VIRUS INFECTIVITY; CELL CULTURE; CHEMISTRY; DOWN REGULATION; DRUG EFFECT; GENETICS; HEPATITIS C; METABOLISM; PHYSIOLOGY; VIROLOGY;

HEPATITIS C VIRUS; SENDAI VIRUS;

CHEMOKINES; DOWN-REGULATION; GENE EXPRESSION REGULATION, VIRAL; HEPACIVIRUS; HEPATITIS C; MITOCHONDRIA; POLYPROTEINS; PROMOTER REGIONS (GENETICS); SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; VIRAL NONSTRUCTURAL PROTEINS;

EID: 41649113404     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.83316-0     Document Type: Article

References (57)

1. Alexopoulou, L., Holt, A. C., Medzhitov, R. & Flavell, R. A. (2001). Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 413, 732-738.
2. Barba, G., Harper, F., Harada, T., Kohara, M., Goulinet, S., Matsuura, Y., Eder, G., Schaff, Z., Chapman, M. J. & other authors (1997). Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. Proc Natl Acad Sci U S A 94, 1200-1205.
3. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
4. Casola, A., Garofalo, R. P., Jamaluddin, M., Vlahopoulos, S. & Brasier, A. R. (2000). Requirement of a novel upstream response element in respiratory syncytial virus-induced IL-8 gene expression. J Immunol 164, 5944-5951.
5. Cheng, G., Zhong, J. & Chisari, F. V. (2006). Inhibition of dsRNA-induced signaling in hepatitis C virus-infected cells by NS3 protease-dependent and -independent mechanisms. Proc Natl Acad Sci U S A 103, 8499-8504.
6. Chirgwin, J. M., Przybyla, A. E., MacDonald, R. J. & Rutter, W. J. (1979). Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18, 5294-5299.
7. Ciccaglione, A. R., Stellacci, E., Marcantonio, C., Muto, V., Equestre, M., Marsili, G., Rapicetta, M. & Battistini, A. (2007). Repression of interferon regulatory factor 1 by hepatitis C virus core protein results in inhibition of antiviral and immunomodulatory genes. J Virol 81, 202-214.
8. Ferreon, J. C., Ferreon, A. C., Li, K. & Lemon, S. M. (2005). Molecular determinants of TRIF proteolysis mediated by the hepatitis C virus NS3/4A protease. J Biol Chem 280, 20483-20492.
9. Foy, E., Li, K., Wang, C., Sumpter, R., Jr, Ikeda, M., Lemon, S. M. & Gale, M., Jr (2003). Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease. Science 300, 1145-1148.
10. Foy, E., Li, K., Sumpter, R., Jr, Loo, Y. M., Johnson, C. L., Wang, C., Fish, P. M., Yoneyama, M., Fujita, T. & other authors (2005). Control of antiviral defenses through hepatitis C virus disruption of retinoic acid-inducible gene-I signaling. Proc Natl Acad Sci U S A 102, 2986-2991.
11. Gack, M. U., Shin, Y. C., Joo, C. H., Urano, T., Liang, C., Sun, L., Takeuchi, O., Akira, S., Chen, Z. & other authors (2007). TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446, 916-920.
12. Gale, M., Jr & Foy, E. M. (2005). Evasion of intracellular host defence by hepatitis C virus. Nature 436, 939-945.
13. Genin, P., Algarte, M. Roof, P., Lin, R. & Hiscott, J. (2000). Regulation of RANTES chemokine gene expression requires cooperativity between NF-κB and IFN-regulatory factor transcription factors. J Immunol 164, 5352-5361.
14. Glisin, V., Crkvenjakov, R. & Byus, C. (1974). Ribonucleic acid isolated by cesium chloride centrifugation. Biochemistry 13, 2633-2637.
15. Green, J., Khabar, K. S., Koo, B. C., Williams, B. R. & Polyak, S. J. (2006). Stability of CXCL-8 and related AU-rich mRNAs in the context of hepatitis C virus replication in vitro. J Infect Dis 193, 802-811.
