Activation of endogenous type I IFN signaling contributes to persistent HCV infection

Reviews in Medical Virology

Volumn 24, Issue 5, 2014, Pages 332-342

  Li, Yujia ^a   Li, Shilin ^a   Duan, Xiaoqiong ^a   Liu, Bing ^a   Yang, Chunhui ^a   Zeng, Peibin ^a   Mcgilvray, Ian ^a,b   Chen, Limin ^a,b  

^a INSTITUTE OF BLOOD TRANSFUSION   (China)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DEUBIQUITINASE; INTERFERON; UBIQUITIN; UBIQUITIN SPECIFIC PROTEASE 18; UNCLASSIFIED DRUG;

ANTIVIRAL ACTIVITY; ANTIVIRAL RESISTANCE; ANTIVIRAL THERAPY; ARTICLE; GENE EXPRESSION; HEALTH CARE QUALITY; HEPATITIS C; HUMAN; INFECTION CONTROL; INNATE IMMUNITY; INTERFERON PRODUCTION; LIVER; PERSISTENT INFECTION; SIGNAL TRANSDUCTION; TREATMENT RESPONSE; UPREGULATION; ANIMAL; GENETICS; HEPACIVIRUS; HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGY; VIROLOGY;

ANIMALS; HEPACIVIRUS; HEPATITIS C; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERFERON TYPE I; SIGNAL TRANSDUCTION;

EID: 84910640644     PISSN: 10529276     EISSN: 10991654     Source Type: Journal    
DOI: 10.1002/rmv.1795     Document Type: Article

References (85)

