Hepatitis C virus reveals a novel early control in acute immune response

PLoS Pathogens

Volumn 7, Issue 10, 2011, Pages

  Arnaud, Noëlla ^a   Dabo, Stéphanie ^a   Akazawa, Daisuke ^b   Fukasawa, Masayoshi ^b   Shinkai Ouchi, Fumiko ^b   Hugon, Jacques ^c   Wakita, Takaji ^b   Meurs, Eliane F ^a  

^a INSTITUT PASTEUR   (France)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^c INSTITUT DU FER À MOULIN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; INTERFERON STIMULATED GENE FACTOR 15; INTERFERON STIMULATED GENE FACTOR 3; PHOSPHOTRANSFERASE; RETINOIC ACID INDUCIBLE PROTEIN I; UNCLASSIFIED DRUG; VIRUS RNA; CYTOKINE; INTERFERON REGULATORY FACTOR 3; IRF3 PROTEIN, HUMAN; ISG15 PROTEIN, HUMAN; PROTEIN KINASE R; RARRES3 PROTEIN, HUMAN; RETINOIC ACID RECEPTOR; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMALL INTERFERING RNA; TRAF3 PROTEIN, HUMAN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 3; UBIQUITIN; VISA PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENE SILENCING; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INNATE IMMUNITY; LIVER CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; TRANSCRIPTOMICS; UBIQUITINATION; BIOSYNTHESIS; CELL LINE; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; METABOLISM; PATHOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; VIROLOGY;

HEPATITIS C VIRUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CELL LINE; CYTOKINES; EIF-2 KINASE; GENE EXPRESSION PROFILING; HEPACIVIRUS; HEPATOCYTES; HUMANS; INTERFERON REGULATORY FACTOR-3; INTERFERONS; RECEPTORS, RETINOIC ACID; RNA INTERFERENCE; RNA, SMALL INTERFERING; RNA, VIRAL; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED FACTOR 3; UBIQUITINATION; UBIQUITINS;

EID: 80055065839     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002289     Document Type: Article

References (57)

