Hepatitis C virus evasion from RIG-I-dependent hepatic innate immunity

Gastroenterology Research and Practice

Volumn , Issue , 2010, Pages

  Gale, Michael ^a   Liu, Helene Minyi ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; RECEPTOR; RETINOIC ACID INDUCIBLE PROTEIN I; RIG I LIKE RECEPTOR; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

GENE; HEPATITIS C VIRUS; HUMAN; INNATE IMMUNITY; INTERFERON PRODUCTION; INTERFERON STIMULATED GENE; LIVER CELL; MOLECULAR RECOGNITION; NONHUMAN; PERSISTENT VIRUS INFECTION; REVIEW; VIRUS IMMUNITY;

EID: 79952233520     PISSN: 16876121     EISSN: 1687630X     Source Type: Journal    
DOI: 10.1155/2010/548390     Document Type: Review

References (79)

1. Gale M., Effector genes of interferon action against hepatitis C virus Hepatology 2003 37 5 975 978
2. O'Neill L. A. J., Afte (Pubitemid 38314409)
3. McGettrick A. F., O'Neill L. A., Localisation and trafficking of Toll-like receptors: an important mode of regulation Current Opinion in Immunology 2010 22 1 20 27
4. Takeda K., Akira S., Toll-like receptors Current Protocols in Immunology 2007 14 14.12
5. Leulier F., Lemaitre B., Toll-like receptorstaking an evolutionary approach Nature Reviews Genetics 2008 9 3 165 178
6. Iwakiri D., Zhou L., Samanta M., Matsumoto M., Ebihara T., Seya T., Imai S., Fujieda M., Kawa K., Takada K., Epstein-Barr virus (EBV)-encoded small RNA is released from EBV-infected cells and activates signaling from Toll-like receptor 3 Journal of Experimental Medicine 2009 206 10 2091 2099
7. Koyama S., Ishii K. J., Kumar H., Tanimoto T., Coban C., Uematsu S., Kawai T., Akira S., Differential role of TLR- and RLR-signaling in the immune responses to influenza A virus infection and vaccination Journal of Immunology 2007 179 7 4711 4720
8. Zhang Y., Guo Y., Lv KE., Wang K., Sun S., Molecular cloning and functional characterization of porcine Toll-like receptor 7 involved in recognition of single-stranded RNA virus/ssRNA Molecular Immunology 2008 45 4 1184 1190 (Pubitemid 350016327)
9. Loo Y. M., Fornek J., Crochet N., Bajwa G., Perwitasari O., Martinez-Sobrido L., Akira S., Gill M. A., Garca-Sastre A., Katze M. G., Gale M., Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity Journal of Virology 2008 82 1 335 345 (Pubitemid 350309149)
10. Malmgaard L., Induction and regulation of IFNs during viral infections Journal of Interferon and Cytokine Research 2004 24 8 439 454 (Pubitemid 39120592)
11. Barnes B. J., Moore P. A., Pitha P. M., Virus-specific activation of a novel interferon regulatory factor, IRF-5, results in the induction of distinct interferon genes Journal of Biological Chemistry 2001 276 26 23382 23390
12. Kawai T., Sato S., Ishii K. J., Coban C., Hemmi H., Yamamoto M., Terai K., Matsuda M., Inoue J. I., Uematsu S., Takeuchi O., Akira S., Interferon- induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6 Nature Immunology 2004 5 10 1061 1068 (Pubitemid 41057726)
13. Hashimoto C., Hudson K. L., Anderson K. V., The Toll gene of drosophila, required for dorsal-ventral embryonic polarity, appears to encode a transmembrane protein Cell 1988 52 2 269 279
14. Lemaitre B., Nicolas E., Michaut L., Reichhart J. M., Hoffmann J. A., The dorsoventral regulatory gene cassette spatzle/Toll/Cactus controls the potent antifungal response in Drosophila adults Cell 1996 86 6 973 983 (Pubitemid 26336801)
15. Takeda K., Akira S., Toll-like receptors in innate immunity International Immunology 2005 17 1 1 14
16. Tsai Y. T., Chang S. Y., Lee C. N., Kao C. L., Human TLR3 recognizes dengue virus and modulates viral replication in vitro Cellular Microbiology 2009 11 4 604 615
