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Host Innate Immunity against Hepatitis E Virus and Viral Evasion Mechanisms

  • Kang, Sangmin (Korea Zoonosis Research Institute, Chonbuk National University) ;
  • Myoung, Jinjong (Korea Zoonosis Research Institute, Chonbuk National University)
  • Received : 2017.08.21
  • Accepted : 2017.09.25
  • Published : 2017.10.28

Abstract

Hepatitis E virus (HEV) infections cause epidemic or sporadic acute hepatitis, which are mostly self-limiting. However, viral infection in immunocompromised patients and pregnant women may result in serious consequences, such as chronic hepatitis and liver damage, mortality of the latter of which reaches up to 20-30%. Type I interferon (IFN)-induced antiviral immunity is known to be the first-line defense against virus infection. Upon HEV infection in the cell, the virus genome is recognized by pathogen recognition receptors, leading to rapid activation of intracellular signaling cascades. Expression of type I IFN triggers induction of a barrage of IFN-stimulated genes, helping the cells cope with viral infection. Interestingly, some of the HEV-encoded genes seem to be involved in disrupting signaling cascades for antiviral immune responses, and thus crippling cytokine/chemokine production. Antagonistic mechanisms of type I IFN responses by HEV have only recently begun to emerge, and in this review, we summarize known HEV evasion strategies and compare them with those of other hepatitis viruses.

Keywords

References

  1. Jameel S. 1999. Molecular biology and pathogenesis of hepatitis E virus. Expert Rev. Mol. Med. 1999: 1-16.
  2. Smith DB, Purdy MA, Simmonds P. 2013. Genetic variability and the classification of hepatitis E virus. J. Virol. 87: 4161-4169. https://doi.org/10.1128/JVI.02762-12
  3. Sridhar S, Teng JLL, Chiu TH, Lau SKP, Woo PCY. 2017. Hepatitis E virus genotypes and evolution: emergence of camel hepatitis E variants. Int. J. Mol. Sci. 18: E869. https://doi.org/10.3390/ijms18040869
  4. Pavio N, Meng XJ, Doceul V. 2015. Zoonotic origin of hepatitis E. Curr. Opin. Virol. 10: 34-41. https://doi.org/10.1016/j.coviro.2014.12.006
  5. Meng XJ. 2010. Hepatitis E virus: animal reservoirs and zoonotic risk. Vet. Microbiol. 140: 256-265. https://doi.org/10.1016/j.vetmic.2009.03.017
  6. Tam AW, Smith MM, Guerra ME, Huang CC, Bradley DW, Fry KE, et al. 1991. Hepatitis E virus (HEV): molecular cloning and sequencing of the full-length viral genome. Virology 185: 120-131. https://doi.org/10.1016/0042-6822(91)90760-9
  7. Graff J, Torian U, Nguyen H, Emerson SU. 2006. A bicistronic subgenomic mRNA encodes both the ORF2 and ORF3 proteins of hepatitis E virus. J. Virol. 80: 5919-5926. https://doi.org/10.1128/JVI.00046-06
  8. Kabrane-Lazizi Y, Fine JB, Elm J, Glass GE, Higa H, Diwan A, et al. 1999. Evidence for widespread infection of wild rats with hepatitis E virus in the United States. Am. J. Trop. Med. Hyg. 61: 331-335. https://doi.org/10.4269/ajtmh.1999.61.331
  9. Ropp S L, T am AW, B eames B, P urdy M , Frey TK. 2000. Expression of the hepatitis E virus ORF1. Arch. Virol. 145: 1321-1337. https://doi.org/10.1007/s007050070093
  10. Sehgal D, Thomas S, Chakraborty M, Jameel S. 2006. Expression and processing of the hepatitis E virus ORF1 nonstructural polyprotein. Virol. J. 3: 38. https://doi.org/10.1186/1743-422X-3-38
  11. Suppiah S , Zhou Y , Frey TK. 2011. Lack of processing of the expressed ORF1 gene product of hepatitis E virus. Virol. J. 8: 245. https://doi.org/10.1186/1743-422X-8-245