1. Gack MU, Shin YC, Joo CH, Urano T, Liang C, et al. (2007) TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446: 916-920.
2. Gack MU, Kirchhofer A, Shin YC, Inn KS, Liang C, et al. (2008) Roles of RIG-I N-terminal tandem CARD and splice variant in TRIM25-mediated antiviral signal transduction. Proc Natl Acad Sci U S A 105: 16743-16748.
3. Yoneyama M, Fujita T, (2009) RNA recognition and signal transduction by RIG-I-like receptors. Immunol Rev 227: 54-65.
4. Binder M, Kochs G, Bartenschlager R, Lohmann V, (2007) Hepatitis C virus escape from the interferon regulatory factor 3 pathway by a passive and active evasion strategy. Hepatology 46: 1365-1374.
5. Saito T, Owen DM, Jiang F, Marcotrigiano J, Gale M Jr, (2008) Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 454: 523-527.
6. Sumpter R Jr, Loo YM, Foy E, Li K, Yoneyama M, et al. (2005) Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J Virol 79: 2689-2699.
7. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, et al. (2005) Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437: 1167-1172.
8. Arnaud N, Dabo S, Maillard P, Budkowska A, Kalliampakou KI, et al. (2010) Hepatitis C virus controls interferon production through PKR activation. PLoS One 5: e10575.
9. Garaigorta U, Chisari FV, (2009) Hepatitis C virus blocks interferon effector function by inducing protein kinase R phosphorylation. Cell Host Microbe 6: 513-522.
10. Mihm S, Frese M, Meier V, Wietzke-Braun P, Scharf JG, et al. (2004) Interferon type I gene expression in chronic hepatitis C. Lab Invest 84: 1148-1159.
11. Sarasin-Filipowicz M, Oakeley EJ, Duong FH, Christen V, Terracciano L, et al. (2008) Interferon signaling and treatment outcome in chronic hepatitis C. Proc Natl Acad Sci U S A 105: 7034-7039.
12. Bigger CB, Guerra B, Brasky KM, Hubbard G, Beard MR, et al. (2004) Intrahepatic gene expression during chronic hepatitis C virus infection in chimpanzees. J Virol 78: 13779-13792.
13. Takahashi K, Asabe S, Wieland S, Garaigorta U, Gastaminza P, et al. (2010) Plasmacytoid dendritic cells sense hepatitis C virus-infected cells, produce interferon, and inhibit infection. Proc Natl Acad Sci U S A 107: 7431-7436.
14. Askarieh G, Alsio A, Pugnale P, Negro F, Ferrari C, et al. (2010) Systemic and intrahepatic interferon-gamma-inducible protein 10 kDa predicts the first-phase decline in hepatitis C virus RNA and overall viral response to therapy in chronic hepatitis C. Hepatology 51: 1523-1530.
15. Asselah T, Bieche I, Narguet S, Sabbagh A, Laurendeau I, et al. (2008) Liver gene expression signature to predict response to pegylated interferon plus ribavirin combination therapy in patients with chronic hepatitis C. Gut 57: 516-524.
16. Chen L, Borozan I, Feld J, Sun J, Tannis LL, et al. (2005) Hepatic gene expression discriminates responders and nonresponders in treatment of chronic hepatitis C viral infection. Gastroenterology 128: 1437-1444.
17. Chen L, Sun J, Meng L, Heathcote J, Edwards A, et al. (2010) ISG15, a ubiquitin-like interferon stimulated gene, promotes Hepatitis C Virus production in vitro: Implications for chronic infection and response to treatment. J Gen Virol 91: 382-388.
18. Kim MJ, Hwang SY, Imaizumi T, Yoo JY, (2008) Negative feedback regulation of RIG-I-mediated antiviral signaling by interferon-induced ISG15 conjugation. J Virol 82: 1474-1483.
19. Akazawa D, Date T, Morikawa K, Murayama A, Miyamoto M, et al. (2007) CD81 expression is important for the permissiveness of Huh7 cell clones for heterogeneous hepatitis C virus infection. J Virol 81: 5036-5045.
20. Nisole S, Stoye JP, Saib A, (2005) TRIM family proteins: retroviral restriction and antiviral defence. Nat Rev Microbiol 3: 799-808.
21. Zou W, Wang J, Zhang DE, (2007) Negative regulation of ISG15 E3 ligase EFP through its autoISGylation. Biochem Biophys Res Commun 354: 321-327.
22. Jeon YJ, Yoo HM, Chung CH, (2010) ISG15 and immune diseases. Biochim Biophys Acta 1802: 485-496.
23. Kim KI, Yan M, Malakhova O, Luo JK, Shen MF, et al. (2006) Ube1L and protein ISGylation are not essential for alpha/beta interferon signaling. Mol Cell Biol 26: 472-479.
24. Chen WH, Basu S, Bhattacharjee AK, Cross AS, (2010) Enhanced antibody responses to a detoxified lipopolysaccharide-group B meningococcal outer membrane protein vaccine are due to synergistic engagement of Toll-like receptors. Innate Immun 16: 322-332.
25. Broering R, Zhang X, Kottilil S, Trippler M, Jiang M, et al. (2010) The interferon stimulated gene 15 functions as a proviral factor for the hepatitis C virus and as a regulator of the IFN response. Gut 59: 1111-1119.
26. Elco CP, Guenther JM, Williams BRG, Sen GC, (2005) Analysis of genes induced by Sendai virus infection of mutant cell lines reveals essential roles of interferon regulatory factor 3, NF-kappaB, and interferon but not toll-like receptor 3. J Virol 79: 3920-3929.
27. Loo YM, Owen DM, Li K, Erickson AK, Johnson CL, et al. (2006) Viral and therapeutic control of IFN-beta promoter stimulator 1 during hepatitis C virus infection. Proc Natl Acad Sci U S A 103: 6001-6006.
28. Bigger CB, Brasky KM, Lanford RE, (2001) DNA microarray analysis of chimpanzee liver during acute resolving hepatitis C virus infection. J Virol 75: 7059-7066.
29. Farell PJ, Broeze RJ, Lengyel P, (1979) Accumulation of an mRNA and protein in interferon-treated Ehrlich ascites tumour cells. Nature (London) 279: 523-524.