17. Le Goffic R., Pothlichet J., Vitour D., Fujita T., Meurs E., Chignard M., Si-Tahar M., Cutting edge: influenza A virus activates TLR3-dependent inflammatory and RIG-I-dependent antiviral responses in human lung epithelial cells Journal of Immunology 2007 178 6 3368 3372 (Pubitemid 46417600)
18. Rudd B. D., Burstein E., Duckett C. S., Li X., Lukacs N. W., Differential role for TLR3 in respiratory syncytial virus-induced chemokine expression Journal of Virology 2005 79 6 3350 3357 (Pubitemid 40327923)
19. Huang S., Wei W., Yun Y., Upregulation of TLR7 and TLR3 gene expression in the lung of respiratory syncytial virus infected mice Wei Sheng Wu Xue Bao 2009 49 2 239 245
20. Ahmed M., Mitchell L. M., Puckett S., Brzoza-Lewis K. L., Lyles D. S., Hiltbold E. M., Vesicular stomatitis virus M protein mutant stimulates maturation of Toll-like receptor 7 (TLR7)-positive dendritic cells through TLR-dependent and-independent mechanisms Journal of Virology 2009 83 7 2962 2975
21. Mandl J. N., Barry A. P., Vanderford T. H., Kozyr N., Chavan R., Klucking S., Barrat F. J., Coffman R. L., Staprans S. I., Feinberg M. B., Divergent TLR7 and TLR9 signaling and type I interferon production distinguish pathogenic and nonpathogenic AIDS virus infections Nature Medicine 2008 14 10 1077 1087
22. Barchet W., Krug A., Cella M., Newby C., Fischer J. A. A., Dzionek A., Pekosz A., Colonna M., Dendritic cells respond to influenza virus through TLR7- and PKR-independent pathways European Journal of Immunology 2005 35 1 236 242 (Pubitemid 40123870)
23. Diebold S. S., Kaisho T., Hemmi H., Akira S., Reis E Sousa C., Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA Science 2004 303 5663 1529 1531 (Pubitemid 38314425)
24. Heil F., Ahmad-Nejad P., Hemmi H., Hochrein H., Ampenberger F., Gellert T., Dietrich H., Lipford G., Takeda K., Akira S., Wagner H., Bauer S., The Toll-like receptor 7 (TLR7)-specific stimulus loxoribine uncovers a strong relationship within the TLR7, 8 and 9 subfamily European Journal of Immunology 2003 33 11 2987 2997 (Pubitemid 37428331)
25. Krug A., French A. R., Barchet W., Fischer J. A. A., Dzionek A., Pingel J. T., Orihuela M. M., Akira S., Yokoyama W. M., Colonna M., TLR9-dependent recognition of MCMV by IPC and DC generates coordinated cytokine responses that activate antiviral NK cell function Immunity 2004 21 1 107 119 (Pubitemid 38925271)
26. Lund J., Sato A., Akira S., Medzhitov R., Iwasaki A., Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells Journal of Experimental Medicine 2003 198 3 513 520 (Pubitemid 36976063)
27. Diebold S. S., Massacrier C., Akira S., Paturel C., Morel Y., Reis e Sousa C., Nucleic acid agonists for Toll-like receptor 7 are defined by the presence of uridine ribonucleotides European Journal of Immunology 2006 36 12 3256 3267 (Pubitemid 44932727)
28. Rutz M., Metzger J., Gellert T., Luppa P., Lipford G. B., Wagner H., Bauer S., Toll-like receptor 9 binds single-stranded CpG-DNA in a sequence- and pH-dependent manner European Journal of Immunology 2004 34 9 2541 2550 (Pubitemid 39302811)
29. Haas T., Metzger J., Schmitz F., Heit A., Mller T., Latz E., Wagner H., The DNA sugar backbone 2′ deoxyribose determines Toll-like receptor 9 activation Immunity 2008 28 3 315 323 (Pubitemid 351335308)
30. Chang S., Dolganiuc A., Szabo G., Toll-like receptors 1 and 6 are involved in TLR2-mediated macrophage activation by hepatitis C virus core and NS3 proteins Journal of Leukocyte Biology 2007 82 3 479 487 (Pubitemid 47367138)
31. Dolganiuc A., Oak S., Kodys K., Golenbock D. T., Finberg R. W., Kurt-Jones E., Szabo G., Hepatitis C core and nonstructural 3 proteins trigger Toll-like receptor 2-mediated pathways and inflammatory activation Gastroenterology 2004 127 5 1513 1524 (Pubitemid 39457776)