16. Griffin, S. D., Beales, L. P., Clarke, D. S., Worsfold, O., Evans, S. D., Jaeger, J., Harris, M. P. & Rowlands, D. J. (2003). The p7 protein of hepatitis C virus forms an ion channel that is blocked by the antiviral drug, Amantadine. FEBS Lett 535, 34-38.
17. Hoffmann, E., Dittrich-Breiholz, O., Holtmann, H. & Kracht, M. (2002). Multiple control of interleukin-8 gene expression. J Leukoc Biol 72, 847-855.
18. Hugle, T., Fehrmann, F., Bieck, E., Kohara, M., Krausslich, H. G., Rice, C. M., Blum, H. E. & Moradpour, D. (2001). The hepatitis C virus nonstructural protein 4B is an integral endoplasmic reticulum membrane protein. Virology 284, 70-81.
19. Kato, N., Yoshida, H., Kioko Ono-Nita, S., Kato, J., Goto, T., Otsuka, M., Lan, K., Matsushima, K., Shiratori, Y. & Omata, M. (2000). Activation of intracellular signaling by hepatitis B and C viruses: C-viral core is the most potent signal inducer. Hepatology 32, 405-412.
20. Kaukinen, P., Sillanpaa, M., Kotenko, S., Lin, R., Hiscott, J., Melen, K. & Julkunen, I. (2006). Hepatitis C virus NS2 and NS3/4A proteins are potent inhibitors of host cell cytokine/chemokine gene expression. Virol J 3, 66.
21. Kawai, T., Takahashi, K., Sato, S., Coban, C., Kumar, H., Kato, H., Ishii, K. J., Takeuchi, O. & Akira, S. (2005). IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 6, 981-988.
22. Koike, K. & Miyoshi, H. (2006). Oxidative stress and hepatitis C viral infection. Hepatol Res 34, 65-73
23. Koo, B. C., McPoland, P., Wagoner, J. P., Kane, O. J., Lohmann, V. & Polyak, S. J. (2006). Relationships between hepatitis C virus replication and CXCL-8 production in vitro. J Virol 80, 7885-7893.
24. Li, K., Foy, E., Ferreon, J. C., Nakamura, M., Ferreon, A. C., Ikeda, M., Ray, S. C., Gale, M., Jr & Lemon, S. M. (2005a). Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF. Proc Natl Acad Sci U S A 102, 2992-2997.
25. Li, X. D., Sun, L., Seth, R. B., Pineda, G. & Chen, Z. J. (2005b). Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signaling protein off the mitochondria to evade innate immunity. Proc Natl Acad Sci U S A 102, 17717-17722.
26. Lin, R., Lacoste, J., Nakhaei, P., Sun, O., Yang, L., Paz, S., Wilkinson, P., Julkunen, I., Vitour, D. & other authors (2006a). Dissociation of a MAVS/IPS-1/VISA/Cardif-IKKε molecular complex from the mitochondrial outer membrane by hepatitis C virus NS3-4A proteolytic cleavage. J Virol 80, 6072-6083.
27. Lin, W., Kim, S. S., Yeung, E., Kamegaya, Y., Blackard, J. T., Kim, K. A., Holtzman, M. J. & Chung, R. T. (2006b). Hepatitis C virus core protein blocks interferon signaling by interaction with the STAT1 SH2 domain. J Virol 80, 9226-9235.
28. Lindenbach, B. D. & Rice, C. M. (2005). Unravelling hepatitis C virus replication from genome to function. Nature 436, 933-938.
29. Loo, Y. M., Owen, D. M., Li, K., Erickson, A. K., Johnson, C. L., Fish, P. M., Carney, D. S., Wang, T., Ishida, H. & other authors (2006). Viral and therapeutic control of IFN-β promoter stimulator 1 during hepatitis C virus infection. Proc Natl Acad Sci U S A 103, 6001-6006.