  12. Graff J, Zhou YH, Torian U, Nguyen H, St Claire M, Yu C, et al. 2008. Mutations within potential glycosylation sites in the capsid protein of hepatitis E virus prevent the formation of infectious virus particles. J. Virol. 82: 1185-1194. https://doi.org/10.1128/JVI.01219-07
  13. Qi Y, Zhang F, Zhang L, Harrison TJ, Huang W, Zhao C, et al. 2015. Hepatitis E virus produced from cell culture has a lipid envelope. PLoS One 10: e0132503. https://doi.org/10.1371/journal.pone.0132503
  14. Shiota T, Li TC, Yoshizaki S, Kato T, Wakita T, Ishii K. 2013. The hepatitis E virus capsid C-terminal region is essential for the viral life cycle: implication for viral genome encapsidation and particle stabilization. J. Virol. 87: 6031-6036. https://doi.org/10.1128/JVI.00444-13
  15. Takahashi M, Yamada K, Hoshino Y, Takahashi H, Ichiyama K, Tanaka T, et al. 2008. Monoclonal antibodies raised against the ORF3 protein of hepatitis E virus (HEV) can capture HEV particles in culture supernatant and serum but not those in feces. Arch. Virol. 153: 1703-1713. https://doi.org/10.1007/s00705-008-0179-6
  16. Yamada K, Takahashi M, Hoshino Y, Takahashi H, Ichiyama K, Nagashima S, et al. 2009. ORF3 p rotein of hepatitis E virus is essential for virion release from infected cells. J. Gen. Virol. 90: 1880-1891. https://doi.org/10.1099/vir.0.010561-0
  17. Nagashima S, Takahashi M, Jirintai, Tanaka T, Yamada K, Nishizawa T, et al. 2011. A PSAP motif in the ORF3 protein of hepatitis E virus is necessary for virion release from infected cells. J. Gen. Virol. 92: 269-278. https://doi.org/10.1099/vir.0.025791-0
  18. Kenney SP, Pudupakam RS, Huang YW, Pierson FW, LeRoith T, Meng XJ. 2012. The PSAP motif within the ORF3 protein of an avian strain of the hepatitis E virus is not critical for viral infectivity in vivo but plays a role in virus release. J. Virol. 86: 5637-5646. https://doi.org/10.1128/JVI.06711-11
  19. Nair VP, Anang S, Subramani C, Madhvi A, Bakshi K, Srivastava A, et al. 2016. Endoplasmic reticulum stress induced synthesis of a novel viral factor mediates efficient replication of genotype-1 hepatitis E virus. PLoS Pathog. 12: e1005521. https://doi.org/10.1371/journal.ppat.1005521
  20. Akira S, Uematsu S, Takeuchi O. 2006. Pathogen recognition and innate immunity. Cell 124: 783-801. https://doi.org/10.1016/j.cell.2006.02.015
  21. Medzhitov R. 2007. Recognition of microorganisms and activation of the immune response. Nature 449: 819-826. https://doi.org/10.1038/nature06246
  22. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, Kato H, et al. 2005. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 6: 981-988. https://doi.org/10.1038/ni1243
  23. Seth RB, Sun L, Ea CK, Chen ZJ. 2005. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122: 669-682. https://doi.org/10.1016/j.cell.2005.08.012
  24. Xu LG, Wang YY, Han KJ, Li LY, Z hai Z, S hu H B. 2005. VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol. Cell 19: 727-740. https://doi.org/10.1016/j.molcel.2005.08.014
  25. Hardy MP, McGettrick AF, O'Neill LA. 2004. Transcriptional regulation of the human TRIF (TIR domain-containing adaptor protein inducing interferon beta) gene. Biochem. J. 380: 83-93. https://doi.org/10.1042/bj20040030
  26. Yamamoto M, Sato S, Hemmi H, Hoshino K, Kaisho T, Sanjo H, et al. 2003. Role of adaptor TRIF in the MyD88- independent Toll-like receptor signaling pathway. Science 301: 640-643. https://doi.org/10.1126/science.1087262
  27. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, Golenbock DT, et al. 2003. IKKepsilon a nd TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4: 491-496.
