Hepatitis C virus impairs TLR3 signaling and inhibits IFN-λ 1 expression in human hepatoma cell line

Innate Immunity

Volumn 20, Issue 1, 2014, Pages 3-11

  Wang, Yizhong ^a,b   Li, Jieliang ^b   Wang, Xu ^b   Ye, Li ^a   Zhou, Yu ^b   Thomas, Rebecca M ^b   Ho, Wenzhe ^a,b  

^a WUHAN UNIVERSITY   (China)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Hepatitis C virus; IFN stimulated genes; interferon ; poly I:C; Toll like receptor 3

Indexed keywords

2',5' OLIGOADENYLATE SYNTHETASE; IFN STIMULATED GENE 56; INTERLEUKIN 29; MYXOVIRUS RESISTANCE PROTEIN; NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 4A; NONSTRUCTURAL PROTEIN 5A; NONSTRUCTURAL PROTEIN 5B; POLYINOSINIC POLYCYTIDYLIC ACID; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CELL LINE; CONTROLLED STUDY; ENZYME ACTIVATION; HEPATITIS C; HEPATITIS C VIRUS; HEPATOMA CELL; HUH7 CELL; HUMAN; HUMAN CELL; INNATE IMMUNITY; JAPANESE FULMINANT HEPATITIS 1; PROTEIN EXPRESSION; VIRUS REPLICATION;

HEPATITIS C VIRUS; IFN-STIMULATED GENES; INTERFERON-Λ; POLY I:C; TOLL-LIKE RECEPTOR 3;

2',5'-OLIGOADENYLATE SYNTHETASE; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; DOWN-REGULATION; HEPACIVIRUS; HEPATITIS C; HUMANS; IMMUNITY, INNATE; INTERLEUKINS; LIVER NEOPLASMS; MYXOVIRUS RESISTANCE PROTEINS; POLY I-C; RNA, DOUBLE-STRANDED; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3; TRANSCRIPTION FACTORS; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84891334795     PISSN: 17534259     EISSN: 17534267     Source Type: Journal    
DOI: 10.1177/1753425913478991     Document Type: Article

References (48)

