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Journal of Immunology Research
Volume 2017, Article ID 7232361, 12 pages
https://doi.org/10.1155/2017/7232361
Review Article

The Role of Type III Interferons in Hepatitis C Virus Infection and Therapy

Institute for Experimental Virology, Centre for Experimental and Clinical Infection Research (TWINCORE), Hannover, Germany

Correspondence should be addressed to Gisa Gerold; ed.erocniwt@dloreg.asig

Received 11 November 2016; Accepted 9 January 2017; Published 1 February 2017

Academic Editor: Frank A. Schildberg

Copyright © 2017 Janina Bruening et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. V. Kotenko, G. Gallagher, V. V. Baurin et al., “IFN-λs mediate antiviral protection through a distinct class II cytokine receptor complex,” Nature Immunology, vol. 4, no. 1, pp. 69–77, 2003. View at Publisher · View at Google Scholar · View at Scopus
  2. P. Sheppard, W. Kindsvogel, W. Xu et al., “IL-28, IL-29 and their class II cytokine receptor IL-28R,” Nature Immunology, vol. 4, no. 1, pp. 63–68, 2003. View at Publisher · View at Google Scholar · View at Scopus
  3. O. J. Hamming, E. Terczyńska-Dyla, G. Vieyres et al., “Interferon lambda 4 signals via the IFNλ receptor to regulate antiviral activity against HCV and coronaviruses,” The EMBO Journal, vol. 32, no. 23, pp. 3055–3065, 2013. View at Publisher · View at Google Scholar · View at Scopus
  4. L. Prokunina-Olsson, B. Muchmore, W. Tang et al., “A variant upstream of IFNL3 (IL28B) creating a new interferon gene IFNL4 is associated with impaired clearance of hepatitis C virus,” Nature Genetics, vol. 45, no. 2, pp. 164–171, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. R. P. Donnelly and S. V. Kotenko, “Interferon-lambda: a new addition to an old family,” Journal of Interferon and Cytokine Research, vol. 30, no. 8, pp. 555–564, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. S. V. Kotenko, “The family of IL-10-related cytokines and their receptors: related, but to what extent?” Cytokine and Growth Factor Reviews, vol. 13, no. 3, pp. 223–240, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. B. A. Fox, P. O. Sheppard, and P. J. O'Hara, “The role of genomic data in the discovery, annotation and evolutionary interpretation of the interferon-lambda family,” PLoS ONE, vol. 4, no. 3, Article ID e4933, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. P. Hillyer, V. P. Mane, L. M. Schramm et al., “Expression profiles of human interferon-alpha and interferon-lambda subtypes are ligand- and cell-dependent,” Immunology and Cell Biology, vol. 90, no. 8, pp. 774–783, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. K. M. Spann, K. C. Tran, B. Chi, R. L. Rabin, and P. L. Collins, “Suppression of the induction of alpha, beta, and lambda interferons by the NS1 and NS2 proteins of human respiratory syncytial virus in human epithelial cells and macrophages [corrected],” Journal of Virology, vol. 78, pp. 4363–4369, 2004. View at Google Scholar
  10. I. Ioannidis, F. Ye, B. McNally, M. Willette, and E. Flaño, “Toll-like receptor expression and induction of type I and type III interferons in primary airway epithelial cells,” Journal of Virology, vol. 87, no. 6, pp. 3261–3270, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. N. Ank, H. West, C. Bartholdy, K. Eriksson, A. R. Thomsen, and S. R. Paludan, “Lambda interferon (IFN-λ), a type III IFN, is induced by viruses and IFNs and displays potent antiviral activity against select virus infections in vivo,” Journal of Virology, vol. 80, no. 9, pp. 4501–4509, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. E. M. Coccia, M. Severa, E. Giacomini et al., “Viral infection and toll-like receptor agonists induce a differential expression of type I and λ interferons in humans plasmacytoid and monocyte-derived dendritic cells,” European Journal of Immunology, vol. 34, no. 3, pp. 796–805, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. B. Langhans, B. Kupfer, I. Braunschweiger et al., “Interferon-lambda serum levels in hepatitis C,” Journal of Hepatology, vol. 54, no. 5, pp. 859–865, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. J. Diegelmann, F. Beigel, K. Zitzmann et al., “Comparative analysis of the lambda-interferons IL-28A and IL-29 regarding their transcriptome and their antiviral properties against hepatitis C virus,” PLoS ONE, vol. 5, no. 12, Article ID e15200, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. S. Mihm, M. Frese, V. Meier et al., “Interferon type I gene expression in chronic hepatitis C,” Laboratory Investigation, vol. 84, no. 9, pp. 1148–1159, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Egli, D. M. Santer, D. O'Shea, D. L. Tyrrell, and M. Houghton, “The