Early inhibition of hepatocyte innate responses by hepatitis B virus

Journal of Hepatology

Volumn 63, Issue 6, 2015, Pages 1314-1322

  Luangsay, Souphalone ^a,b   Gruffaz, Marion ^a,b   Isorce, Nathalie ^a,b   Testoni, Barbara ^a,b   Michelet, Maud ^a,b   Faure Dupuy, Suzanne ^a,b   Maadadi, Sarah ^a,b   Ait Goughoulte, Malika ^a,b   Parent, Romain ^a,b   Rivoire, Michel ^c,d   Javanbakht, Hassan ^e   Lucifora, Julie ^a,b   Durantel, David ^a,b   Zoulim, Fabien ^a,b,f,g  

^a CENTRE DE RECHERCHE EN CANCÉROLOGIE DE LYON   (France)

^b UNIVERSITÉ LYON 1   (France)

^c CENTRE LÉON BÉRARD   (France)

^d LABTAU   (France)

^e F HOFFMANN LA ROCHE LTD   (Switzerland)

^f HOSPICES CIVILS DE LYON   (France)

^g INSTITUT UNIVERSITAIRE DE FRANCE   (France)

Author keywords

dsRNA mediated innate immunity; Early host virus interaction; Hepatitis B virus; Hepatocytes; IFN response

Indexed keywords

BETA INTERFERON; GAMMA INTERFERON; INTERLEUKIN 1BETA; INTERLEUKIN 29; INTERLEUKIN 6; MELANOMA DIFFERENTIATION ASSOCIATED 5 PROTEIN; PROTEIN; RETINOIC ACID INDUCIBLE PROTEIN I; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG; DOUBLE STRANDED RNA; HEPATITIS B SURFACE ANTIGEN; HEPATITIS B(E) ANTIGEN; IL6 PROTEIN, HUMAN;

ANTIGEN DETECTION; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; GENE EXPRESSION; HEPATITIS B; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; IMMUNOGENETICS; IN VITRO STUDY; INNATE IMMUNITY; LIVER CELL; MOLECULAR PATHOLOGY; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VIRAL CLEARANCE; VIRION; VIRUS CELL INTERACTION; VIRUS DETECTION; VIRUS IMMUNITY; VIRUS PATHOGENESIS; BIOSYNTHESIS; CELL CULTURE; CELL LINE; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; PATHOGENICITY; VIROLOGY;

CELL LINE; CELLS, CULTURED; GENE EXPRESSION; HEPATITIS B E ANTIGENS; HEPATITIS B SURFACE ANTIGENS; HEPATITIS B VIRUS; HEPATOCYTES; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; INTERLEUKIN-6; RNA, DOUBLE-STRANDED;

EID: 84951107024     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2015.07.014     Document Type: Article

References (39)

