Induction of interferon-λ contributes to Toll-like receptor-3-activated hepatic stellate cell-mediated hepatitis C virus inhibition in hepatocytes

Journal of Viral Hepatitis

Volumn 20, Issue 6, 2013, Pages 385-394

  Wang, Y ^a,b   Li, J ^b   Wang, X ^b   Ye, L ^a   Zhou, Y ^b   Ho, W ^a,b  

^a WUHAN UNIVERSITY   (China)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

hepatic stellate cells; hepatitis C virus; interferon ; interferon stimulated genes; Toll like receptor 3

Indexed keywords

INTERFERON; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 28A; INTERLEUKIN 29; LAMBDA INTERFERON; MESSENGER RNA; MYXOVIRUS RESISTANCE PROTEIN A; POLYINOSINIC POLYCYTIDYLIC ACID; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG;

ANTIVIRAL ACTIVITY; ARTICLE; COCULTURE; CONTROLLED STUDY; GENE EXPRESSION; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; INNATE IMMUNITY; INTERFERON INDUCTION; LIVER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STELLATE CELL; SUPERNATANT; VIRUS INHIBITION; VIRUS REPLICATION;

CELL LINE, TUMOR; COCULTURE TECHNIQUES; CULTURE MEDIA, CONDITIONED; HEPACIVIRUS; HEPATIC STELLATE CELLS; HEPATOCYTES; HUMANS; INTERFERON REGULATORY FACTOR-7; INTERFERON-GAMMA; LIVER; MYXOVIRUS RESISTANCE PROTEINS; POLY I-C; RNA, MESSENGER; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3; VIRUS REPLICATION;

EID: 84877583444     PISSN: 13520504     EISSN: 13652893     Source Type: Journal    
DOI: 10.1111/jvh.12040     Document Type: Article

References (50)