impact of the interferon-lambda family on the innate and adaptive immune response to viral infections,” Emerging Microbes and Infections, vol. 3, article no. e51, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. S. J. Griffiths, M. Koegl, C. Boutell et al., “A systematic analysis of host factors reveals a Med23-interferon-λ regulatory axis against herpes simplex virus type 1 replication,” PLoS Pathogens, vol. 9, no. 8, Article ID e1003514, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. K. Wolk, K. Witte, E. Witte et al., “Maturing dendritic cells are an important source of IL-29 and IL-20 that may cooperatively increase the innate immunity of keratinocytes,” Journal of Leukocyte Biology, vol. 83, no. 5, pp. 1181–1193, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. Z. Yin, J. Dai, J. Deng et al., “Type III IFNs are produced by and stimulate human plasmacytoid dendritic cells,” Journal of Immunology, vol. 189, no. 6, pp. 2735–2745, 2012. View at Publisher · View at Google Scholar · View at Scopus
  20. H. Lauterbach, B. Bathke, S. Gilles et al., “Mouse CD8α+ DCs and human BDCA3+ DCs are major producers of IFN-λ in response to poly IC,” Journal of Experimental Medicine, vol. 207, no. 12, pp. 2703–2717, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. N. J. Megjugorac, G. E. Gallagher, and G. Gallagher, “IL-4 enhances IFN-λ1 (IL-29) production by plasmacytoid DCs via monocyte secretion of IL-1Ra,” Blood, vol. 115, no. 21, pp. 4185–4190, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. N. A. Jewell, T. Cline, S. E. Mertz et al., “Lambda interferon is the predominant interferon induced by influenza A virus infection in vivo,” Journal of Virology, vol. 84, no. 21, pp. 11515–11522, 2010. View at Publisher · View at Google Scholar · View at Scopus
  23. M. R. Khaitov, V. Laza-Stanca, M. R. Edwards et al., “Respiratory virus induction of alpha-, beta- and lambda-interferons in bronchial epithelial cells and peripheral blood mononuclear cells,” Allergy, vol. 64, no. 3, pp. 375–386, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Sheahan, T. E. Morrison, W. Funkhouser et al., “MyD88 is required for protection from lethal infection with a mouse-adapted SARS-CoV,” PLoS Pathogens, vol. 4, no. 12, Article ID e1000240, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. P. K. Chandra, L. Bao, K. Song et al., “HCV infection selectively impairs type i but not type III IFN signaling,” American Journal of Pathology, vol. 184, no. 1, pp. 214–229, 2014. View at Publisher · View at Google Scholar · View at Scopus
  26. W. Hou, X. Wang, L. Ye et al., “Lambda interferon inhibits human immunodeficiency virus type 1 infection of macrophages,” Journal of Virology, vol. 83, no. 8, pp. 3834–3842, 2009. View at Publisher · View at Google Scholar · View at Scopus
  27. N. Ank, M. B. Iversen, C. Bartholdy et al., “An important role for type III interferon (IFN-λ/IL-28) in TLR-induced antiviral activity,” Journal of Immunology, vol. 180, no. 4, pp. 2474–2485, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Stoltz and J. Klingström, “Alpha/beta interferon (IFN-α/β)-independent induction of IFN-λ1 (interleukin-29) in response to Hantaan virus infection,” Journal of Virology, vol. 84, no. 18, pp. 9140–9148, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. A. G. Bowie and L. Unterholzner, “Viral evasion and subversion of pattern-recognition receptor signalling,” Nature Reviews Immunology, vol. 8, no. 12, pp. 911–922, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. M. G. Wathelet, C. H. Lin, B. S. Parekh, L. V. Ronco, P. M. Howley, and T. Maniatis, “Virus infection induces the assembly of coordinately activated transcription factors on the IFN-β enhancer in vivo,” Molecular Cell, vol. 1, no. 4, pp. 507–518, 1998. View at Publisher · View at Google Scholar · View at Scopus
  31. K. Onoguchi, M. Yoneyama, A. Takemura et al., “Viral infections activate types I and III interferon genes through a common mechanism,” Journal of Biological Chemistry, vol. 282, no. 10, pp. 7576–7581, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. P. I. Österlund, T. E. Pietilä, V. Veckman, S. V. Kotenko, and I. Julkunen, “IFN regulatory factor family members differentially regulate the expression of type III IFN (IFN-λ) genes,” Journal of Immunology, vol. 179, no. 6, pp. 3434–3442, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. S. J. P. Thomson, F. G. Goh, H. Banks et al., “The role of transposable elements in the regulation of IFN-λ1 gene expression,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 28, pp. 11564–11569, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. P. Génin, A. Vaccaro, and A. Civas, “The role of differential expression of human interferon—a genes in antiviral immunity,” Cytokine and Growth Factor Reviews, vol. 20, no. 4, pp. 283–295, 2009. View at Publisher · View at Google Scholar · View at Scopus
