Evasion and disruption of innate immune signalling by hepatitis C and West Nile viruses

Cellular Microbiology

Volumn 11, Issue 6, 2009, Pages 880-888

  Suthar, Mehul S ^a   Gale Jr , Michael ^a,b   Owen, David M ^a,b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; INTERFERON; RETINOIC ACID INDUCIBLE PROTEIN I; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR;

3' UNTRANSLATED REGION; AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CELL COMPARTMENTALIZATION; CELL SURFACE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENETIC TRANSFECTION; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; IMMUNOMODULATION; IMMUNOSTIMULATION; INNATE IMMUNITY; MICROBIAL ACTIVITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN TARGETING; REGULATORY MECHANISM; SHORT SURVEY; SIGNAL TRANSDUCTION; SYMPTOM; VIRUS CELL INTERACTION; VIRUS ENCEPHALITIS; VIRUS GENOME; VIRUS REPLICATION; WEST NILE FLAVIVIRUS;

ANIMALS; HEPACIVIRUS; HUMANS; IMMUNITY, INNATE; INTERFERON TYPE I; SIGNAL TRANSDUCTION; WEST NILE VIRUS;

EQUIDAE; FLAVIVIRIDAE; HEPATITIS C VIRUS; RNA VIRUSES; WEST NILE VIRUS;

EID: 65549134705     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2009.01311.x     Document Type: Short Survey

References (79)