1. Alter MJ. Prevention of spread of hepatitis C. Hepatology. 2002 ; 36: S93 - S98
2. Chen SL, Morgan TR. The natural history of hepatitis C virus (HCV) infection. Int J Med Sci. 2006 ; 3: 47-52
3. Battaglia AM, Hagmeyer KO. Combination therapy with interferon and ribavirin in the treatment of chronic hepatitis C infection. Ann Pharmacother. 2000 ; 34: 487-494
4. Hu KQ, Vierling JM, Redeker AG. Viral, host and interferon-related factors modulating the effect of interferon therapy for hepatitis C virus infection. J Viral Hepat. 2001 ; 8: 1-18
5. Foy E, Li K, Wang C, Sumpter R, Ikeda M, Lemon SM, et al. Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease. Science. 2003 ; 300: 1145-1148
6. He Y, Katze MG. To interfere and to anti-interfere: the interplay between hepatitis C virus and interferon. Viral Immunol. 2002 ; 15: 95-119
7. Racanelli V, Rehermann B. Hepatitis C virus infection: when silence is deception. Trends Immunol. 2003 ; 24: 456-464
8. Tan SL, Katze MG. How hepatitis C virus counteracts the interferon response: the jury is still out on NS5A. Virology. 2001 ; 284: 1-12
9. Katze MG, He Y, Gale M. Viruses and interferon: a fight for supremacy. Nat Rev Immunol. 2002 ; 2: 675-687
10. Kawai T, Akira S. TLR signaling. Cell Death Differ. 2006 ; 13: 816-825
11. Li K, Foy E, Ferreon JC, Nakamura M, Ferreon AC, Ikeda M, et al. 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. 2005 ; 102: 2992-2997
12. Pagliaccetti NE, Eduardo R, Kleinstein SH, Mu XJ, Bandi P, Robek MD. Interleukin-29 functions cooperatively with interferon to induce antiviral gene expression and inhibit hepatitis C virus replication. J Biol Chem. 2008 ; 283: 30079-30089
13. Marcello T, Grakoui A, Barba-Spaeth G, Machlin ES, Kotenko SV, MacDonald MR, et al. Interferons alpha and lambda inhibit hepatitis C virus replication with distinct signal transduction and gene regulation kinetics. Gastroenterology. 2006 ; 131: 1887-1898
14. Doyle SE, Schreckhise H, Khuu-Duong K, Henderson K, Rosler R, Storey H, et al. Interleukin-29 uses a type 1 interferon-like program to promote antiviral responses in human hepatocytes. Hepatology. 2006 ; 44: 896-906
15. Zhu H, Butera M, Nelson DR, Liu C. Novel type I interferon IL-28A suppresses hepatitis C viral RNA replication. Virol J. 2005 ; 2: 80-80
16. Robek MD, Boyd BS, Chisari FV. Lambda interferon inhibits hepatitis B and C virus replication. J Virol. 2005 ; 79: 3851-3854
17. Muir AJ, Shiffman ML, Zaman A, Yoffe B, de la Torre A, Flamm S, et al. Phase 1b study of pegylated interferon lambda 1 with or without ribavirin in patients with chronic genotype 1 hepatitis C virus infection. Hepatology. 2010 ; 52: 822-832
18. Zhong J, Gastaminza P, Cheng G, Kapadia S, Kato T, Burton DR, et al. Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci U S A. 2005 ; 102: 9294-9299
19. Ye L, Wang X, Wang S, Wang Y, Song L, Hou W, et al. CD56+ T cells inhibit hepatitis C virus replication in human hepatocytes. Hepatology. 2009 ; 49: 753-762
20. Vijay-Kumar M, Gentsch JR, Kaiser WJ, Borregaard N, Offermann MK, Neish AS, et al. Protein kinase R mediates intestinal epithelial gene remodeling in response to double-stranded RNA and live rotavirus. J Immunol. 2005 ; 174: 6322-6331
21. Yang JH, Lai JP, Douglas SD, Metzger D, Zhu XH, Ho WZ. Real-time RT-PCR for quantitation of hepatitis C virus RNA. J Virol Methods. 2002 ; 102: 119-128
22. Zhang T, Lin RT, Li Y, Douglas SD, Maxcey C, Ho C, et al. Hepatitis C virus inhibits intracellular interferon alpha expression in human hepatic cell lines. Hepatology. 2005 ; 42: 819-827
23. Li K, Chen Z, Kato N, Gale M, Lemon SM. Distinct poly(I-C) and virus-activated signaling pathways leading to interferon-beta production in hepatocytes. J Biol Chem. 2005 ; 280: 16739-16747
24. Bartenschlager R, Pietschmann T. Efficient hepatitis C virus cell culture system: what a difference the host cell makes. Proc Natl Acad Sci U S A. 2005 ; 102: 9739-9740
25. Bluyssen AR, Durbin JE, Levy DE. ISGF3 gamma p48, a specificity switch for interferon activated transcription factors. Cytokine Growth Factor Rev. 1996 ; 7: 11-17