  35. K. Honda, A. Takaoka, and T. Taniguchi, “Type I inteferon gene induction by the interferon regulatory factor family of transcription factors,” Immunity, vol. 25, no. 3, pp. 349–360, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. H. C. Lee, S. Narayanan, S. J. Park, S. Y. Seong, and Y. S. Hahn, “Transcriptional regulation of IFN-λ genes in hepatitis C virus-infected hepatocytes via IRF-3IRF-7NF-κB complex,” The Journal of Biological Chemistry, vol. 289, pp. 5310–5319, 2014. View at Google Scholar
  37. F. Sievers, A. Wilm, D. Dineen et al., “Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega,” Molecular Systems Biology, vol. 7, article 539, 2011. View at Publisher · View at Google Scholar · View at Scopus
  38. T. R. O'Brien, L. Prokunina-Olsson, and R. P. Donnelly, “IFN-λ4: the paradoxical new member of the interferon lambda family,” Journal of Interferon & Cytokine Research, vol. 34, no. 11, pp. 829–838, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. S. M. Laidlaw and L. B. Dustin, “Interferon lambda: opportunities, risks, and uncertainties in the fight against HCV,” Frontiers in Immunology, vol. 5, article no. 545, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. Z. J. Miknis, E. Magracheva, W. Li, A. Zdanov, S. V. Kotenko, and A. Wlodawer, “Crystal structure of human interferon-λ1 in complex with its high-affinity receptor interferon-λR1,” Journal of Molecular Biology, vol. 404, no. 4, pp. 650–664, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. M. A. Jiménez-Sousa, J. Berenguer, A. Fernández-Rodríguez et al., “IL28RA polymorphism (rs10903035) is associated with insulin resistance in HIV/HCV-coinfected patients,” Journal of Viral Hepatitis, vol. 21, no. 3, pp. 189–197, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. V. Suppiah, M. Moldovan, G. Ahlenstiel et al., “IL28B is associated with response to chronic hepatitis C interferon-α and ribavirin therapy,” Nature Genetics, vol. 41, no. 10, pp. 1100–1104, 2009. View at Publisher · View at Google Scholar · View at Scopus
  43. H. H. Gad, C. Dellgren, O. J. Hamming, S. Vends, S. R. Paludan, and R. Hartmann, “Interferon-λ is functionally an interferon but structurally related to the interleukin-10 family,” Journal of Biological Chemistry, vol. 284, no. 31, pp. 20869–20875, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. J. Reboul, K. Gardiner, D. Monneron, G. Uzé, and G. Lutfalla, “Comparative genomic analysis of the interferon/interleukin-10 receptor gene cluster,” Genome Research, vol. 9, no. 3, pp. 242–250, 1999. View at Google Scholar · View at Scopus
  45. R. P. Donnelly, F. Sheikh, S. V. Kotenko, and H. Dickensheets, “The expanded family of class II cytokines that share the IL-10 receptor-2 (IL-10R2) chain,” Journal of Leukocyte Biology, vol. 76, no. 2, pp. 314–321, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. C. Sommereyns, S. Paul, P. Staeheli, and T. Michiels, “IFN-lambda (IFN-λ) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo,” PLoS Pathogens, vol. 4, no. 3, Article ID e1000017, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. H. Dickensheets, F. Sheikh, O. Park, B. Gao, and R. P. Donnelly, “Interferon-lambda (IFN-λ) induces signal transduction and gene expression in human hepatocytes, but not in lymphocytes or monocytes,” Journal of Leukocyte Biology, vol. 93, no. 3, pp. 377–385, 2013. View at Publisher · View at Google Scholar · View at Scopus
  48. E. Magracheva, S. Pletnev, S. Kotenko, W. Li, A. Wlodawer, and A. Zdanov, “Purification, crystallization and preliminary crystallographic studies of the complex of interferon-λ1 with its receptor,” Acta Crystallographica Section F: Structural Biology and Crystallization Communications, vol. 66, no. 1, pp. 61–63, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. S. E. Doyle, H. Schreckhise, K. Khuu-Duong et al., “Interleukin-29 uses a type 1 interferon-like program to promote antiviral responses in human hepatocytes,” Hepatology, vol. 44, no. 4, pp. 896–906, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. H. H. Gad, O. J. Hamming, and R. Hartmann, “The structure of human interferon lambda and what it has taught us,” Journal of Interferon and Cytokine Research, vol. 30, no. 8, pp. 565–571, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. N. Au-Yeung, R. Mandhana, and C. M. Horvath, “Transcriptional regulation by STAT1 and STAT2 in the interferon JAK-STAT pathway,” JAK-STAT, vol. 2, no. 3, Article ID e23931, 2013. View at Publisher · View at Google Scholar