30. Haas AL, Ahrens P, Bright PM, Ankel H, (1987) Interferon induces a 15-kilodalton protein exhibiting marked homology to ubiquitin. J Biol Chem 262: 11315-11323.
31. Zhao C, Denison C, Huibregtse JM, Gygi S, Krug RM, (2005) Human ISG15 conjugation targets both IFN-induced and constitutively expressed proteins functioning in diverse cellular pathways. Proc Natl Acad Sci U S A 102: 10200-10205.
32. Yuan W, Krug RM, (2001) Influenza B virus NS1 protein inhibits conjugation of the interferon (IFN)-induced ubiquitin-like ISG15 protein. Embo J 20: 362-371.
33. Wong JJ, Pung YF, Sze NS, Chin KC, (2006) HERC5 is an IFN-induced HECT-type E3 protein ligase that mediates type I IFN-induced ISGylation of protein targets. Proc Natl Acad Sci U S A 103: 10735-10740.
34. Zou W, Zhang DE, (2006) The interferon-inducible ubiquitin-protein isopeptide ligase (E3) EFP also functions as an ISG15 E3 ligase. J Biol Chem 281: 3989-3994.
35. Durfee LA, Lyon N, Seo K, Huibregtse JM, (2010) The ISG15 conjugation system broadly targets newly synthesized proteins: implications for the antiviral function of ISG15. Mol Cell 38: 722-732.
36. Wieland SF, Chisari FV, (2005) Stealth and cunning: hepatitis B and hepatitis C viruses. J Virol 79: 9369-9380.
37. Jiang J, Tang H, (2010) Mechanism of inhibiting type I interferon induction by hepatitis B virus×protein. Prein Cell 1: 1106-1117.
38. Wei C, Ni C, Song T, Liu Y, Yang X, et al. (2010) The hepatitis B virus×protein disrupts innate immunity by downregulating mitochondrial antiviral signaling protein. J Immunol 185: 1158-1168.
39. Chen GG, Lai PB, Ho RL, Chan PK, Xu H, et al. (2004) Reduction of double-stranded RNA-activated protein kinase in hepatocellular carcinoma associated with hepatitis B virus. J Med Virol 73: 187-194.
40. Shimoike T, McKenna SA, Lindhout DA, Puglisi JD, (2009) Translational insensitivity to potent activation of PKR by HCV IRES RNA. Antiviral Res 83: 228-237.
41. Nallagatla SR, Hwang J, Toroney R, Zheng X, Cameron CE, et al. (2007) 5′-triphosphate-dependent activation of PKR by RNAs with short stem-loops. Science 318: 1455-1458.
42. Gil J, Garcia MA, Gomez-Puertas P, Guerra S, Rullas J, et al. (2004) TRAF family proteins link PKR with NF-kappa B activation. Mol Cell Biol 24: 4502-4512.
43. Oganesyan G, Saha SK, Guo B, He JQ, Shahangian A, et al. (2006) Critical role of TRAF3 in the Toll-like receptor-dependent and-independent antiviral response. Nature 439: 208-211.
44. Zhang P, Samuel CE, (2008) Induction of protein kinase PKR-dependent activation of interferon regulatory factor 3 by vaccinia virus occurs through adapter IPS-1 signaling. J Biol Chem 283: 34580-34587.
45. McAllister CS, Samuel CE, (2009) The RNA-activated protein kinase enhances the induction of interferon-beta and apoptosis mediated by cytoplasmic RNA sensors. J Biol Chem 284: 1644-1651.
46. McAllister CS, Toth AM, Zhang P, Devaux P, Cattaneo R, et al. (2010) Mechanisms of protein kinase PKR-mediated amplification of beta interferon induction by C protein-deficient measles virus. J Virol 84: 380-386.
47. Strahle L, Marq JB, Brini A, Hausmann S, Kolakofsky D, et al. (2007) Activation of the beta interferon promoter by unnatural Sendai virus infection requires RIG-I and is inhibited by viral C proteins. J Virol 81: 12227-12237.
48. Biron-Andreani C, Raulet E, Pichard-Garcia L, Maurel P, (2010) Use of human hepatocytes to investigate blood coagulation factor. Methods Mol Biol 640: 431-445.
49. Strahle L, Garcin D, Kolakofsky D, (2006) Sendai virus defective-interfering genomes and the activation of interferon-beta. Virology 351: 101-111.
50. Jammi NV, Whitby LR, Beal PA, (2003) Small molecule inhibitors of the RNA-dependent protein kinase. Biochem Biophys Res Commun 308: 50-57.
51. Nekhai S, Bottaro DP, Woldehawariat G, Spellerberg A, Petryshyn R, (2000) A cell-permeable peptide inhibits activation of PKR and enhances cell proliferation. Peptides 21: 1449-1456.
52. Grandvaux N, Servant MJ, tenOever B, Sen GC, Balachandran S, et al. (2002) Transcriptional profiling of interferon regulatory factor 3 target genes: direct involvement in the regulation of interferon-stimulated genes. J Virol 76: 5532-5539.
53. Bonnet MC, Daurat C, Ottone C, Meurs EF, (2006) The N-terminus of PKR is responsible for the activation of the NF-kappaB signaling pathway by interacting with the IKK complex. Cell Signal 18: 1865-1875.
54. Malakhov MP, Kim KI, Malakhova OA, Jacobs BS, Borden EC, et al. (2003) High-throughput immunoblotting. Ubiquitiin-like protein ISG15 modifies key regulators of signal transduction. J Biol Chem 278: 16608-16613.
55. Laurent AG, Krust B, Galabru J, Svab J, Hovanessian AG, (1985) Monoclonal antibodies to interferon induced 68,000 Mr protein and their use for the detection of double-stranded RNA dependent protein kinase in human cells. Proc Natl Acad SciUSA 82: 4341-4345.
56. Iwano S, Ichikawa M, Takizawa S, Hashimoto H, Miyamoto Y, (2010) Identification of AhR-regulated genes involved in PAH-induced immunotoxicity using a highly-sensitive DNA chip, 3D-Gene Human Immunity and Metabolic Syndrome 9k. Toxicol In Vitro 24: 85-91.
57. Wolff B, Sanglier JJ, Wang Y, (1997) Leptomycin B is an inhibitor of nuclear export: inhibition of nucleo-cytoplasmic translocation of the human immunodeficiency virus type 1 (HIV-1) Rev protein and Rev-dependent mRNA. Chem Biol 4: 139-147.