30. Matikainen, S., Ronni, T., Hurme, M., Pine, R. & Julkunen, I. (1996). Retinoic acid activates interferon regulatory factor-1 gene expression in myeloid cells. Blood 88, 114-123.
31. Matikainen, S., Siren, J., Tissari, J., Veckman, V., Pirhonen, J., Severa, M., Sun, O., Lin, R., Meri, S. & other authors (2006). Tumor necrosis factor alpha enhances influenza A virus-induced expression of antiviral cytokines by activating RIG-I gene expression. J Virol 80, 3515-3522.
32. Melchjorsen, J., Jensen, S. B., Malmgaard, L., Rasmussen, S. B., Weber, F., Bowie, A. G., Matikainen, S. & Paludan, S. R. (2005). Activation of innate defense against a paramyxovirus is mediated by RIG-I and TLR7 and TLR8 in a cell-type-specific manner. J Virol 79, 12944-12951.
33. Melen, K., Fagerlund, R., Nyqvist, M., Keskinen, P. & Julkunen, I. (2004). Expression of hepatitis C virus core protein inhibits interferon-induced nuclear import of STATs. J Med Virol 73, 536-547.
34. Meylan, E., Curran, J., Hofmann, K., Moradpour, D., Binder, M., Bartenschlager, R. & Tschopp, J. (2005). Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437, 1167-1172.
35. Miettinen, M., Matikainen, S., Vuopio-Varkila, J., Pirhonen, J., Varkila, K., Kurimoto, M. & Juikunen, I. (1998). Lactobacilli and streptococci induce interleukin-12 (IL-12), IL-18, and gamma interferon production in human peripheral blood mononuclear cells. Infect Immun 66, 6058-6062.
36. Moradpour, D., Kary, P., Rice, C. M. & Blum, H. E. (1998). Continuous human cell lines inducibly expressing hepatitis C virus structural and nonstructural proteins. Hepatology 28, 192-201.
37. Moradpour, D., Brass, V., Gosert, R., Wolk, B. & Blum, H. E. (2002). Hepatitis C: molecular virology and antiviral targets. Trends Mol Med 8, 476-482.
38. Mukaida, N., Okamoto, S., Ishikawa, Y. & Matsushima, K. (1994). Molecular mechanism of interleukin-8 gene expression. J Leukoc Biol 56, 554-558.
39. Nomura-Takigawa, Y., Nagano-Fujii, M., Deng, L., Kitazawa, S., Ishido, S., Sada, K. & Hotta, H. (2006). Non-structural protein 4A of hepatitis C virus accumulates on mitochondria and renders the cells prone to undergoing mitochondria-mediated apoptosis. J Gen Virol 87, 1935-1945.
40. Ohmori, Y. & Hamilton, T. A. (1993). Cooperative interaction between interferon (IFN) stimulus response element and κB sequence motifs controls IFNγ- and lipopolysaccharide-stimulated transcription from the murine IP-10 promoter. J Biol Chem 268, 6677-6688.
41. Osterlund, P., Veckman, V., Siren, J., Klucher, K. M., Hiscott, J., Matikainen, S. & Julkunen, I. (2005). Gene expression and antiviral activity of alpha/beta interferons and interleukin-29 in virus-infected human myeloid dendritic cells. J Virol 79, 9608-9617.
42. Otsuka, M., Kato, N., Moriyama, M., Taniguchi, H., Wang, Y., Dharel, N., Kawabe, T. & Omata, M. (2005). Interaction between the HCV NS3 protein and the host TBK1 protein leads to inhibition of cellular antiviral responses. Hepatology 41, 1004-1012.
43. Piccoli, C., Scrima, R., D'Aprile, A., Ripoli, M., Lecce, L., Boffoll, D. & Capitanio, N. (2006). Mitochondrial dysfunction in hepatitis C virus infection. Biochim Biophys Acta 1757, 1429-1437.