  52. A. J. Sadler and B. R. G. Williams, “Interferon-inducible antiviral effectors,” Nature Reviews Immunology, vol. 8, no. 7, pp. 559–568, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. C. Kelly, P. Klenerman, and E. Barnes, “Interferon lambdas: the next cytokine storm,” Gut, vol. 60, no. 9, pp. 1284–1293, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. E. Kalie, D. A. Jaitin, Y. Podoplelova, J. Piehler, and G. Schreiber, “The stability of the ternary interferon-receptor complex rather than the affinity to the individual subunits dictates differential biological activities,” Journal of Biological Chemistry, vol. 283, no. 47, pp. 32925–32936, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. C. R. Bolen, S. Ding, M. D. Robek, and S. H. Kleinstein, “Dynamic expression profiling of type I and type III interferon-stimulated hepatocytes reveals a stable hierarchy of gene expression,” Hepatology, vol. 59, no. 4, pp. 1262–1272, 2014. View at Publisher · View at Google Scholar · View at Scopus
  56. S. Kearney, C. Delgado, and L. L. Lenz, “Differential effects of type I and II interferons on myeloid cells and resistance to intracellular bacterial infections,” Immunologic Research, vol. 55, no. 1, pp. 187–200, 2013. View at Publisher · View at Google Scholar · View at Scopus
  57. W. M. Schneider, M. D. Chevillotte, and C. M. Rice, “Interferon-stimulated genes: a complex web of host defenses,” Annual Review of Immunology, vol. 32, pp. 513–545, 2014. View at Publisher · View at Google Scholar · View at Scopus
  58. S. Ghosh and M. S. Hayden, “New regulators of NF-κB in inflammation,” Nature Reviews Immunology, vol. 8, no. 11, pp. 837–848, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. T. Mahlakõiv, D. Ritz, M. Mordstein et al., “Combined action of type I and type III interferon restricts initial replication of severe acute respiratory syndrome coronavirus in the lung but fails to inhibit systemic virus spread,” Journal of General Virology, vol. 93, no. 12, pp. 2601–2605, 2012. View at Publisher · View at Google Scholar · View at Scopus
  60. A. Yoshimura, T. Naka, and M. Kubo, “SOCS proteins, cytokine signalling and immune regulation,” Nature Reviews Immunology, vol. 7, no. 6, pp. 454–465, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. V. François-Newton, G. M. de Freitas Almeida, B. Payelle-Brogard et al., “USP18-based negative feedback control is induced by type I and type III interferons and specifically inactivates interferon α response,” PLoS ONE, vol. 6, no. 7, Article ID e22200, 2011. View at Publisher · View at Google Scholar · View at Scopus
  62. C. Dellgren, H. H. Gad, O. J. Hamming, J. Melchjorsen, and R. Hartmann, “Human interferon-λ3 is a potent member of the type III interferon family,” Genes and Immunity, vol. 10, no. 2, pp. 125–131, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. D. B. Smith, J. Bukh, C. Kuiken et al., “Expanded classification of hepatitis C virus into 7 genotypes and 67 subtypes: updated criteria and genotype assignment web resource,” Hepatology, vol. 59, no. 1, pp. 318–327, 2014. View at Publisher · View at Google Scholar · View at Scopus
  64. B. D. Lindenbach and C. M. Rice, “The ins and outs of hepatitis C virus entry and assembly,” Nature Reviews Microbiology, vol. 11, no. 10, pp. 688–700, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. D. Paul, V. Madan, and R. Bartenschlager, “Hepatitis C virus RNA replication and assembly: living on the fat of the land,” Cell Host and Microbe, vol. 16, no. 5, pp. 569–579, 2014. View at Publisher · View at Google Scholar · View at Scopus
  66. E. Gower, C. Estes, S. Blach, K. Razavi-Shearer, and H. Razavi, “Global epidemiology and genotype distribution of the hepatitis C virus infection,” Journal of Hepatology, vol. 61, no. 1, pp. S45–S57, 2014. View at Publisher · View at Google Scholar · View at Scopus
  67. P. K. Nelson, B. M. Mathers, B. Cowie et al., “Global epidemiology of hepatitis B and hepatitis C in people who inject drugs: results of systematic reviews,” The Lancet, vol. 378, no. 9791, pp. 571–583, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. Q. Ding, M. Von Schaewen, and A. Ploss, “The impact of hepatitis C virus entry on viral tropism,” Cell Host and Microbe, vol. 16, no. 5, pp. 562–568, 2014. View at Publisher · View at Google Scholar · View at Scopus
  69. V. Rocha-Perugini, C. Montpellier, D. Delgrange et al., “The CD81 partner EWI-2wint inhibits hepatitis C virus entry,” PLoS ONE, vol. 3, no. 4, Article ID e1866, 2008. View at Publisher · View at Google Scholar · View at Scopus
  70. WHO, “Guidelines for the screening, care and treatment of persons with chronic hepatitis C infection,” http://www.who.int/hepatitis/publications/hepatitis-c-guidelines-2016/en/.