  28. Hacker H, Karin M. 2006. Regulation and function of IKK and IKK-related kinases. Sci. STKE 2006: re13.
  29. Gatot JS, Gioia R, Chau TL, Patrascu F, Warnier M, Close P, et al. 2007. Lipopolysaccharide-mediated interferon regulatory factor activation involves TBK1-IKKepsilon-dependent Lys(63)-linked polyubiquitination and phosphorylation of TANK/I-TRAF. J. Biol. Chem. 282: 31131-31146. https://doi.org/10.1074/jbc.M701690200
  30. Grandvaux N, Servant MJ, tenOever B, Sen GC, Balachandran S, Barber GN, et al. 2002. Transcriptional profiling of interferon regulatory factor 3 target genes: direct involvement in the regulation of interferon-stimulated genes. J. Virol. 76: 5532-5539. https://doi.org/10.1128/JVI.76.11.5532-5539.2002
  31. Hiscott J. 2007. Triggering the innate antiviral response through IRF-3 activation. J. Biol. Chem. 282: 15325-15329. https://doi.org/10.1074/jbc.R700002200
  32. Honda K, Taniguchi T. 2006. IRFs: master regulators of signalling by Toll-like receptors and cytosolic patternrecognition receptors. Nat. Rev. Immunol. 6: 644-658. https://doi.org/10.1038/nri1900
  33. Yoneyama M, Suhara W, Fukuhara Y, Fukuda M, Nishida E, Fujita T. 1998. Direct triggering of the type I interferon system by virus infection: activation of a transcription factor complex containing IRF-3 and CBP/p300. EMBO J. 17: 1087-1095. https://doi.org/10.1093/emboj/17.4.1087
  34. Weaver BK, Kumar KP, Reich NC. 1998. Interferon regulatory factor 3 and CREB-binding protein/p300 are subunits of double-stranded RNA-activated transcription factor DRAF1. Mol. Cell. Biol. 18: 1359-1368. https://doi.org/10.1128/MCB.18.3.1359
  35. Au WC, Yeow WS, Pitha PM. 2 001. Analysis of functional domains of interferon regulatory factor 7 and its association with IRF-3. Virology 280: 273-282. https://doi.org/10.1006/viro.2000.0782
  36. Honda K, Yanai H, Negishi H, Asagiri M, Sato M, Mizutani T, et al. 2005. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434: 772-777. https://doi.org/10.1038/nature03464
  37. Hiscott J, Grandvaux N, Sharma S, Tenoever BR, Servant MJ, Lin R. 2003. Convergence of the NF-kappaB and interferon signaling pathways in the regulation of antiviral defense and apoptosis. Ann. NY Acad. Sci. 1010: 237-248. https://doi.org/10.1196/annals.1299.042
  38. Wang J, Basagoudanavar SH, Wang X, Hopewell E, Albrecht R, Garcia-Sastre A, et al. 2010. NF-kappa B RelA subunit is crucial for early IFN-beta expression and resistance to RNA virus replication. J. Immunol. 185: 1720-1729. https://doi.org/10.4049/jimmunol.1000114
  39. Yu C, Boon D, McDonald SL, Myers TG, Tomioka K, Nguyen H, et al. 2010. Pathogenesis of hepatitis E virus and hepatitis C virus in chimpanzees: similarities and differences. J. Virol. 84: 11264-11278. https://doi.org/10.1128/JVI.01205-10
  40. Hardy MP, Owczarek CM, Jermiin LS, Ejdeback M, Hertzog PJ. 2004. Characterization of the type I interferon locus and identification of novel genes. Genomics 84: 331-345. https://doi.org/10.1016/j.ygeno.2004.03.003
  41. Zitvogel L, Galluzzi L, Kepp O, Smyth MJ, Kroemer G. 2015. Type I interferons in anticancer immunity. Nat. Rev. Immunol. 15: 405-414. https://doi.org/10.1038/nri3845
  42. Xi Y, D ay S L, J ackson R J, R anasinghe C. 2012 . Role of novel type Iinterferon epsilon in viral infection and mucosal immunity. Mucosal Immunol. 5: 610-622. https://doi.org/10.1038/mi.2012.35
  43. Dunn GP, Bruce AT, Sheehan KC, Shankaran V, Uppaluri R, Bui JD, et al. 2005. A critical function for type I interferons in cancer immunoediting. Nat. Immunol. 6: 722-729. https://doi.org/10.1038/ni1213