1. A. Arzumanyan, H.M. Reis, and M.A. Feitelson Pathogenic mechanisms in HBV- and HCV-associated hepatocellular carcinoma Nat Rev Cancer 13 2013 123 135
2. A. Bertoletti, and C. Ferrari Innate and adaptive immune responses in chronic hepatitis B virus infections: towards restoration of immune control of viral infection Gut 61 2012 1754 1764
3. F. Zoulim Are novel combination therapies needed for chronic hepatitis B? Antiviral Res 96 2012 256 259
4. H. Kumar, T. Kawai, and S. Akira Pathogen recognition by the innate immune system Int Rev Immunol 30 2011 16 34
5. M. Ait-Goughoulte, J. Lucifora, F. Zoulim, and D. Durantel Innate antiviral immune responses to hepatitis B virus Viruses 2 2010 1394 1410
6. M. Dandri, and S. Locarnini New insight in the pathobiology of hepatitis B virus infection Gut 61 2012 i6 i17
7. C. Dunn, D. Peppa, P. Khanna, G. Nebbia, M. Jones, N. Brendish, and et al. Temporal analysis of early immune responses in patients with acute hepatitis B virus infection Gastroenterology 137 2009 1289 1300
8. S.P. Fletcher, D.J. Chin, Y. Ji, A.L. Iniguez, B. Taillon, D.C. Swinney, and et al. Transcriptomic analysis of the woodchuck model of chronic hepatitis B Hepatology 56 2012 820 830
9. A.R. Stacey, P.J. Norris, L. Qin, E.A. Haygreen, E. Taylor, J. Heitman, and et al. Induction of a striking systemic cytokine cascade prior to peak viremia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections J Virol 83 2009 3719 3733
10. S. Wieland, R. Thimme, R.H. Purcell, and F.V. Chisari Genomic analysis of the host response to hepatitis B virus infection Proc Natl Acad Sci U S A 101 2004 6669 6674
11. S.F. Wieland, A. Eustaquio, C. Whitten-Bauer, B. Boyd, and F.V. Chisari Interferon prevents formation of replication-competent hepatitis B virus RNA-containing nucleocapsids Proc Natl Acad Sci U S A 102 2005 9913 9917
12. T. Lang, C. Lo, N. Skinner, S. Locarnini, K. Visvanathan, and A. Mansell The hepatitis B e antigen (HBeAg) targets and suppresses activation of the toll-like receptor signaling pathway J Hepatol 55 2011 762 769
13. K. Visvanathan, N.A. Skinner, A.J. Thompson, S.M. Riordan, V. Sozzi, R. Edwards, and et al. Regulation of Toll-like receptor-2 expression in chronic hepatitis B by the precore protein Hepatology 45 2007 102 110
14. J. Wu, Z. Meng, M. Jiang, R. Pei, M. Trippler, R. Broering, and et al. Hepatitis B virus suppresses toll-like receptor-mediated innate immune responses in murine parenchymal and nonparenchymal liver cells Hepatology 49 2009 1132 1140
15. V. Christen, F. Duong, C. Bernsmeier, D. Sun, M. Nassal, and M.H. Heim Inhibition of alpha interferon signaling by hepatitis B virus J Virol 81 2007 159 165
16. M. Fernandez, J.A. Quiroga, and V. Carreno Hepatitis B virus downregulates the human interferon-inducible MxA promoter through direct interaction of precore/core proteins J Gen Virol 84 2003 2073 2082
17. M. Lutgehetmann, T. Bornscheuer, T. Volz, L. Allweiss, J.H. Bockmann, J.M. Pollok, and et al. Hepatitis B virus limits response of human hepatocytes to interferon-alpha in chimeric mice Gastroenterology 140 2011 2074 2083 2083, e2071-e2072
18. M. Tsuge, S. Takahashi, N. Hiraga, Y. Fujimoto, Y. Zhang, F. Mitsui, and et al. Effects of hepatitis B virus infection on the interferon response in immunodeficient human hepatocyte chimeric mice J Infect Dis 204 2011 224 228
19. J.S. Twu, C.H. Lee, P.M. Lin, and R.H. Schloemer Hepatitis B virus suppresses expression of human beta-interferon Proc Natl Acad Sci U S A 85 1988 252 256
20. M. Hosel, M. Quasdorff, K. Wiegmann, D. Webb, U. Zedler, M. Broxtermann, and et al. Not interferon, but interleukin-6 controls early gene expression in hepatitis B virus infection Hepatology 50 2009 1773 1782