  71. F. Douam, Q. Ding, and A. Ploss, “Recent advances in understanding hepatitis C,” F1000Research, vol. 5, Article ID F1000 Faculty Rev-131, 2016. View at Publisher · View at Google Scholar
  72. C. M. Lange, I. M. Jacobson, C. M. Rice, and S. Zeuzem, “Emerging therapies for the treatment of hepatitis C,” EMBO Molecular Medicine, vol. 6, no. 1, pp. 4–15, 2014. View at Publisher · View at Google Scholar · View at Scopus
  73. R. Sumpter Jr., Y.-M. Loo, E. Foy et al., “Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I,” Journal of Virology, vol. 79, no. 5, pp. 2689–2699, 2005. View at Publisher · View at Google Scholar · View at Scopus
  74. B. Israelow, C. M. Narbus, M. Sourisseau, and M. J. Evans, “HepG2 cells mount an effective antiviral interferon-lambda based innate immune response to hepatitis C virus infection,” Hepatology, vol. 60, no. 4, pp. 1170–1179, 2014. View at Publisher · View at Google Scholar · View at Scopus
  75. X. Du, T. Pan, J. Xu et al., “Hepatitis C virus replicative double-stranded RNA is a potent interferon inducer that triggers interferon production through MDA5,” Journal of General Virology, vol. 97, no. 11, pp. 2868–2882, 2016. View at Publisher · View at Google Scholar
  76. F. Hou, L. Sun, H. Zheng, B. Skaug, Q. X. Jiang, and Z. J. Chen, “MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response,” Cell, vol. 146, no. 3, pp. 448–461, 2011. View at Publisher · View at Google Scholar
  77. H. Dansako, D. Yamane, C. Welsch et al., “Class A scavenger receptor 1 (MSR1) restricts hepatitis C virus replication by mediating toll-like receptor 3 recognition of viral RNAs produced in neighboring cells,” PLoS Pathogens, vol. 9, no. 5, Article ID e1003345, 2013. View at Publisher · View at Google Scholar · View at Scopus
  78. M. Dreux, P. Gastaminza, S. F. Wieland, and F. V. Chisari, “The autophagy machinery is required to initiate hepatitis C virus replication,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 33, pp. 14046–14051, 2009. View at Publisher · View at Google Scholar · View at Scopus
  79. K. A. Fitzgerald, S. M. McWhirter, K. L. Faia et al., “IKKE and TBKI are essential components of the IRF3 signalling pathway,” Nature Immunology, vol. 4, no. 5, pp. 491–496, 2003. View at Publisher · View at Google Scholar · View at Scopus
  80. R. B. Seth, L. Sun, C.-K. Ea, and Z. J. Chen, “Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-κB and IRF3,” Cell, vol. 122, no. 5, pp. 669–682, 2005. View at Publisher · View at Google Scholar · View at Scopus
  81. E. Foy, K. Li, C. Wang et al., “Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease,” Science, vol. 300, no. 5622, pp. 1145–1148, 2003. View at Publisher · View at Google Scholar · View at Scopus
  82. X.-D. Li, L. Sun, R. B. Seth, G. Pineda, and Z. J. Chen, “Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signaling protein off the mitochondria to evade innate immunity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 49, pp. 17717–17722, 2005. View at Publisher · View at Google Scholar · View at Scopus
  83. E. Meylan, J. Curran, K. Hofmann et al., “Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus,” Nature, vol. 437, no. 7062, pp. 1167–1172, 2005. View at Publisher · View at Google Scholar · View at Scopus
  84. A. R. Ferreira, A. C. Magalhães, F. Camões et al., “Hepatitis C virus NS3-4A inhibits the peroxisomal MAVS-dependent antiviral signalling response,” Journal of Cellular and Molecular Medicine, vol. 20, no. 4, pp. 750–757, 2016. View at Publisher · View at Google Scholar · View at Scopus
  85. K. Li, E. Foy, J. C. Ferreon et al., “Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 8, pp. 2992–2997, 2005. View at Publisher · View at Google Scholar · View at Scopus
  86. Anggakusuma, R. J. Brown, D. Banda et al., “Hepacivirus NS3/4A proteases interfere with MAVS signaling in both their cognate animal hosts and humans: implications for zoonotic transmission,” Journal of Virology, vol. 90, no. 23, pp. 10670–10681, 2016. View at Google Scholar
  87. A. Dolganiuc, K. Kodys, C. Marshall et al., “Type III interferons, IL-28 and IL-29, are increased in chronic HCV infection and induce myeloid dendritic cell-mediated FoxP3+ regulatory T cells,” PLoS ONE, vol. 7, no. 10, Article ID e44915, 2012. View at Publisher · View at Google Scholar · View at Scopus