44. Ray, R. B., Steele, R., Basu, A., Meyer, K., Majumder, M., Ghosh, A. K. & Ray, R. (2002). Distinct functional role of hepatitis C virus core protein on NF-κB regulation is linked to genomic variation. Virus Res 87, 21-29.
45. Schwer, B. Ren, S., Pietschmann, T., Kartenbeck, J., Kaehlcke, K., Bartenschlager, R., Yen, T. S. & Ott M. (2004). Targeting of hepatitis C virus core protein to mitochondria through a novel C-terminal localization motif. J Virol 78, 7958-7968.
46. Seth, R. B., Sun, L., Ea, C. K. & Chen, Z. J. (2005). Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-κB and IRF 3. Cell 122, 669-682.
47. Siren, J., Pirhonen, J., Julkunen, I. & Matikainen, S. (2005). IFN-α regulates TLR-dependent gene expression of IFN-α, IFN-β, IL-28, and IL-29. J Immunol 174, 1932-1937.
48. Veckman, V., Osterlund, P., Fagerlund, R., Melen, K., Matikainen, S. & Julkunen, I. (2006). TNF-α and IFN-α enhance influenza-A-virus-induced chemokine gene expression in human A549 lung epithelial cells. Virology 345, 96-104.
49. Wagoner, J., Austin, M., Green, J., Imaizumi, T., Casola, A., Brasier, A., Khabar, K. S., Wakita, T., Gale, M., Jr & Polyak, S. J. (2007). Regulation of CXCL-8 (interleukin-8) induction by double-stranded RNA signaling pathways during hepatitis C virus infection. J Virol 81, 309-318.
50. Wathelet, M. G., Lin, C. H., Parekh, B. S., Ronco, L. V., Howley, P. M. & Maniatis, T. (1998). Virus infection induces the assembly of coordinately activated transcription factors on the IFN-β enhancer in vivo. Mol Cell 1, 507-518.
51. Winzen, R., Kracht, M., Ritter, B., Wilhelm, A., Chen, C. Y., Shyu, A. B., Muller, M., Gaestel, M., Resch, K. & Holtmann, H. (1999). The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J 18, 4969-4980.
52. Winzen, R., Gowrishankar, G., Bollig, F., Redich, N., Resch, K. & Holtmann, H. (2004). Distinct domains of AU-rich elements exert different functions in mRNA destabilization and stabilization by p38 mitogen-activated protein kinase or HuR. Mol Cell Biol 24, 4835-4847.
53. Wolk, B., Sansonno, D., Krausslich, H. G., Dammacco, F., Rice, C. M., Blum, H. E. & Moradpour, D. (2000). Subcellular localization, stability, and trans-cleavage competence of the hepatitis C virus NS3-NS4A complex expressed in tetracycline-regulated cell lines. J Virol 74, 2293-2304.
54. Xu, L. G., Wang, Y. Y., Han, K. J., Li, L. Y., Zhai, Z. & Shu, H. B. (2005). VISA is an adapter protein required for virus-triggered IFN-β signaling. Mol Cell 19, 727-740.
55. Yamamoto, M., Sato, S., Mori, K., Hoshino, K., Takeuchi, O., Takeda, K. & Akira, S. (2002). Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-β promoter in the Toll-like receptor signaling. J Immunol 169, 6668-6672.
56. Yoneyama, M., Kikuchi, M., Natsukawa, T., Shinobu, N., Imaizumi, T., Miyagishi, M., Taira, K., Akira, S. & Fujita, T. (2004). The RNA helicase RIG-I has an essential function in double-stranded RNA-induced, innate antiviral responses. Nat Immunol 5, 730-737.
57. Zhao, T., Yang, L., Sun, O., Arguello, M., Ballard, D. W., Hiscott, J. & Lin, R. (2007). The NEMO adaptor bridges the nuclear factor-κB and interferon regulatory factor signaling pathways. Nat Immunol 8, 592-600.