32. Abe T., Kaname Y., Hamamoto I., Tsuda Y., Wen X., Taguwa S., Moriishi K., Takeuchi O., Kawai T., Kanto T., Hayashi N., Akira S., Matsuura Y., Hepatitis C virus nonstructural protein 5A modulates the Toll-like receptor-MyD88-dependent signaling pathway in macrophage cell lines Journal of Virology 2007 81 17 8953 8966 (Pubitemid 47311439)
33. Wang N., Liang Y., Devaraj S., Wang J., Lemon S. M., Li K., Toll-like receptor 3 mediates establishment of an antiviral state against hepatitis C virus in hepatoma cells Journal of Virology 2009 83 19 9824 9834
34. Szabo G., Chang S., Dolganiuc A., Altered innate immunity in chronic hepatitis C infection: cause or effect? Hepatology 2007 46 4 1279 1290 (Pubitemid 350144792)
35. Yoneyama M., Kikuchi M., Matsumoto K., Imaizumi T., Miyagishi M., Taira K., Foy E., Loo Y. M., Gale M., Akira S., Yonehara S., Kato A., Fujita T., Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity Journal of Immunology 2005 175 5 2851 2858 (Pubitemid 41170502)
36. Saito T., Hirai R., Loo Y. M., Owen D., Johnson C. L., Sinha S. C., Akira S., Fujita T., Gale M., Regulation of innate antiviral defenses through a shared repressor domain in RIG-1 and LGP2 Proceedings of the National Academy of Sciences of the United States of America 2007 104 2 582 587 (Pubitemid 46123068)
37. Takahasi K., Kumeta H., Tsuduki N., Narita R., Shigemoto T., Hirai R., Yoneyama M., Horiuchi M., Ogura K., Fujita T., Inagaki F., Solution structures of cytosolic RNA sensor MDA5 and LGP2 C-terminal domains: identification of the RNA recognition loop in RIG-I-like receptors Journal of Biological Chemistry 2009 284 26 17465 17474
38. Kato H., Takeuchi O., Sato S., Yoneyama M., Yamamoto M., Matsui K., Uematsu S., Jung A., Kawai T., Ishii K. J., Yamaguchi O., Otsu K., Tsujimura T., Koh C. S., Reis E Sousa C., Matsuura Y., Fujita T., Akira S., Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses Nature 2006 441 1 101 105
39. Kato H., Takeuchi O., Mikamo-Satoh E., Hirai R., Kawai T., Matsushita K., Hiiragi A., Dermody T. S., Fujita T., Akira S., Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5 Journal of Experimental Medicine 2008 205 7 1601 1610 (Pubitemid 351962024)
40. Matikainen S., Ronni T., Hurme M., Pine R., Julkunen I., Retinoic acid activates interferon regulatory factor-1 gene expression in myeloid cells Blood 1996 88 1 114 123 (Pubitemid 26230678)
41. Dao C. T., Luo J. K., Zhang D. E., Retinoic acid-induced protein ISGylation is dependent on interferon signal transduction Blood Cells, Molecules, and Diseases 2006 36 3 406 413 (Pubitemid 43792437)
42. Yoneyama M., Kikuchi M., Natsukawa T., Shinobu N., Imaizumi T., Miyagishi M., Taira K., Akira S., Fujita T., The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses Nature Immunology 2004 5 7 730 737 (Pubitemid 39023305)
43. Sumpter R. Jr., Loo Y. M., Foy E., Li K., Yoneyama M., Fujita T., Lemon S. M., Gale M., Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I Journal of Virology 2005 79 5 2689 2699 (Pubitemid 40270547)
44. Gack M. U., Shin Y. C., Joo C. H., Urano T., Liang C., Sun L., Takeuchi O., Akira S., Chen Z., Inoue S., Jung J. U., TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity Nature 2007 446 7138 916 920 (Pubitemid 46633167)
45. Hornung V., Ellegast J., Kim S., Brzzka K., Jung A., Kato H., Poeck H., Akira S., Conzelmann K. K., Schlee M., Endres S., Hartmann G., 5 ′ -Triphosphate RNA is the ligand for RIG-I Science 2006 314 5801 994 997
46. Pichlmair A., Schulz O., Tan C. P., Nslund T. I., Liljestrm P., Weber F., Reis E Sousa C., RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′ -phosphates Science 2006 314 5801 997 1001 (Pubitemid 44749946)
47. Takahasi K., Yoneyama M., Nishihori T., Hirai R., Kumeta H., Narita R., Gale M., Inagaki F., Fujita T., Nonself RNA-sensing mechanism of RIG-I helicase and activation of antiviral immune responses Molecular Cell 2008 29 4 428 440