1. Abe T., Kaname, Y., Hamamoto, I., Tsuda, Y., Wen, X., Taguwa, S., et al. (2007) Hepatitis C virus nonstructural protein 5A modulates the toll-like receptor-MyD88-dependent signalling pathway in macrophage cell lines. J Virol 81: 8953-8966.
2. Akira, S., Uematsu, S., and Takeuchi, O. (2006) Pathogen recognition and innate immunity. Cell 124: 783-801.
3. Alexopoulou, L., Holt, A.C., Medzhitov, R., and Flavell, R.A. (2001) Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413: 732-738.
4. Bartenschlager, R., Lohmann, V., Wilkinson, T., and Koch, J.O. (1995) Complex formation between the NS3 serine-type proteinase of the hepatitis C virus and NS4A and its importance for polyprotein maturation. J Virol 69: 7519-7528.
5. Bode, J.G., Ludwig, S., Ehrhardt, C., Albrecht, U., Erhardt, A., Schaper, F., et al. (2003) IFN-alpha antagonistic activity of HCV core protein involves induction of suppressor of cytokine signalling-3. FASEB J 17: 488-490.
6. Breiman, A., Grandvaux, N., Lin, R., Ottone, C., Akira, S., Yoneyama, M., et al. (2005) Inhibition of RIG-I-dependent signalling to the interferon pathway during hepatitis C virus expression and restoration of signalling by IKK{varepsilon}. J Virol 79: 3969-3978.
7. CDC (2008) West Nile virus activity -United States, 2007. MMWR Morb Mortal Wkly Rep 57: 720-723.
8. Chang, S., Dolganiuc, A., and Szabo, G. (2007) Toll-like receptors 1 and 6 are involved in TLR2-mediated macrophage activation by hepatitis C virus core and NS3 proteins. J Leukoc Biol 82: 479-487.
9. Chen, L., Borozan, I., Feld, J., Sun, J., Tannis, L.L., Coltescu, C., et al. (2005) Hepatic gene expression discriminates responders and nonresponders in treatment of chronic hepatitis C viral infection. Gastroenterology 128: 1437-1444.
10. Chen, Z., Benureau, Y., Rijnbrand, R., Yi, J., Wang, T., Warter, L., et al. (2007) GB virus B disrupts RIG-I signaling by NS3/4A-mediated cleavage of the adaptor protein MAVS. J Virol 81: 964-976.
11. Cheng, G., Zhong, J., and 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 USA 103: 8499-8504.
12. Daffis, S., Samuel, M.A., Keller, B.C., Gale, M. Jr and Diamond, M.S. (2007) Cell-specific IRF-3 responses protect against West Nile virus infection by interferon-dependent and -independent mechanisms. PLoS Pathog 3: E106.
13. Daffis, S., Samuel, M.A., Suthar, M.S., Keller, B.C., Gale, M., Jr, and Diamond, M.S. (2008a) Interferon regulatory factor IRF-7 induces the antiviral alpha interferon response and protects against lethal West Nile virus infection. J Virol 82: 8465-8475.
14. Daffis, S., Samuel, M.A., Suthar, M.S., Gale, M., Jr, and Diamond, M.S. (2008b) Toll-like receptor 3 has a protective role against West Nile virus infection. J Virol 82: 10349-10358.
15. Dansako, H., Ikeda, M., and Kato, N. (2007) Limited suppression of the interferon-beta production by hepatitis C virus serine protease in cultured human hepatocytes. FEBS J 274: 4161-4176.
16. Davis, L.E., Debiasi, R., Goade, D.E., Haaland, K.Y., Harrington, J.A., Harnar, J.B., et al. (2006) West Nile virus neuroinvasive disease. Ann Neurol 60: 286-300.
17. Debiasi, R.L., Parsons, J.A., and Grabert, B.E. (2005) West Nile virus meningoencephalitis in an immunocompetent adolescent. Pediatr Neurol 33: 217-219.
18. Diebold, S.S., Kaisho, T., Hemmi, H., Akira, S., and Reis e Sousa (2004) Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303: 1529-1531.
19. Dolganiuc, A., Oak, S., Kodys, K., Golenbock, D.T., Finberg, R.W., Kurt-Jones, E., and Szabo, G. (2004) Hepatitis C core and nonstructural 3 proteins trigger toll-like receptor 2-mediated pathways and inflammatory activation. Gastroenterology 127: 1513-1524.
20. Emig, M., and Apple, D.J. (2004) Severe West Nile virus disease in healthy adults. Clin Infect Dis 38: 289-292.
21. Evans, J.D., and Seeger, C. (2007) Differential effects of mutations in NS4B on West Nile virus replication and inhibition of interferon signalling. J Virol 81: 11809-11816.
22. Feld, J.J., and Hoofnagle, J.H. (2005) Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 436: 967-972.
23. Fischer, S.A. (2008) Emerging viruses in transplantation: There is more to infection after transplant than CMV and EBV. Transplantation 86: 1327-1339.
24. Foy, E., Li, K., Wang, C., Sumpter, R., 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.
25. Foy, E., Li, K., Sumpter, R., Jr, Loo, Y.M., Johnson, C.L., Wang, C., et al. (2005) Control of antiviral defenses through hepatitis C virus disruption of retinoic acid-inducible gene-I signalling. Proc Natl Acad Sci USA 102: 2986-2991.
26. Fredericksen, B.L., and Gale, M., Jr (2006) West Nile virus evades activation of interferon regulatory factor 3 through RIG-I-dependent and -independent pathways without antagonizing host defense signalling. J Virol 80: 2913-2923.