  44. Vilcek J. 2003. Novel interferons. Nat. Immunol. 4: 8-9.
  45. Biron CA, Nguyen KB, Pien GC, Cousens LP, Salazar-Mather TP. 1999. Natural killer cells in antiviral defense: function and regulation by innate cytokines. Annu. Rev. Immunol. 17: 189-220. https://doi.org/10.1146/annurev.immunol.17.1.189
  46. Swann JB, Hayakawa Y, Zerafa N, Sheehan KC, Scott B, Schreiber RD, et al. 2007. Type I IFN contributes to NK cell homeostasis, activation, and antitumor function. J. Immunol. 178: 7540-7549. https://doi.org/10.4049/jimmunol.178.12.7540
  47. Asselin-Paturel C, Brizard G, Chemin K, Boonstra A, O'Garra A, Vicari A, et al. 2005. Type I interferon dependence of plasmacytoid dendritic cell activation and migration. J. Exp. Med. 201: 1157-1167. https://doi.org/10.1084/jem.20041930
  48. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA. 2001. Recognition of double-stranded RNA and activation of NFkappaB by Toll-like receptor 3. Nature 413: 732-738. https://doi.org/10.1038/35099560
  49. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, et al. 2011. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472: 481-485. https://doi.org/10.1038/nature09907
  50. Nan Y , Nan G, Z hang YJ. 2014. Interferon induction by RNA viruses and antagonism by viral pathogens. Viruses 6: 4999-5027. https://doi.org/10.3390/v6124999
  51. Noppert SJ, Fitzgerald KA, Hertzog PJ. 2007. The role of type I interferons in TLR responses. Immunol. Cell Biol. 85: 446-457. https://doi.org/10.1038/sj.icb.7100099
  52. Fujita T, Onoguchi K, Onomoto K, Hirai R, Yoneyama M. 2007. Triggering antiviral response by RIG-I-related RNA helicases. Biochimie 89: 754-760. https://doi.org/10.1016/j.biochi.2007.01.013
  53. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, et al. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNAinduced innate antiviral responses. Nat. Immunol. 5: 730-737. https://doi.org/10.1038/ni1087
  54. Nakhaei P, Genin P, Civas A, Hiscott J. 2009. RIG-I-like receptors: sensing and responding to RNA virus infection. Semin. Immunol. 21: 215-222. https://doi.org/10.1016/j.smim.2009.05.001
  55. Devhare PB, Chatterjee SN, Arankalle VA, Lole KS. 2013. Analysis of antiviral response in human epithelial cells infected with hepatitis E virus. PLoS One 8: e63793. https://doi.org/10.1371/journal.pone.0063793
  56. Nan Y, Ma Z, Wang R, Yu Y, Kannan H, Fredericksen B, et al. 2014. Enhancement of interferon induction by ORF3 product of hepatitis E virus. J. Virol. 88: 8696-8705. https://doi.org/10.1128/JVI.01228-14
  57. Gack MU, Shin YC, Joo CH, Urano T, Liang C, Sun L, et al. 2007. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446: 916-920. https://doi.org/10.1038/nature05732
  58. Oshiumi H, Miyashita M, Matsumoto M, Seya T. 2013. A distinct role of Riplet-mediated K63-linked polyubiquitination of the RIG-I repressor domain in human antiviral innate immune responses. PLoS Pathog. 9: e1003533. https://doi.org/10.1371/journal.ppat.1003533
  59. Xu L, Wang W, Li Y, Zhou X, Yin Y, Wang Y, et al. 2017. RIG-I is a key antiviral interferon-stimulated gene against hepatitis E virus regardless of interferon production. Hepatology 65: 1823-1839. https://doi.org/10.1002/hep.29105
  60. Shukla P, Nguyen HT, Torian U, Engle RE, Faulk K, Dalton HR, et al. 2011. Cross-species infections of cultured cells by hepatitis E virus and discovery of an infectious virus-host recombinant. Proc. Natl. Acad. Sci. USA 108: 2438-2443. https://doi.org/10.1073/pnas.1018878108
  61. Shukla P, Nguyen HT, Faulk K, Mather K, Torian U, Engle RE, et al. 2012. Adaptation of a genotype 3 hepatitis E virus to efficient growth in cell culture depends on an inserted human gene segment acquired by recombination. J. Virol. 86: 5697-5707. https://doi.org/10.1128/JVI.00146-12