21. P. Gripon, S. Rumin, S. Urban, J. Le Seyec, D. Glaise, I. Cannie, and et al. Infection of a human hepatoma cell line by hepatitis B virus Proc Natl Acad Sci U S A 99 2002 15655 15660
22. O. Hantz, R. Parent, D. Durantel, P. Gripon, C. Guguen-Guillouzo, and F. Zoulim Persistence of the hepatitis B virus covalently closed circular DNA in HepaRG human hepatocyte-like cells J Gen Virol 90 2009 127 135
23. R. Parent, M.J. Marion, L. Furio, C. Trepo, and M.A. Petit Origin and characterization of a human bipotent liver progenitor cell line Gastroenterology 126 2004 1147 1156
24. J. Lucifora, D. Durantel, B. Testoni, O. Hantz, M. Levrero, and F. Zoulim Control of hepatitis B virus replication by innate response of HepaRG cells Hepatology 51 2010 63 72
25. J. Lucifora, S. Arzberger, D. Durantel, L. Belloni, M. Strubin, M. Levrero, and et al. Hepatitis B virus X protein is essential to initiate and maintain virus replication after infection J Hepatol 55 2011 996 1003
26. A. Schulze, P. Gripon, and S. Urban Hepatitis B virus infection initiates with a large surface protein-dependent binding to heparan sulfate proteoglycans Hepatology 46 2007 1759 1768
27. E.L. Lecluyse, and E. Alexandre Isolation and culture of primary hepatocytes from resected human liver tissue Methods Mol Biol 640 2010 57 82
28. J. Lucifora, D. Durantel, L. Belloni, L. Barraud, S. Villet, I.E. Vincent, and et al. Initiation of hepatitis B virus genome replication and production of infectious virus following delivery in HepG2 cells by novel recombinant baculovirus vector J Gen Virol 89 2008 1819 1828
29. M. Ait-goughoulte, S. Luangsay, M. Gruffaz, S. Fletcher, M. Tommasino, D. Durantel, and et al. Characterisation of pathogen recognition receptors in an hepatocyte cell line (heparg cells) J Hepatol 54 2011 S110 S111
30. J. Lucifora, D. Durantel, B. Testoni, O. Hantz, M. Levrero, and F. Zoulim Control of hepatitis B virus replication by innate response of HepaRG cells Hepatology 51 2010 63 72
31. S. Urban, R. Bartenschlager, R. Kubitz, and F. Zoulim Strategies to inhibit entry of HBV and HDV into hepatocytes Gastroenterology 147 2014 48 64
32. C. Seeger, F. Zoulim, and W.S. Mason Hepadnaviruses D.M. Knipe, P.M. Howley, Fields virology 2007 Lippincott Williams and Wilkins Philadelphia 2977 3030
33. V. Pasquetto, S.F. Wieland, S.L. Uprichard, M. Tripodi, and F.V. Chisari Cytokine-sensitive replication of hepatitis B virus in immortalized mouse hepatocyte cultures J Virol 76 2002 5646 5653
34. J. Oquendo, S. Dubanchet, F. Capel, H. Mabit, and M.A. Petit Suppressive effect of hepatitis B virus on the induction of interleukin-1 beta and interleukin-6 gene expression in the THP-1 human monocytic cell line Eur Cytokine Netw 7 1996 793 800
35. P. Vanlandschoot, F. Van Houtte, A. Roobrouck, A. Farhoudi, and G. Leroux-Roels Hepatitis B virus surface antigen suppresses the activation of monocytes through interaction with a serum protein and a monocyte-specific receptor J Gen Virol 83 2002 1281 1289
36. P. Vanlandschoot, F. Van Houtte, A. Roobrouck, A. Farhoudi, F. Stelter, D.L. Peterson, and et al. LPS-binding protein and CD14-dependent attachment of hepatitis B surface antigen to monocytes is determined by the phospholipid moiety of the particles J Gen Virol 83 2002 2279 2289
37. I.E. Vincent, C. Zannetti, J. Lucifora, H. Norder, U. Protzer, P. Hainaut, and et al. Hepatitis B virus impairs TLR9 expression and function in plasmacytoid dendritic cells PLoS One 6 2011 e26315
38. N. Xu, H.P. Yao, G.C. Lv, and Z. Chen Downregulation of TLR7/9 leads to deficient production of IFN-alpha from plasmacytoid dendritic cells in chronic hepatitis B Inflamm Res 61 2012 997 1004
39. Y. Xu, Y. Hu, B. Shi, X. Zhang, J. Wang, Z. Zhang, and et al. HBsAg inhibits TLR9-mediated activation and IFN-alpha production in plasmacytoid dendritic cells Mol Immunol 46 2009 2640 2646