1. Geerts A,. History, heterogeneity, developmental biology, and functions of quiescent hepatic stellate cells. Semin Liver Dis 2001; 21 (3): 311-335.
2. Senoo H,. Structure and function of hepatic stellate cells. Med Electron Microsc 2004; 37 (1): 3-15.
3. Reynaert H, Thompson MG, Thomas T, Geerts A,. Hepatic stellate cells: role in microcirculation and pathophysiology of portal hypertension. Gut 2002; 50 (4): 571-581.
4. Friedman SL,. Mechanisms of hepatic fibrogenesis. Gastroenterology 2008; 134 (6): 1655-1669.
5. Winau F, Hegasy G, Weiskirchen R, et al,. Ito cells are liver-resident antigen-presenting cells for activating T cell responses. Immunity 2007; 26 (1): 117-129.
6. Ichikawa S, Mucida D, Tyznik AJ, Kronenberg M, Cheroutre H,. Hepatic stellate cells function as regulatory bystanders. J Immunol 2011; 186 (10): 5549-5555.
7. Seki E, De Minicis S, Osterreicher CH, et al,. TLR4 enhances TGF-beta signaling and hepatic fibrosis. Nat Med 2007; 13 (11): 1324-1332.
8. Watanabe A, Hashmi A, Gomes DA, et al,. Apoptotic hepatocyte DNA inhibits hepatic stellate cell chemotaxis via toll-like receptor 9. Hepatology 2007; 46 (5): 1509-1518.
9. Kawai T, Akira S,. Innate immune recognition of viral infection. Nat Immunol 2006; 7 (2): 131-137.
10. 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 (1): 11-21.
11. Starace D, Galli R, Paone A, et al,. Toll-like receptor 3 activation induces antiviral immune responses in mouse sertoli cells. Biol Reprod 2008; 79 (4): 766-775.
12. West J, Damania B,. Upregulation of the TLR3 pathway by Kaposi's sarcoma-associated herpesvirus during primary infection. J Virol 2008; 82 (11): 5440-5449.
13. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA,. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001; 413 (6857): 732-738.
14. Wang N, Liang Y, Devaraj S, Wang J, Lemon SM, Li K,. Toll-like receptor 3 mediates establishment of an antiviral state against hepatitis C virus in hepatoma cells. J Virol 2009; 83 (19): 9824-9834.
15. Janeway Jr CA, Medzhitov R,. Innate immune recognition. Annu Rev Immunol 2002; 20: 197-216.
16. Li J, Ye L, Wang X, Hu S, Ho W,. Induction of interferon-lambda contributes to toll-like receptor 3-mediated herpes simplex virus type 1 inhibition in astrocytes. J Neurosci Res 2011; 90 (2): 399-406.
17. Ank N, Iversen MB, Bartholdy C, et al,. An important role for type III interferon (IFN-lambda/IL-28) in TLR-induced antiviral activity. J Immunol 2008; 180 (4): 2474-2485.
18. Zhou L, Wang X, Wang YJ, et al,. Activation of toll-like receptor-3 induces interferon-lambda expression in human neuronal cells. Neuroscience 2009; 159 (2): 629-637.
19. Zhou Y, Ye L, Wan Q, et al,. Activation of Toll-like receptors inhibits herpes simplex virus-1 infection of human neuronal cells. J Neurosci Res 2009; 87 (13): 2916-2925.
20. Zhou Y, Wang X, Liu M, et al,. A critical function of toll-like receptor-3 in the induction of anti-human immunodeficiency virus activities in macrophages. Immunology 2010; 131 (1): 40-49.
21. Li K, Foy E, Ferreon JC, 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 USA 2005; 102 (8): 2992-2997.
22. Xu L, Hui AY, Albanis E, et al,. Human hepatic stellate cell lines, LX-1 and LX-2: new tools for analysis of hepatic fibrosis. Gut 2005; 54 (1): 142-151.
23. Vijay-Kumar M, Gentsch JR, Kaiser WJ, et al,. Protein kinase R mediates intestinal epithelial gene remodeling in response to double-stranded RNA and live rotavirus. J Immunol 2005; 174 (10): 6322-6331.
24. Zhong J, Gastaminza P, Cheng G, et al,. Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci USA 2005; 102 (26): 9294-9299.
25. Ye L, Wang X, Wang S, et al,. CD56 + T cells inhibit hepatitis C virus replication in human hepatocytes. Hepatology 2009; 49 (3): 753-762.
26. 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 (1-2): 119-128.
27. Zhang T, Lin RT, Li Y, et al,. Hepatitis C virus inhibits intracellular interferon alpha expression in human hepatic cell lines. Hepatology 2005; 42 (4): 819-827.
28. Katze MG, He Y, Gale Jr M,. Viruses and interferon: a fight for supremacy. Nat Rev Immunol 2002; 2 (9): 675-687.
29. Radaeva S, Wang L, Radaev S, Jeong WI, Park O, Gao B,. Retinoic acid signaling sensitizes hepatic stellate cells to NK cell killing via upregulation of NK cell activating ligand RAE1. Am J Physiol Gastrointest Liver Physiol 2007; 293 (4): G809-G816.
30. Wang B, Trippler M, Pei R, et al,. Toll-like receptor activated human and murine hepatic stellate cells are potent regulators of hepatitis C virus replication. J Hepatol 2009; 51 (6): 1037-1045.
31. 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 (7089): 101-105.
32. Ank N, West H, Bartholdy C, Eriksson K, Thomsen AR, Paludan SR,. Lambda interferon (IFN-lambda), a type III IFN, is induced by viruses and IFNs and displays potent antiviral activity against select virus infections in vivo. J Virol 2006; 80 (9): 4501-4509.
33. Doyle SE, Schreckhise H, Khuu-Duong K, et al,. Interleukin-29 uses a type 1 interferon-like program to promote antiviral responses in human hepatocytes. Hepatology 2006; 44 (4): 896-906.
34. Hou W, Wang X, Ye L, et al,. Lambda interferon inhibits human immunodeficiency virus type 1 infection of macrophages. J Virol 2009; 83 (8): 3834-3842.
35. Kotenko SV, Gallagher G, Baurin VV, et al,. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol 2003; 4 (1): 69-77.
36. Marcello T, Grakoui A, Barba-Spaeth G, et al,. Interferons alpha and lambda inhibit hepatitis C virus replication with distinct signal transduction and gene regulation kinetics. Gastroenterology 2006; 131 (6): 1887-1898.
37. Robek MD, Boyd BS, Chisari FV,. Lambda interferon inhibits hepatitis B and C virus replication. J Virol 2005; 79 (6): 3851-3854.
38. Zhang L, Jilg N, Shao RX, et al,. IL28B inhibits hepatitis C virus replication through the JAK-STAT pathway. J Hepatol 2011; 55 (2): 289-298.
39. Marukian S, Andrus L, Sheahan TP, et al,. Hepatitis C virus induces interferon-lambda and interferon-stimulated genes in primary liver cultures. Hepatology 2011; 54 (6): 1913-1923.
40. 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 (44): 30079-30089.
41. 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.
42. Suppiah V, Moldovan M, Ahlenstiel G, et al,. IL28B is associated with response to chronic hepatitis C interferon-alpha and ribavirin therapy. Nat Genet 2009; 41 (10): 1100-1104.
43. Tanaka Y, Nishida N, Sugiyama M, et al,. Genome-wide association of IL28B with response to pegylated interferon-alpha and ribavirin therapy for chronic hepatitis C. Nat Genet 2009; 41 (10): 1105-1109.
44. Thomas DL, Thio CL, Martin MP, et al,. Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature 2009; 461 (7265): 798-801.
45. Ge D, Fellay J, Thompson AJ, et al,. Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature 2009; 461 (7262): 399-401.
46. Miller DM, Klucher KM, Freeman JA, Hausman DF, Fontana D, Williams DE,. Interferon lambda as a potential new therapeutic for hepatitis C. Ann N Y Acad Sci 2009; 1182: 80-87.
47. Muir AJ, Shiffman ML, Zaman A, 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 (3): 822-832.
48. Bataller R, Paik YH, Lindquist JN, Lemasters JJ, Brenner DA,. Hepatitis C virus core and nonstructural proteins induce fibrogenic effects in hepatic stellate cells. Gastroenterology 2004; 126 (2): 529-540.
49. Mazzocca A, Carloni V, Sciammetta S, et al,. Expression of transmembrane 4 superfamily (TM4SF) proteins and their role in hepatic stellate cell motility and wound healing migration. J Hepatol 2002; 37 (3): 322-330.
50. Kanzler H, Barrat FJ, Hessel EM, Coffman RL,. Therapeutic targeting of innate immunity with Toll-like receptor agonists and antagonists. Nat Med 2007; 13 (5): 552-559.