1. Sorrell MF, Belongia EA, Costa J, et al. National Institutes of Health consensus development conference statement: management of hepatitis B. Hepatology 2009; 49: S4-S12. DOI: 10.1002/hep.22946
2. Poynard T, Yuen MF, Ratziu V, et al. Viral hepatitis C. Lancet 2003; 362: 2095-2100. DOI: 10.1016/S0140-6736(03)15109-4
3. Shepard CW, Finelli L, Alter MJ. Global epidemiology of hepatitis C virus infection. The Lancet Infectious Diseases 2005; 5: 558-567. DOI: 10.1016/S1473-3099(05)70216-4
4. Fried MW. Side effects of therapy of hepatitis C and their management. Hepatology 2002; 36: S237-S244. DOI: 10.1002/hep.1840360730
5. Pawlotsky JM. Treatment failure and resistance with direct-acting antiviral drugs against hepatitis C virus. Hepatology 2011; 53: 1742-1751. DOI: 10.1002/hep.24262
6. Thompson AJ, McHutchison JG. Will IL28B polymorphism remain relevant in the era of direct-acting antiviral agents for hepatitis C virus? Hepatology 2012; 56: 373-381. DOI: 10.1002/hep.25792
7. Selzner N, Chen L, Borozan I, et al. Hepatic gene expression and prediction of therapy response in chronic hepatitis C patients. Journal of Hepatology 2008; 48: 708-713. DOI: 10.1016/j.jhep.2008.02.010
8. Kaisho T, Akira S. Toll-like receptor function and signaling. Journal of Allergy and Clinical Immunology 2006; 117: 979-987. DOI: 10.1016/j.jaci.2006.02.023
9. Kato H, Takeuchi O, Sato S, et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006; 441: 101-105. DOI: 10.1038/nature04734
10. de Veer MJ, Holko M, Frevel M, et al. Functional classification of interferon-stimulated genes identified using microarrays. Journal of Leukocyte Biology 2001; 69: 912. DOI: 10.1189/jlb.1938-3673
11. Sadler AJ, Williams BR. Interferon-inducible antiviral effectors. Nature Reviews Immunology 2008; 8: 559-568. DOI: 10.1038/nri2314
12. Sen G, Sarkar S. The interferon-stimulated genes: targets of direct signaling by interferons, double-stranded RNA, and viruses. In Interferon: The 50th Anniversary, Pitha PM (ed). Springer: Berlin Heidelberg, 2007; 233-250.
13. Chen L, Sun J, Meng L, et al. ISG15, a ubiquitin-like interferon-stimulated gene, promotes hepatitis C virus production in vitro: implications for chronic infection and response to treatment. Journal of General Virology 2009; 91: 382-388. DOI: 10.1099/vir.0.015388-0
14. Broering R, Zhang X, Kottilil S, et al. The interferon stimulated gene 15 functions as a proviral factor for the hepatitis C virus and as a regulator of the IFN response. Gut 2010; 59: 1111-1119. DOI: 10.1136/gut.2009.195545
15. Zhu Y, Qin B, Xiao C, et al. Cell-type specific interferon stimulated gene staining in liver underlies response to interferon therapy in chronic HBV infected patients. Digestive Diseases and Sciences 2012; 57: 2355-2361. DOI: 10.1007/s10620-012-2169-5
16. Xiao C, Qin B, Chen L, et al. Preactivation of the interferon signalling in liver is correlated with nonresponse to interferon alpha therapy in patients chronically infected with hepatitis B virus. Journal of Viral Hepatitis 2012; 19: e1-e10. DOI: 10.1111/j.1365-2893.2011.01471.x
17. Bertoletti A, Gehring AJ. The immune response during hepatitis B virus infection. Journal of General Virology 2006; 87: 1439-1449. DOI: 10.1099/vir.0.81920-0
18. Rehermann B, Nascimbeni M. Immunology of hepatitis B virus and hepatitis C virus infection. Nature Reviews Immunology 2005; 5: 215-229. DOI: 10.1038/nri1573
19. Wilson EB, Yamada DH, Elsaesser H, et al. Blockade of chronic type I interferon signaling to control persistent LCMV infection. Science 2013; 340: 202-207. DOI: 10.1126/science.1235208
20. Teijaro JR, Ng C, Lee AM, et al. Persistent LCMV infection is controlled by blockade of type I interferon signaling. Science 2013; 340: 207-211. DOI: 10.1126/science.1235214
21. Platanias LC. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nature Reviews Immunology 2005; 5: 375-386. DOI: 10.1038/nri1604
22. Stark GR, Kerr IM, Williams BRG, et al. How cells respond to interferons. Annual Review of Biochemistry 1998; 67: 227-264. DOI: 10.1146/annurev.biochem.67.1.227
23. Kotenko SV. IFN-λs. Current Opinion in Immunology 2011; 23: 583-590. DOI: 10.1016/j.coi.2011.07.007
24. Donnelly RP, Kotenko SV. Interferon-lambda: a new addition to an old family. Journal of Interferon & Cytokine Research 2010; 30: 555-564. DOI: 10.1089/jir.2010.0078