48. Saito T., Owen D. M., Jiang F., Marcotrigiano J., Gale M., Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA Nature 2008 454 7203 523 527
49. Chiu Y. H., MacMillan J. B., Chen Z. J., RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway Cell 2009 138 3 576 591
50. Ablasser A., Bauernfeind F., Hartmann G., Latz E., Fitzgerald K. A., Hornung V., RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate Nature Immunology 2009 10 10 1065 1072
51. Cui S., Eisencher K., Kirchhofer A., Brzzka K., Lammens A., Lammens K., Fujita T., Conzelmann K. K., Krug A., Hopfner K. P., The C-terminal regulatory domain is the RNA 5′ -triphosphate sensor of RIG-I Molecular Cell 2008 29 2 169 179 (Pubitemid 351172822)
52. Myong S., Cui S., Cornish P. V., Kirchhofer A., Gack M. U., Jung J. U., Hopfner K. P., Ha T., Cytosolic viral sensor RIG-I is a 5′ -triphosphate-dependent translocase on double-stranded RNA Science 2009 323 5917 1070 1074
53. Blight K. J., McKeating J. A., Rice C. M., Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication Journal of Virology 2002 76 24 13001 13014 (Pubitemid 35386984)
54. Saito T., Gale M., Differential recognition of double-stranded RNA by RIG-I-like receptors in antiviral immunity Journal of Experimental Medicine 2008 205 7 1523 1527 (Pubitemid 351962014)
55. Yanagi M., St. Claire M. M., Emerson S. U., Purcell R. H., Bukh J., In vivo analysis of the 3′ untranslated region of the hepatitis C virus after in vitro mutagenesis of an infectious cDNA clone Proceedings of the National Academy of Sciences of the United States of America 1999 96 5 2291 2295 (Pubitemid 29117907)
56. Song Y., Friebe P., Tzima E., Jnemann C., Bartenschlager R., Niepmann M., The hepatitis C virus RNA 3′ -untranslated region strongly enhances translation directed by the internal ribosome entry site Journal of Virology 2006 80 23 11579 11588 (Pubitemid 44788872)
57. Bradrick S. S., Walters R. W., Gromeier M., The hepatitis C virus 3′ -untranslated region or a poly(A) tract promote efficient translation subsequent to the initiation phase Nucleic Acids Research 2006 34 4 1293 1303
58. Ito T., Tahara S. M., Lai M. M. C., The 3′ -untranslated region of hepatitis C virus RNA enhances translation from an internal ribosomal entry site Journal of Virology 1998 72 11 8789 8796 (Pubitemid 28471822)
59. Moore C. B., Bergstralh D. T., Duncan J. A., Lei YU., Morrison T. E., Zimmermann A. G., Accavitti-Loper M. A., Madden V. J., Sun L., Ye Z., Lich J. D., Heise M. T., Chen Z., Ting J. P. Y., NLRX1 is a regulator of mitochondrial antiviral immunity Nature 2008 451 7178 573 577 (Pubitemid 351186265)
60. Tattoli I., Carneiro L. A., Jhanno M., Magalhaes J. G., Shu Y., Philpott D. J., Arnoult D., Girardin S. E., NLRX1 is a mitochondrial NOD-like receptor that amplifies NF- B and JNK pathways by inducing reactive oxygen species production EMBO Reports 2008 9 3 293 300 (Pubitemid 351330996)
61. Xu L., Xiao N., Liu F., Ren H., Gu J., Inhibition of RIG-I and MDA5-dependent antiviralm response by gC1qR at mitochondria Proceedings of the National Academy of Sciences of the United States of America 2009 106 5 1530 1535
62. hman T., Rintahaka J., Kalkkinen N., Matikainen S., Nyman T. A., Actin and RIG-I/MAVS signaling components translocate to mitochondria upon influenza a virus infection of human primary macrophages Journal of Immunology 2009 182 9 5682 5692
63. Cames F., Bonekamp N. A., Delille H. K., Schrader M., Organelle dynamics and dysfunction: a closer link between peroxisomes and mitochondria Journal of Inherited Metabolic Disease 2009 32 2 163 180