27. Fredericksen, B.L., Smith, M., Katze, M.G., Shi, P.Y., and Gale, M., Jr (2004) The host response to West Nile Virus infection limits viral spreadthrough the activation of the interferon regulatory factor 3 pathway. J Virol 78: 7737-7747.
28. Fredericksen, B.L., Keller, B.C., Fornek, J., Katze, M.G., and Gale, M., Jr (2008) Establishment and maintenance of the innate antiviral response to West Nile virus involves both RIG-I and MDA5 signalling through IPS-1. J Virol 82: 609-616.
29. Gack, M.U., Shin, Y.C., Joo, C.H., Urano, T., Liang, C., Sun, L., et al. (2007) TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446: 916-920.
30. Gubler, D.J., Kuno, G., and Markoff, L. (2007) Flaviviruses. In Fields Virology. Knipe, D.M., and Howley, P.M. (eds). Philadelphia: Lippincott Williams and Wilkins, pp. 1153-1252.
31. Guo, B., and Cheng, G. (2007) Modulation of the interferon antiviral response by the TBK1/IKKi adaptor protein TANK. J Biol Chem 282: 11817-11826.
32. Guo, J.T., Hayashi, J., and Seeger, C. (2005) West Nile virus inhibits the signal transduction pathway of alpha interferon. J Virol 79: 1343-1350.
33. Hayes, E.B., Sejvar, J., Zaki, S., Lanciotti, R., Bode, A., and Campbell, G. (2005) Virology, pathology, and clinical manifestations of West Nile Virus disease. Emerg Infect Dis 11: 1174-1296.
34. Heil, F., Hemmi, H., Hochrein, H., Ampenberger, F., Kirschning, C., Akira, S., et al. (2004) Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 303: 1526-1529.
35. Hornung, V., Ellegast, J., Kim, S., Brzozka, K., Jung, A., Kato, H., et al. (2006) 5′-Triphosphate RNA is the ligand for RIG-I. Science 314: 994-997.
36. Horvath, C.M. (2004) The Jak-STAT pathway stimulated by interferon alpha or interferon beta. Sci STKE 2004: Tr10.
37. Ishikawa, H., and Barber, G.N. (2008) STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455: 674-678.
38. Johnson, C.L., and Gale, M., Jr (2005) CARD games between virus and host get a new player. Trends Immunol 27: 1-4.
39. Johnson, C.L., Owen, D.M., and Gale, M. Jr (2007) Functional and therapeutic analysis of hepatitis C virus NS3/4A protease control of antiviral immune defense. J Biol Chem 282: 10792-10803.
40. Kang, D.C., Gopalkrishnan, R.V., Wu, Q., Jankowsky, E., Pyle, A.M., and Fisher, P.B. (2002) MDA5: An interferon-inducible putative RNA helicase with double-stranded RNA-dependent ATPase activity and melanoma growth-suppressive properties. Proc Natl Acad Sci USA 99: 637-642.
41. Kato, H., Takeuchi, O., Mikamo-Satoh, E., Hirai, R., Kawai, T., Matsushita, K., et al. (2008) Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J Exp Med 205: 1601-1610.
42. Kawai, T., Takahashi, K., Sato, S., Coban, C., Kumar, H., Kato, H., et al. (2005) IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 6: 981-988.
43. Keller, B.C., Fredericksen, B.L., Samuel, M.A., Mock, R.E., Mason, P.W., Diamond, M.S., and Gale, M., Jr (2006) Resistance to alpha/beta interferon is a determinant of west nile virus replication fitness and virulence. J Virol 80: 9424-9434.
44. Lanciotti, R.S., Roehrig, J.T., Deubel, V., Smith, J., Parker, M., Steele, K., et al. (1999) Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science 286: 2333-2337.
45. Lanciotti, R.S., Ebel, G.D., Deubel, V., Kerst, A.J., Murri, S., Meyer, R., et al. (2002) Complete genome sequences and phylogenetic analysis of West Nile virus strains isolated from the United States, Europe, and the Middle East. Virology 298: 96-105.
46. Lauer, G.M., and Walker, B.D. (2001) Hepatitis C virus infection. N Engl J Med 345: 41-52.
47. Li, X.D., Sun, L., Seth, R.B., Pineda, G., and Chen, Z. J. (2005a) Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signalling protein off the mitochondria to evade innate immunity. Proc Natl Acad Sci USA 102: 17717-17722.
48. Li, K., Foy, E., Ferreon, J.C., Nakamura, M., Ferreon, A.C., Ikeda, M., et al. (2005b) Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the toll-like receptor 3 adaptor protein TRIF. Proc Natl Acad Sci USA 102: 2992-2997.
49. Lin, R., Lacoste, J., Nakhaei, P., Sun, Q., Yang, L., Paz, S., et al. (2006) Dissociation of a MAVS/IPS-1/VISA/Cardif-IKKepsilon molecular complex from the mitochondrial outer membrane by hepatitis C virus NS3-4A proteolytic cleavage. J Virol 80: 6072-6083.
50. Liu, W.J., Wang, X.J., Mokhonov, V.V., Shi, P.Y., Randall, R., and Khromykh, A.A. (2005) Inhibition of interferon signalling by the New York 99 strain and Kunjin subtype of West Nile virus involves blockage of STAT1 and STAT2 activation by nonstructural proteins. J Virol 79: 1934-1942.
51. Lohmann, V., Hoffmann, S., Herian, U., Penin, F., and Bartenschlager, R. (2003) Viral and cellular determinants of hepatitis C virus RNA replication in cell culture. J Virol 77: 3007-3019.
52. Loo, Y.M., Owen, D.M., Li, K., Erickson, A.K., Johnson, C.L., Fish, P.M., et al. (2006) Viral and therapeutic control of IFN-beta promoter stimulator 1 during hepatitis C virus infection. Proc Natl Acad Sci USA 103: 6001-6006.