25. Broering R, Lutterbeck M, Trippler M, et al. Long-term stimulation of Toll-like receptor 3 in primary human hepatocytes leads to sensitization for antiviral responses induced by poly I: C treatment. Journal of Viral Hepatitis 2013. DOI: 10.1111/jvh.12174
26. Coccia EM, Severa M, Giacomini E, et al. Viral infection and Toll-like receptor agonists induce a differential expression of type I and λ interferons in human plasmacytoid and monocyte-derived dendritic cells. European Journal of Immunology 2004; 34: 796-805. DOI: 10.1002/eji.200324610
27. Thomas E, Gonzalez VD, Li Q, et al. HCV infection induces a unique hepatic innate immune response associated with robust production of type III interferons. Gastroenterology 2012; 142: 978-988. DOI: 10.1053/j.gastro.2011.12.055
28. Liu S-Y, Sanchez DJ, Cheng G. New developments in the induction and antiviral effectors of type I interferon. Current Opinion in Immunology 2011; 23: 57-64. DOI: 10.1016/j.coi.2010.11.003
29. Brass AL, Huang I, Benita Y, et al. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 2009; 139: 1243-1254. DOI: 10.1016/j.cell.2009.12.017
30. Chin K-C, Cresswell P. Viperin (cig5), an IFN-inducible antiviral protein directly induced by human cytomegalovirus. Proceedings of the National Academy of Sciences 2001; 98: 15125-15130. DOI: 10.1073/pnas.011593298
31. Wang X, Hinson ER, Cresswell P. The interferon-inducible protein viperin inhibits influenza virus release by perturbing lipid rafts. Cell Host & Microbe 2007; 2: 96-105. DOI: 10.1016/j.chom.2007.06.009
32. Szretter KJ, Brien JD, Thackray LB, et al. The interferon-inducible gene viperin restricts West Nile virus pathogenesis. Journal of Virology 2011; 85: 11557-11566. DOI: 10.1128/JVI.05519-11
33. Chan YL, Chang TH, Liao CL, et al. The cellular antiviral protein viperin is attenuated by proteasome-mediated protein degradation in Japanese encephalitis virus-infected cells. Journal of Virology 2008; 82: 10455-10464. DOI: 10.1128/JVI.00438-08
34. Nasr N, Maddocks S, Turville SG, et al. HIV-1 infection of human macrophages directly induces viperin which inhibits viral production. Blood 2012; 120: 778-788. DOI: 10.1182/blood-2012-01-407395
35. Yurkovetsky ZR, Kirkwood JM, Edington HD, et al. Multiplex analysis of serum cytokines in melanoma patients treated with interferon-α2b. Clinical Cancer Research 2007; 13: 2422-2428. DOI: 10.1158/1078-0432.CCR-06-1805
36. Zimmerer JM, Lesinski GB, Ruppert AS, et al. Gene expression profiling reveals similarities between the in vitro and in vivo responses of immune effector cells to IFN-α. Clinical Cancer Research 2008; 14: 5900-5906. DOI: 10.1158/1078-0432.CCR-08-0846
37. Li Y, Li C, Xue P, et al. ISG56 is a negative-feedback regulator of virus-triggered signaling and cellular antiviral response. Proceedings of the National Academy of Sciences 2009; 106: 7945-7950. DOI: 10.1073/pnas.0900818106
38. Chen L, Borozan I, Feld J, et al. Hepatic gene expression discriminates responders and nonresponders in treatment of chronic hepatitis C viral infection. Gastroenterology 2005; 128: 1437. DOI: 10.1053/j.gastro.2005.01.059
39. Chen L, Borozan I, Sun J, et al. Cell-type specific gene expression signature in liver underlies response to interferon therapy in chronic hepatitis C infection. Gastroenterology 2010; 138: 1123-1133. DOI: 10.1053/j.gastro.2009.10.046
40. McGilvray I, Feld JJ, Chen L, et al. Hepatic cell-type specific gene expression better predicts HCV treatment outcome than IL28B genotype. Gastroenterology 2012; 142: 1122-1131. e1121. DOI: 10.1053/j.gastro.2012.01.028
41. Dill MT, Duong FH, Vogt JE, et al. Interferon-induced gene expression is a stronger predictor of treatment response than IL28B genotype in patients with hepatitis C. Gastroenterology 2011; 140: 1021-1031. e1010. DOI: 10.1053/j.gastro.2010.11.039
42. Ge D, Fellay J, Thompson AJ, et al. Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature 2009; 461: 399-401. DOI: 10.1038/nature08309
43. Thomas DL, Thio CL, Martin MP, et al. Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature 2009; 461: 798-801. DOI: 10.1038/nature08463
44. Tanaka Y, Nishida N, Sugiyama M, et al. Genome-wide association of IL28B with response to pegylated interferon-α and ribavirin therapy for chronic hepatitis C. Nature Genetics 2009; 41: 1105-1109. DOI: 10.1038/ng.449