26. Justesen J, Hartmann R, Kjeldgaard NO. Gene structure and function of the 2′-5′-oligoadenylate synthetase family. Cell Mol Life Sci. 2000 ; 57: 1593-1612
27. Sen GC, Sarkar SN. The interferon-stimulated genes: targets of direct signaling by interferons, double-stranded RNA, and viruses. Curr Top Microbiol Immunol. 2007 ; 316: 233-250
28. Garcia MA, Meurs EF, Esteban M. The dsRNA protein kinase PKR: virus and cell control. Biochimie. 2007 ; 89: 799-811
29. Carroll TD, Matzinger SR, Genesca M, Fritts L, Colon R, McChesney MB, et al. Interferon-induced expression of MxA in the respiratory tract of rhesus macaques is suppressed by influenza virus replication. J Immunol. 2008 ; 180: 2385-2395
30. Castet V, Fournier C, Soulier A, Brillet R, Coste J, Larrey D, et al. Alpha interferon inhibits hepatitis C virus replication in primary human hepatocytes infected in vitro. J Virol. 2002 ; 76: 8189-8199
31. Dash S, Prabhu R, Hazari S, Bastian F, Garry R, Zou W, et al. Interferons alpha, beta, gamma each inhibit hepatitis C virus replication at the level of internal ribosome entry site-mediated translation. Liver Int. 2005 ; 25: 580-594
32. Ank N, Paludan SR. Type III IFNs: new layers of complexity in innate antiviral immunity. Biofactors. 2009 ; 35: 82-87
33. West J, Damania B. Upregulation of the TLR3 pathway by Kaposi's sarcoma-associated herpesvirus during primary infection. J Virol. 2008 ; 82: 5440-5449
34. Starace D, Galli R, Paone A, De Cesaris P, Filippini A, Ziparo E, et al. Toll-like receptor 3 activation induces antiviral immune responses in mouse sertoli cells. Biol Reprod. 2008 ; 79: 766-775
35. Kumar A, Zhang J, Yu FS. Toll-like receptor 3 agonist poly(I:C)-induced antiviral response in human corneal epithelial cells. Immunology. 2006 ; 117: 11-21
36. Marukian S, Andrus L, Sheahan TP, Jones CT, Charles ED, Ploss A, et al. Hepatitis C virus induces interferon-lambda and interferon-stimulated genes in primary liver cultures. Hepatology. 2011 ; 54: 1913-1923
37. Jiang M, Osterlund P, Sarin LP, Poranen MM, Bamford DH, Guo D, et al. Innate immune responses in human monocyte-derived dendritic cells are highly dependent on the size and the 5′ phosphorylation of RNA molecules. J Immunol. 2011 ; 187: 1713-1721
38. Kato H, Takeuchi O, Mikamo-Satoh E, Hirai R, Kawai T, Matsushita K, et al. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J Exp Med. 2008 ; 205: 1601-1610
39. Zhou Y, Guo M, Wang X, Li J, Wang Y, Ye L, et al. TLR3 activation efficiency by high or low molecular mass poly I:C. Innate Immun. Epub ahead of print 3 October 2012.
40. Gale M, Foy EM. Evasion of intracellular host defence by hepatitis C virus. Nature. 2005 ; 436: 939-945
41. Foy E, Li K, Sumpter R, Loo YM, Johnson CL, Wang C, et al. Control of antiviral defenses through hepatitis C virus disruption of retinoic acid-inducible gene-I signaling. Proc Natl Acad Sci USA. 2005 ; 102: 2986-2991
42. Li XD, Sun L, Seth RB, Pineda G, Chen ZJ. 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. 2005 ; 102: 17717-17722
43. Raychoudhuri A, Shrivastava S, Steele R, Dash S, Kanda T, Ray R, et al. Hepatitis C virus infection impairs IRF-7 translocation and Alpha interferon synthesis in immortalized human hepatocytes. J Virol. 2010 ; 84: 10991-10998
44. Taylor DR, Shi ST, Romano PR, Barber GN, Lai MM. Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein. Science. 1999 ; 285: 107-110
45. Gale M, Blakely CM, Kwieciszewski B, Tan SL, Dossett M, Tang NM, et al. Control of PKR protein kinase by hepatitis C virus nonstructural 5A protein: molecular mechanisms of kinase regulation. Mol Cell Biol. 1998 ; 18: 5208-5218
46. Melen K, Fagerlund R, Nyqvist M, Keskinen P, Julkunen I. Expression of hepatitis C virus core protein inhibits interferon-induced nuclear import of STATs. J Med Virol. 2004 ; 73: 536-547
47. Behrens SE, Tomei L, De Francesco R. Identification and properties of the RNA-dependent RNA polymerase of hepatitis C virus. EMBO J. 1996 ; 15: 12-22
48. Reed KE, Rice CM. Overview of hepatitis C virus genome structure, polyprotein processing, and protein properties. Curr Top Microbiol Immunol. 2000 ; 242: 55-84