53. Maheshwari, A., Ray, S., and Thuluvath, P.J. (2008) Acute hepatitis C. Lancet 372: 321-332.
54. Marques, J.T., Devosse, T., Wang, D., Zamanian-Daryoush, M., Serbinowski, P., Hartmann, R., et al. (2006) A structural basis for discriminating between self and nonself double-stranded RNAs in mammalian cells. Nat Biotechnol 24: 559-565.
55. Matsumoto, M., Funami, K., Tanabe, M., Oshiumi, H., Shingai, M., Seto, Y., et al. (2003) Subcellular localization of Toll-like receptor 3 in human dendritic cells. J Immunol 171: 3154-3162.
56. Meylan, E., Curran, J., Hofmann, K., Moradpour, D., Binder, M., Bartenschlager, R., and 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.
57. Moradpour, D., Penin, F., and Rice, C.M. (2007) Replication of hepatitis C virus. Nat Rev Micro 5: 453-463.
58. Munoz-Jordan, J.L., Laurent-Rolle, M., Ashour, J., Martinez-Sobrido, L., Ashok, M., Lipkin, W.I., and Garcia-Sastre, A. (2005) Inhibition of alpha/beta interferon signalling by the NS4B protein of flaviviruses. J Virol 79: 8004-8013.
59. Saito, T., and Gale, M., Jr (2008) Differential recognition of double-stranded RNA by RIG-I-like receptors in antiviral immunity. J Exp Med 205: 1523-1527.
60. Saito, T., Hirai, R., Loo, Y.M., Owen, D., Johnson, C.L., Sinha, S.C., et al. (2006) Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2. Proc Natl Acad Sci USA 104: 582-587.
61. Saito, T., Owen, D.M., Jiang, F., Marcotrigiano, J., and Gale, M., Jr (2008) Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 454: 523-527.
62. Samuel, M.A., and Diamond, M.S. (2006) Pathogensis of West NIle virus infection: A balance between virulence, innate and adaptive immunity, and viral evasion. J Virol 80: 9349-9360.
63. Schroder, M., Baran, M., and Bowie, A.G. (2008) Viral targeting of DEAD box protein 3 reveals its role in TBK1/IKKepsilon-mediated IRF activation. EMBO J 27: 2147-2157.
64. Sen, G.C. (2001) Viruses and interferons. Annu Rev Microbiol 55: 255-281.
65. Seth, R.B., Sun, L., Ea, C.K., and Chen, Z.J. (2005) Identification and characterization of MAVS, a mitochondrial antiviral signalling protein that activates NF-kappaB and IRF 3. Cell 122: 669-682.
66. Simmonds, P. (2004) Genetic diversity and evolution of hepatitis C virus -15 years on. J Gen Virol 85: 3173-3188.
67. Smith, M.W., Walters, K.A., Korth, M.J., Fitzgibbon, M., Proll, S., Thompson, J.C., et al. (2006) Gene expression patterns that correlate with hepatitis C and early progression to fibrosis in liver transplant recipients. Gastroenterology 130: 179-187.
68. Smithburn, K.C., Hughes, T.P., Burke, A.W., and Paul, J.H. (1940) A neurotropic virus isolated from the blood of a native of Uganda. Am J Trop Med Hyg 20: 471-492.
69. Sumpter, R., Loo, Y.-M., Foy, E., Li, K., Yoneyama, M., Fujita, T., et al. (2005) Regulating intracellular anti-viral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J Virol 79: 2689-2699.
70. Takahasi, K., Yoneyama, M., Nishihori, T., Hirai, R., Kumeta, H., Narita, R., et al. (2008) Nonself RNA-sensing mechanism of RIG-I helicase and activation of antiviral immune responses. Mol Cell 29: 428-440.
71. Venkataraman, T., Valdes, M., Elsby, R., Kakuta, S., Caceres, G., Saijo, S., et al. (2007) Loss of DExD/H box RNA helicase LGP2 manifests disparate antiviral responses. J Immunol 178: 6444-6455.
72. Walsh, M.J., Jonsson, J.R., Richardson, M.M., Lipka, G.M., Purdie, D.M., Clouston, A.D., and Powell, E.E. (2006) Non-response to antiviral therapy is associated with obesity and increased hepatic expression of suppressor of cytokine signalling 3 (SOCS-3) in patients with chronic hepatitis C, viral genotype 1. Gut 55: 529-535.
73. Walters, K.A., Joyce, M.A., Thomson, J., Smith, M.W., Ueh, M.M., Proll, S., et al. (2006) Host-specific response to HCV infection in the chimeric SCID-beige/Alb-uPA mouse model: Role of the innate antiviral immune response. Plos Pathog 2: 1-12.
74. Walters, K.A., and Katze, M.G. (2009) Using high-throughput genomics to study hepatitis C: What determines the outcome of infection? Antiviral Res 81: 198-208.
75. Wang, T., Town, T., Alexopoulou, L., Anderson, J.F., Fikrig, E., and Flavell, R.A. (2004) Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat Med 10: 1366-1373.
76. Wilson, J.R., de Sessions, P.F., Leon, M.A., and Scholle, F. (2008) West Nile virus nonstructural protein 1 inhibits TLR3 signal transduction. J Virol 82: 8262-8271.
77. Xu, L.G., Wang, Y.Y., Han, K.J., Li, L.Y., Zhai, Z., and Shu, H.B. (2005) VISA Is an Adapter Protein Required for Virus-Triggered IFN-beta Signalling. Mol Cell 19: 727-740.
78. Yoneyama, M., Kikuchi, M., Matsumoto, K., Imaizumi, T., Miyagishi, M., Taira, K., et al. (2005) Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J Immunol 175: 2851-2858.
79. Yoneyama, M., Kikuchi, M., Natsukawa, T., Shinobu, N., Imaizumi, T., Miyagishi, M., et al. (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5: 730-737.