45. Yuan W, Krug RM. Influenza B virus NS1 protein inhibits conjugation of the interferon (IFN)-induced ubiquitin-like ISG15 protein. The EMBO Journal 2001; 20: 362-371. DOI: 10.1093/emboj/20.3.362
46. Zhao C, Beaudenon SL, Kelley ML, et al. The UbcH8 ubiquitin E2 enzyme is also the E2 enzyme for ISG15, an IFN-α/β-induced ubiquitin-like protein. Proceedings of the National Academy of Sciences of the United States of America 2004; 101: 7578-7582. DOI: 10.1073/pnas.0402528101
47. Kim KI, Giannakopoulos NV, Virgin HW, et al. Interferon-inducible ubiquitin E2, Ubc8, is a conjugating enzyme for protein ISGylation. Molecular and Cellular Biology 2004; 24: 9592-9600. DOI: 10.1128/MCB.24.21.9592-9600.2004
48. Zou W, Zhang D-E. The interferon-inducible ubiquitin-protein isopeptide ligase (E3) EFP also functions as an ISG15 E3 ligase. Journal of Biological Chemistry 2006; 281: 3989-3994. DOI: 10.1074/jbc. M510787200
49. Wong JJY, Pung YF, Sze NS-K, et al. HERC5 is an IFN-induced HECT-type E3 protein ligase that mediates type I IFN-induced ISGylation of protein targets. Proceedings of the National Academy of Sciences 2006; 103: 10735-10740. DOI: 10.1073/pnas.0600397103
50. Yeh ET, Gong L, Kamitani T. Ubiquitin-like proteins: new wines in new bottles. Gene 2000; 248: 1-14. DOI: 10.1016/S0378-1119(00)00139-6
51. Malakhov MP, Malakhova OA, Kim KI, et al. UBP43 (USP18) specifically removes ISG15 from conjugated proteins. Journal of Biological Chemistry 2002; 277: 9976-9981. DOI: 10.1074/jbc. M109078200
52. Okumura A, Pitha PM, Harty RN. ISG15 inhibits Ebola VP40 VLP budding in an l-domain-dependent manner by blocking Nedd4 ligase activity. Proceedings of the National Academy of Sciences 2008; 105: 3974-3979. DOI: 10.1073/pnas.0710629105
53. Lenschow DJ, Giannakopoulos NV, Gunn LJ, et al. Identification of interferon-stimulated gene 15 as an antiviral molecule during Sindbis virus infection in vivo. Journal of Virology 2005; 79: 13974-13983. DOI: 10.1128/JVI.79.22.13974-13983.2005
54. Lenschow DJ, Lai C, Frias-Staheli N, et al. IFN-stimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses. Proceedings of the National Academy of Sciences 2007; 104: 1371-1376. DOI: 10.1073/pnas.0607038104
55. Guerra S, Cáceres A, Knobeloch K-P, et al. Vaccinia virus E3 protein prevents the antiviral action of ISG15. PLoS Pathogens 2008; 4: e1000096. DOI: 10.1371/journal.ppat.1000096
56. Kim M-J, Hwang S-Y, Imaizumi T, et al. Negative feedback regulation of RIG-I-mediated antiviral signaling by interferon-induced ISG15 conjugation. Journal of Virology 2008; 82: 1474-1483. DOI: 10.1128/JVI.01650-07
57. Durfee LA, Huibregtse JM. Identification and validation of ISG15 target proteins. In Conjugation and Deconjugation of Ubiquitin Family Modifiers, Groettrup M (ed). Springer: New York, 2010; 228-237.
58. Malakhova OA, Yan M, Malakhov MP, et al. Protein ISGylation modulates the JAK-STAT signaling pathway. Genes and Development 2003; 17: 455-460. DOI: 10.1101/gad.1056303
59. Kim KI, Yan M, Malakhova O, et al. Ube1L and protein ISGylation are not essential for alpha/beta interferon signaling. Molecular and Cellular Biology 2006; 26: 472-479. DOI: 10.1128/MCB.26.2.472-479.2006
60. Ritchie KJ, Hahn CS, Kim KI, et al. Role of ISG15 protease UBP43 (USP18) in innate immunity to viral infection. Nature Medicine 2004; 10: 1374-1378. DOI: 10.1038/nm1133
61. Randall G, Chen L, Panis M, et al. Silencing of USP18 potentiates the antiviral activity of interferon against hepatitis C virus infection. Gastroenterology 2006; 131: 1584-1591. 2006.08.043 DOI: 10.1053/j.gastro.2006.08.043
62. François-Newton V, de Freitas Almeida GM, Payelle-Brogard B, et al. USP18-Based negative feedback control is induced by type I and type III interferons and specifically inactivates interferon α response. PLoS One 2011; 6: e22200. DOI: 10.1371/journal.pone.0022200
63. Potu H, Sgorbissa A, Brancolini C. Identification of USP18 as an important regulator of the susceptibility to IFN-α and drug-induced apoptosis. Cancer Research 2010; 70: 655-665. DOI: 10.1158/0008-5472.CAN-09-1942
64. Okumura A, Lu G, Pitha-Rowe I, et al. Innate antiviral response targets HIV-1 release by the induction of ubiquitin-like protein ISG15. Proceedings of the National Academy of Sciences of the United States of America 2006; 103: 1440-1445. DOI: 10.1073/pnas.0510518103