  62. Kenney SP, Meng XJ. 2015. The lysine residues within the human ribosomal protein S17 sequence naturally inserted into the viral nonstructural protein of a unique strain of hepatitis E virus are important for enhanced virus replication. J. Virol. 89: 3793-3803. https://doi.org/10.1128/JVI.03582-14
  63. Nguyen HT, Torian U, Faulk K, Mather K, Engle RE, Thompson E, et al. 2012. A naturally occurring human/ hepatitis E recombinant virus predominates in serum but not in faeces of a chronic hepatitis E patient and has a growth advantage in cell culture. J. Gen. Virol. 93: 526-530. https://doi.org/10.1099/vir.0.037259-0
  64. Saito T, Owen DM, Jiang F, Marcotrigiano J, Gale M Jr. 2008. Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 454: 523-527. https://doi.org/10.1038/nature07106
  65. Zhu H, Dong H, Eksioglu E, Hemming A, Cao M, Crawford JM, et al. 2007. Hepatitis C virus triggers apoptosis of a newly developed hepatoma cell line through antiviral defense system. Gastroenterology 133: 1649-1659. https://doi.org/10.1053/j.gastro.2007.09.017
  66. Eksioglu EA, Zhu H, Bayouth L, Bess J, Liu HY, Nelson DR, et al. 2011. Characterization of HCV interactions with Toll-like receptors and RIG-I in liver cells. PLoS One 6: e21186. https://doi.org/10.1371/journal.pone.0021186
  67. Xu L, Zhou X, Wang W, Wang Y, Yin Y, Laan LJ, et al. 2016. IFN regulatory factor 1 restricts hepatitis E virus replication by activating STAT1 to induce antiviral IFNstimulated genes. FASEB J. 30: 3352-3367. https://doi.org/10.1096/fj.201600356R
  68. Ghasemi H, Ghazanfari T, Yaraee R, Faghihzadeh S, Hassan ZM. 2011. Roles of IL-8 in ocular inflammations: a review. Ocul. Immunol. Inflamm. 19: 401-412. https://doi.org/10.3109/09273948.2011.618902
  69. Rotondi M, Coperchini F, Chiovato L. 2013. CXCL8 in thyroid disease: from basic notions to potential applications in clinical practice. Cytokine Growth Factor Rev. 24: 539-546. https://doi.org/10.1016/j.cytogfr.2013.08.001
  70. Pichert A, Schlorke D, Franz S, Arnhold J. 2012. Functional aspects of the interaction between interleukin-8 and sulfated glycosaminoglycans. Biomatter 2: 142-148. https://doi.org/10.4161/biom.21316
  71. Zarogoulidis P, Katsikogianni F, Tsiouda T, Sakkas A, Katsikogiannis N, Zarogoulidis K. 2014. Interleukin-8 and interleukin-17 for cancer. Cancer Invest. 32: 197-205. https://doi.org/10.3109/07357907.2014.898156
  72. Li Z, Chen L, Liu Q. 2015. Activation of CXCL-8 transcription by hepatitis E virus ORF-1 via AP-1. Mediators Inflamm. 2015: 495370.
  73. Holtmann H, Winzen R, Holland P, Eickemeier S, Hoffmann E, Wallach D, et al. 1999. Induction of interleukin-8 synthesis integrates effects on transcription and mRNA degradation from at least three different cytokine- or stress-activated signal transduction pathways. Mol. Cell. Biol. 19: 6742-6753. https://doi.org/10.1128/MCB.19.10.6742
  74. Cucinotta M, Visalli M, Aguennouz M, Valenti A, Loddo S, Altucci L, et al. 2008. Regulation of interleukin-8 gene at a distinct site of its promoter by CCAAT enhancer-binding protein homologous protein in prostaglandin E2-treated human T cells. J. Biol. Chem. 283: 29760-29769. https://doi.org/10.1074/jbc.M803145200
  75. Nozell S, Laver T, Patel K, Benveniste EN. 2006. Mechanism of IFN-beta-mediated inhibition of IL-8 gene expression in astroglioma cells. J. Immunol. 177: 822-830. https://doi.org/10.4049/jimmunol.177.2.822
  76. Gusella GL, Musso T, Bosco MC, Espinoza-Delgado I, Matsushima K, Varesio L. 1993. IL-2 up-regulates but IFNgamma suppresses IL-8 expression in human monocytes. J. Immunol. 151: 2725-2732.