  88. E. Thomas, V. D. Gonzalez, Q. Li et al., “HCV infection induces a unique hepatic innate immune response associated with robust production of type III interferons,” Gastroenterology, vol. 142, no. 4, pp. 978–988, 2012. View at Publisher · View at Google Scholar · View at Scopus
  89. F. H. Duong, G. Trincucci, T. Boldanova et al., “IFN-λ receptor 1 expression is induced in chronic hepatitis C and correlates with the IFN-λ3 genotype and with nonresponsiveness to IFN-α therapies,” The Journal of Experimental Medicine, vol. 211, no. 5, pp. 857–868, 2014. View at Publisher · View at Google Scholar
  90. E. Terczyńska-Dyla, S. Bibert, F. H. Duong et al., “Reduced IFNλ4 activity is associated with improved HCV clearance and reduced expression of interferon-stimulated genes,” Nature Communications, vol. 5, article 5699, 2014. View at Publisher · View at Google Scholar
  91. H. Park, E. Serti, O. Eke et al., “IL-29 is the dominant type III interferon produced by hepatocytes during acute hepatitis C virus infection,” Hepatology, vol. 56, no. 6, pp. 2060–2070, 2012. View at Publisher · View at Google Scholar · View at Scopus
  92. M. Dorner, J. A. Horwitz, B. M. Donovan et al., “Completion of the entire hepatitis C virus life cycle in genetically humanized mice,” Nature, vol. 501, no. 7466, pp. 237–241, 2013. View at Publisher · View at Google Scholar · View at Scopus
  93. Anggakusuma, A. Frentzen, E. Gürlevik et al., “Control of hepatitis C virus replication in mouse liver-derived cells by MAVS-dependent production of type I and type III interferons,” Journal of Virology, vol. 89, no. 7, pp. 3833–3845, 2015. View at Publisher · View at Google Scholar · View at Scopus
  94. M. A. Scull, C. Shi, Y. P. de Jong et al., “Hepatitis C virus infects rhesus macaque hepatocytes and simianized mice,” Hepatology, vol. 62, no. 1, pp. 57–67, 2015. View at Publisher · View at Google Scholar · View at Scopus
  95. M. Sourisseau, O. Goldman, W. He et al., “Hepatic cells derived from induced pluripotent stem cells of pigtail macaques support hepatitis C virus infection,” Gastroenterology, vol. 145, no. 5, pp. 966.e7–969.e7, 2013. View at Publisher · View at Google Scholar · View at Scopus
  96. A. Kapoor, P. Simmonds, T. K. H. Scheel et al., “Identification of rodent homologs of hepatitis C virus and pegiviruses,” mBio, vol. 4, no. 2, Article ID e00216-13, 2013. View at Publisher · View at Google Scholar · View at Scopus
  97. J. F. Drexler, V. M. Corman, M. A. Müller et al., “Evidence for novel hepaciviruses in rodents,” PLoS Pathogens, vol. 9, no. 6, Article ID e1003438, 2013. View at Publisher · View at Google Scholar · View at Scopus
  98. S. Marukian, L. Andrus, T. P. Sheahan et al., “Hepatitis C virus induces interferon-λ and interferon-stimulated genes in primary liver cultures,” Hepatology, vol. 54, no. 6, pp. 1913–1923, 2011. View at Publisher · View at Google Scholar · View at Scopus
  99. T. Sheahan, N. Imanaka, S. Marukian et al., “Interferon lambda alleles predict innate antiviral immune responses and hepatitis C virus permissiveness,” Cell Host and Microbe, vol. 15, no. 2, pp. 190–202, 2014. View at Publisher · View at Google Scholar · View at Scopus
  100. M. Hong, J. Schwerk, C. Lim et al., “Interferon lambda 4 expression is suppressed by the host during viral infection,” The Journal of Experimental Medicine, vol. 213, no. 12, pp. 2539–2552, 2016. View at Publisher · View at Google Scholar
  101. O. O. Onabajo, P. Porter-Gill, A. Paquin et al., “Expression of interferon lambda 4 is associated with reduced proliferation and increased cell death in human hepatic cells,” Journal of Interferon and Cytokine Research, vol. 35, no. 11, pp. 888–900, 2015. View at Publisher · View at Google Scholar · View at Scopus
  102. U. Protzer, M. K. Maini, and P. A. Knolle, “Living in the liver: hepatic infections,” Nature Reviews Immunology, vol. 12, no. 3, pp. 201–213, 2012. View at Publisher · View at Google Scholar · View at Scopus