65. Hsiao N-W, Chen J-W, Yang T-C, et al. ISG15 over-expression inhibits replication of the Japanese encephalitis virus in human medulloblastoma cells. Antiviral Research 2010; 85: 504-511. DOI: 10.1016/j.antiviral.2009.12.007
66. Harty RN, Pitha PM, Okumura A. Antiviral activity of innate immune protein ISG15. Journal of Innate Immunity 2009; 1: 397-404. DOI: 10.1159/000226245
67. Chen L, Sun J, Meng L, et al. ISG15, a ubiquitin-like interferon-stimulated gene, promotes hepatitis C virus production in vitro: implications for chronic infection and response to treatment. Journal of General Virology 2010; 91: 382-388. DOI: 10.1099/vir.0.015388-0
68. Ritchie KJ, Malakhov MP, Hetherington CJ, et al. Dysregulation of protein modification by ISG15 results in brain cell injury. Genes and Development 2002; 16: 2207-2212. DOI: 10.1101/gad.1010202
69. Sumpter R, Loo Y-M, Foy E, et al. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. Journal of Virology 2005; 79: 2689-2699. DOI: 10.1128/JVI.79.5.2689-2699.2005
70. Jeon YJ, Choi JS, Lee JY, et al. Filamin B serves as a molecular scaffold for type I interferon-induced c-Jun NH2-terminal kinase signaling pathway. Molecular Biology of the Cell 2008; 19: 5116-5130. DOI: 10.1091/mbc. E08-06-0576
71. Jeon YJ, Choi JS, Lee JY, et al. ISG15 modification of filamin B negatively regulates the type I interferon-induced JNK signalling pathway. EMBO Reports 2009; 10: 374-380. DOI: 10.1038/embor.2009.23
72. Real CI, Megger DA, Sitek B, et al. Identification of proteins that mediate the pro-viral functions of the interferon stimulated gene 15 in hepatitis C virus replication. Antiviral Research 2013; 100: 654-661. DOI: 10.1016/j.antiviral.2013.10.009
73. Kim M-J, Yoo J-Y. Inhibition of hepatitis C virus replication by IFN-mediated ISGylation of HCV-NS5A. The Journal of Immunology 2010; 185: 4311-4318. DOI: 10.4049/jimmunol.1000098
74. Sarasin-Filipowicz M, Wang X, Yan M, et al. Alpha interferon induces long-lasting refractoriness of JAK-STAT signaling in the mouse liver through induction of USP18/UBP43. Science Signaling 2009; 29: 4841. DOI: 10.1128/MCB.00224-09
75. Kim J-H, Luo J-K, Zhang D-E. The level of hepatitis B virus replication is not affected by protein ISG15 modification but is reduced by inhibition of UBP43 (USP18) expression. The Journal of Immunology 2008; 181: 6467-6472.
76. Abel K, Alegria-Hartman MJ, Rothaeusler K, et al. The relationship between simian immunodeficiency virus RNA levels and the mRNA levels of alpha/beta interferons (IFN-α/β) and IFN-α/β-inducible Mx in lymphoid tissues of rhesus macaques during acute and chronic infection. Journal of Virology 2002; 76: 8433-8445. DOI: 10.1128/JVI.76.16.8433-8445.2002
77. Chang JJ, Altfeld M. Innate immune activation in primary HIV-1 infection. Journal of Infectious Diseases 2010; 202: S297-S301. DOI: 10.1086/655657
78. Appay V, Sauce D. Immune activation and inflammation in HIV-1 infection: causes and consequences. The Journal of Pathology 2008; 214: 231-241. DOI: 10.1002/path.2276
79. Brooks DG, Trifilo MJ, Edelmann KH, et al. Interleukin-10 determines viral clearance or persistence in vivo. Nature Medicine 2006; 12: 1301-1309. DOI: 10.1038/nm1492
80. Blackburn SD, Wherry EJ. IL-10, T cell exhaustion and viral persistence. Trends in Microbiology 2007; 15: 143-146. DOI: 10.1016/j.tim.2007.02.006
81. Brooks DG, Ha S-J, Elsaesser H, et al. IL-10 and PD-L1 operate through distinct pathways to suppress T-cell activity during persistent viral infection. Proceedings of the National Academy of Sciences 2008; 105: 20428-20433. DOI: 10.1073/pnas.0811139106
82. Shetty RD, Velu V, Titanji K, et al. PD-1 blockade during chronic SIV infection reduces hyperimmune activation and microbial translocation in rhesus macaques. The Journal of Clinical Investigation 2012; 122: 1712. DOI: 10.1172/JCI60612
83. Ejrnaes M, Filippi CM, Martinic MM, et al. Resolution of a chronic viral infection after interleukin-10 receptor blockade. The Journal of Experimental Medicine 2006; 203: 2461-2472. DOI: 10.1084/jem.20061462
84. Barber DL, Wherry EJ, Masopust D, et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 2005; 439: 682-687. DOI: 10.1038/nature04444
85. Sarrazin C, Zeuzem S. Resistance to direct antiviral agents in patients with hepatitis C virus infection. Gastroenterology 2010; 138: 447-462. DOI: 10.1053/j.gastro.2009.11.055