64. Gale M., Foy E. M., Evasion of intracellular host defence by hepatitis C virus Nature 2005 436 7053 939 945 (Pubitemid 41191669)
65. Brass V., Berke J. M., Montserret R., Blum H. E., Penin F., Moradpour D., Structural determinants for membrane association and dynamic organization of the hepatitis C virus NS3-4A complex Proceedings of the National Academy of Sciences of the United States of America 2008 105 38 14545 14550
66. Wlk B., Sansonno D., Krusslich H. G., Dammacco F., Rice C. M., Blum H. E., Moradpour D., Subcellular localization, stability, and trans-cleavage competence of the hepatitis C virus NS3-NS4A complex expressed in tetracycline-regulated cell lines Journal of Virology 2000 74 5 2293 2304 (Pubitemid 30091484)
67. Loo Y. M., Owen D. M., Li K., Erickson A. K., Johnson C. L., Fish P. M., Carney D. S., Wang T., Ishida H., Yoneyama M., Fujita T., Saito T., Lee W. M., Hagedorn C. H., Lau D. T. Y., Weinman S. A., Lemon S. M., Gale M., Viral and therapeutic control of IFN- promoter stimulator 1 during hepatitis C virus infection Proceedings of the National Academy of Sciences of the United States of America 2006 103 15 6001 6006
68. Lin W., Kim S. S., Yeung E., Kamegaya Y., Blackard J. T., Kim K. A., Holtzman M. J., Chung R. T., Hepatitis C virus core protein blocks interferon signaling by interaction with the STAT1 SH2 domain Journal of Virology 2006 80 18 9226 9235 (Pubitemid 44359995)
69. Meylan E., Curran J., Hofmann K., Moradpour D., Binder M., Bartenschlager R., Tschopp J., Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus Nature 2005 437 7062 1167 1172 (Pubitemid 41509355)
70. Foy E., Li K., Wang C., Sumpter R., Ikeda M., Lemon S. M., Gale M., Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease Science 2003 300 5622 1145 1148 (Pubitemid 36583099)
71. Li X. D., Sun L., Seth R. B., Pineda G., Chen Z. J., Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signaling protein off the mitochondria to evade innate immunity Proceedings of the National Academy of Sciences of the United States of America 2005 102 49 17717 17722 (Pubitemid 41803563)
72. Johnson C. L., Owen D. M., Gale M., Functional and therapeutic analysis of hepatitis C virus NS3 4A protease control of antiviral immune defense Journal of Biological Chemistry 2007 282 14 10792 10803 (Pubitemid 47093463)
73. Baril M., Racine M. E., Penin F., Lamarre D., MAVS dimer is a crucial signaling component of innate immunity and the target of hepatitis C virus NS3/4A protease Journal of Virology 2009 83 3 1299 1311
74. Tang E. D., Wang C. Y., MAVS self-association mediates antiviral innate immune signaling Journal of Virology 2009 83 8 3420 3428
75. Ferreon J. C., Ferreon A. C. M., Li K., Lemon S. M., Molecular determinants of TRIF proteolysis mediated by the hepatitis C virus NS3/4A protease Journal of Biological Chemistry 2005 280 21 20483 20492 (Pubitemid 40776748)
76. Li K., Foy E., Ferreon J. C., Nakamura M., Ferreon A. C. M., Ikeda M., Ray S. C., Gale M., Lemon S. M., Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF Proceedings of the National Academy of Sciences of the United States of America 2005 102 8 2992 2997 (Pubitemid 40299904)
77. Dansako H., Ikeda M., Kato N., Limited suppression of the interferon- production by hepatitis C virus serine protease in cultured human hepatocytes FEBS Journal 2007 274 16 4161 4176 (Pubitemid 47228632)
78. Dansako H., Ikeda M., Ariumi Y., Wakita T., Kato N., Double-stranded RNA-induced interferon-beta and inflammatory cytokine production modulated by hepatitis C virus serine proteases derived from patients with hepatic diseases Archives of Virology 2009 154 5 801 810
79. Soriano V., Peters M. G., Zeuzem S., New therapies for hepatitis C virus infection Clinical Infectious Diseases 2009 48 3 313 320