  103. T. Marcello, A. Grakoui, G. Barba-Spaeth et al., “Interferons α and λ inhibit hepatitis c virus replication with distinct signal transduction and gene regulation kinetics,” Gastroenterology, vol. 131, no. 6, pp. 1887–1898, 2006. View at Publisher · View at Google Scholar · View at Scopus
  104. M. D. Robek, B. S. Boyd, and F. V. Chisari, “Lambda interferon inhibits hepatitis B and C virus replication,” Journal of Virology, vol. 79, no. 6, pp. 3851–3854, 2005. View at Publisher · View at Google Scholar · View at Scopus
  105. C. Lauber, G. Vieyres, E. Terczyńska-Dyla et al., “Transcriptome analysis reveals a classical interferon signature induced by IFNλ4 in human primary cells,” Genes and Immunity, vol. 16, no. 6, pp. 414–421, 2015. View at Publisher · View at Google Scholar · View at Scopus
  106. A. Carpentier, A. Tesfaye, V. Chu et al., “Engrafted human stem cell-derived hepatocytes establish an infectious HCV murine model,” Journal of Clinical Investigation, vol. 124, no. 11, pp. 4953–4964, 2014. View at Publisher · View at Google Scholar · View at Scopus
  107. X. Wu, J. M. Robotham, E. Lee et al., “Productive hepatitis C virus infection of stem cell-derived hepatocytes reveals a critical transition to viral permissiveness during differentiation,” PLoS Pathogens, vol. 8, no. 4, Article ID e1002617, 2012. View at Publisher · View at Google Scholar · View at Scopus
  108. R. E. Schwartz, K. Trehan, L. Andrus et al., “Modeling hepatitis C virus infection using human induced pluripotent stem cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 109, no. 7, pp. 2544–2548, 2012. View at Publisher · View at Google Scholar · View at Scopus
  109. V. Ramanan, M. A. Scull, T. P. Sheahan, C. M. Rice, and S. N. Bhatia, “New methods in tissue engineering: improved models for viral infection,” Annual Review of Virology, vol. 1, no. 1, pp. 475–499, 2014. View at Publisher · View at Google Scholar
  110. M. H. Heim, “25 years of interferon-based treatment of chronic hepatitis C: an epoch coming to an end,” Nature Reviews Immunology, vol. 13, no. 7, pp. 535–542, 2013. View at Publisher · View at Google Scholar · View at Scopus
  111. D. L. Thomas, C. L. Thio, M. P. Martin et al., “Genetic variation in IL28B and spontaneous clearance of hepatitis C virus,” Nature, vol. 461, no. 7265, pp. 798–801, 2009. View at Publisher · View at Google Scholar · View at Scopus
  112. D. Ge, J. Fellay, A. J. Thompson et al., “Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance,” Nature, vol. 461, no. 7262, pp. 399–401, 2009. View at Publisher · View at Google Scholar · View at Scopus
  113. A. Rauch, Z. Kutalik, P. Descombes et al., “Genetic variation in IL28B is associated with chronic hepatitis C and treatment failure: A Genome-Wide Association Study,” Gastroenterology, vol. 138, no. 4, pp. 1338.e7–1345.e7, 2010. View at Publisher · View at Google Scholar · View at Scopus
  114. P. Duggal, C. L. Thio, G. L. Wojcik et al., “Genome-wide association study of spontaneous resolution of hepatitis C virus infection: data from multiple cohorts,” Annals of Internal Medicine, vol. 158, no. 4, pp. 235–245, 2013. View at Publisher · View at Google Scholar · View at Scopus
  115. Y. Tanaka, N. Nishida, M. Sugiyama et al., “Genome-wide association of IL28B with response to pegylated interferon-α and ribavirin therapy for chronic hepatitis C,” Nature Genetics, vol. 41, no. 10, pp. 1105–1109, 2009. View at Publisher · View at Google Scholar · View at Scopus
  116. S. Bibert, T. Roger, T. Calandra et al., “IL28B expression depends on a novel TT/-G polymorphism which improves HCV clearance prediction,” The Journal of Experimental Medicine, vol. 210, no. 6, pp. 1109–1116, 2013. View at Publisher · View at Google Scholar · View at Scopus
  117. N. Antaki, S. Bibert, K. Kebbewar et al., “IL28B polymorphisms predict response to therapy among chronic hepatitis C patients with HCV genotype 4,” Journal of Viral Hepatitis, vol. 20, no. 1, pp. 59–64, 2013. View at Publisher · View at Google Scholar · View at Scopus
  118. A. P. McFarland, S. M. Horner, A. Jarret et al., “The favorable IFNL3 genotype escapes mRNA decay mediated by AU-rich elements and hepatitis C virus-induced microRNAs,” Nature Immunology, vol. 15, pp. 72–79, 2014. View at Publisher · View at Google Scholar · View at Scopus
  119. M. Sarasin-Filipowicz, E. J. Oakeley, F. H. T. Duong et al., “Interferon signaling and treatment outcome in chronic hepatitis C,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 19, pp. 7034–7039, 2008. View at Publisher · View at Google Scholar · View at Scopus
  120. T. Asselah, I. Bieche, S. Narguet et al., “Liver gene expression signature to predict response to pegylated interferon plus ribavirin combination therapy in patients with chronic hepatitis C,” Gut, vol. 57, no. 4, pp. 516–524, 2008. View at Publisher · View at Google Scholar · View at Scopus
  121. L. Chen, I. Borozan, J. Feld et al., “Hepatic gene expression discriminates responders and nonresponders in treatment of chronic hepatitis C viral infection,” Gastroenterology, vol. 128, no. 5, pp. 1437–1444, 2005. View at Publisher · View at Google Scholar · View at Scopus
  122. A. J. Muir, “IL28B in the era of direct-acting antivirals for hepatitis C,” Journal of Clinical Gastroenterology, vol. 47, no. 3, pp. 222–227, 2013. View at Publisher · View at Google Scholar · View at Scopus
  123. S. Zeuzem, V. Soriano, T. Asselah et al., “Faldaprevir and deleobuvir for HCV genotype 1 infection,” New England Journal of Medicine, vol. 369, no. 7, pp. 630–639, 2013. View at Publisher · View at Google Scholar · View at Scopus
  124. E. G. Meissner, D. Bon, L. Prokunina-Olsson et al., “IFNL4-ΔG genotype is associated with slower viral clearance in Hepatitis C, genotype-1 patients treated with sofosbuvir and ribavirin,” Journal of Infectious Diseases, vol. 209, no. 11, pp. 1700–1704, 2014. View at Publisher · View at Google Scholar · View at Scopus
  125. P. V. Aka, M. H. Kuniholm, R. M. Pfeiffer et al., “Association of the IFNL4-ΔG allele with impaired spontaneous clearance of hepatitis C virus,” Journal of Infectious Diseases, vol. 209, no. 3, pp. 350–354, 2014. View at Publisher · View at Google Scholar · View at Scopus
  126. S. Chinnaswamy, “Gene-disease association with human IFNL locus polymorphisms extends beyond hepatitis C virus infections,” Genes and Immunity, vol. 17, no. 5, pp. 265–275, 2016. View at Publisher · View at Google Scholar · View at Scopus
  127. N. Jilg, W. Lin, J. Hong et al., “Kinetic differences in the induction of interferon stimulated genes by interferon-α and interleukin 28B are altered by infection with hepatitis C virus,” Hepatology, vol. 59, no. 4, pp. 1250–1261, 2014. View at Publisher · View at Google Scholar · View at Scopus
  128. A. J. Muir, M. L. Shiffman, A. Zaman 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, vol. 52, no. 3, pp. 822–832, 2010. View at Publisher · View at Google Scholar · View at Scopus
  129. A. J. Muir, S. Arora, G. Everson et al., “A randomized phase 2b study of peginterferon lambda-1a for the treatment of chronic HCV infection,” Journal of Hepatology, vol. 61, no. 6, pp. 1238–1246, 2014. View at Publisher · View at Google Scholar · View at Scopus
  130. R. Flisiak, S. Kawazoe, O. Znoyko et al., “Peginterferon lambda-1a/ribavirin with daclatasvir or peginterferon alfa-2a/ribavirin with telaprevir for chronic hepatitis C genotype 1b,” Journal of Interferon & Cytokine Research, vol. 36, no. 11, pp. 635–643, 2016. View at Publisher · View at Google Scholar
  131. R. Flisiak, M. Shiffman, J. Arenas et al., “A randomized study of peginterferon lambda-1a compared to peginterferon Alfa-2a in combination with Ribavirin and telaprevir in patients with genotype-1 chronic hepatitis C,” PLoS ONE, vol. 11, no. 10, Article ID e0164563, p. e0164563, 2016. View at Publisher · View at Google Scholar
  132. D. Yu, M. Zhao, L. Dong et al., “Design and evaluation of novel interferon lambda analogs with enhanced antiviral activity and improved drug attributes,” Drug Design, Development and Therapy, vol. 10, pp. 163–182, 2016. View at Publisher · View at Google Scholar · View at Scopus
  133. “Bringing the hepatitis C virus to life,” Cell, vol. 167, no. 1, pp. 39–42, 2016. View at Publisher · View at Google Scholar
  134. D. Todt, C. François, Anggakusuma et al., “Antiviral activities of different interferon types and subtypes against Hepatitis E virus replication,” Antimicrobial Agents and Chemotherapy, vol. 60, no. 4, pp. 2132–2139, 2016. View at Publisher · View at Google Scholar · View at Scopus