  77. Boost KA, Sadik CD, Bachmann M, Zwissler B, Pfeilschifter J, Muhl H. 2008. IFN-gamma impairs release of IL-8 by IL-1beta-stimulated A549 lung carcinoma cells. BMC Cancer 8: 265. https://doi.org/10.1186/1471-2407-8-265
  78. Chen WC, Tseng CK, Chen YH, Lin CK, Hsu SH, Wang SN, et al. 2015. HCV NS5A up-regulates COX-2 expression via IL-8-mediated activation of the ERK/JNK MAPK pathway. PLoS One 10: e0133264. https://doi.org/10.1371/journal.pone.0133264
  79. Collins AS, Ahmed S, Napoletano S, Schroeder M, Johnston JA, Hegarty JE, et al. 2014. H epatitis C virus (HCV)-induced suppressor of cytokine signaling (SOCS) 3 regulates proinflammatory TNF-alpha responses. J. Leukoc. Biol. 96: 255-263. https://doi.org/10.1189/jlb.2A1211-608RRRR
  80. Kang SM, Won SJ, Lee GH, Lim YS, Hwang SB. 2010. Modulation of interferon signaling by hepatitis C virus non-structural 5A protein: implication of genotypic difference in interferon treatment. FEBS Lett. 584: 4069-4076. https://doi.org/10.1016/j.febslet.2010.08.032
  81. Munir M, Zohari S, Belak S, Berg M. 2012. Doublestranded RNA-induced activation of activating protein-1 promoter is differentially regulated by the non-structural protein 1 of avian influenza A viruses. Viral Immunol. 25: 79-85. https://doi.org/10.1089/vim.2011.0059
  82. Devhare PB, Desai S, Lole KS. 2016. Innate immune responses in human hepatocyte-derived cell lines alter genotype 1 hepatitis E virus replication efficiencies. Sci. Rep. 6: 26827. https://doi.org/10.1038/srep26827
  83. Clark K, Plater L, Peggie M, Cohen P. 2009. Use of the pharmacological inhibitor BX795 to study the regulation and physiological roles of TBK1 and IkappaB kinase epsilon: a distinct upstream kinase mediates Ser-172 phosphorylation and activation. J. Biol. Chem. 284: 14136-14146. https://doi.org/10.1074/jbc.M109.000414
  84. Shimada T, Kawai T, Takeda K, Matsumoto M, Inoue J, Tatsumi Y, et al. 1999. IKK-i, a novel lipopolysaccharideinducible kinase that is related to IkappaB kinases. Int. Immunol. 11: 1357-1362. https://doi.org/10.1093/intimm/11.8.1357
  85. Hemmi H, Takeuchi O, Sato S, Yamamoto M, Kaisho T, Sanjo H, et al. 2004. The roles of two IkappaB kinase-related kinases in lipopolysaccharide and double stranded RNA signaling and viral infection. J. Exp. Med. 199: 1641-1650. https://doi.org/10.1084/jem.20040520
  86. Ortiz NE, Nijhawan RI, Weinberg JM. 2013. Acitretin. Dermatol. Ther. 26: 390-399. https://doi.org/10.1111/dth.12086
  87. Buccheri L, Katchen BR, Karter AJ, Cohen SR. 1997. Acitretin therapy is effective for psoriasis associated with human immunodeficiency virus infection. Arch. Dermatol. 133: 711-715. https://doi.org/10.1001/archderm.1997.03890420043005
  88. Li P, Kaiser P, Lampiris HW, Kim P, Yukl SA, Havlir DV, et al. 2016. Stimulating the RIG-I pathway to kill cells in the latent HIV reservoir following viral reactivation. Nat. Med. 22: 807-811. https://doi.org/10.1038/nm.4124
  89. Horner SM, Gale M Jr. 2013. Regulation of hepatic innate immunity by hepatitis C virus. Nat. Med. 19: 879-888. https://doi.org/10.1038/nm.3253
  90. Gale M Jr, Foy EM. 2005. Evasion of intracellular host defence by hepatitis C virus. Nature 436: 939-945. https://doi.org/10.1038/nature04078
  91. Zhou X, Xu L, Wang W, Watashi K, Wang Y, Sprengers D, et al. 2016. Disparity of basal and therapeutically activated interferon signalling in constraining hepatitis E virus infection. J. Viral Hepat. 23: 294-304. https://doi.org/10.1111/jvh.12491
  92. Dong C, Zafrullah M, Mixson-Hayden T, Dai X, Liang J, Meng J, et al. 2012. Suppression of interferon-alpha signaling by hepatitis E virus. Hepatology 55: 1324-1332. https://doi.org/10.1002/hep.25530
  93. Bode JG, Ludwig S, Ehrhardt C, Albrecht U, Erhardt A, Schaper F, et al. 2003. IFN-alpha antagonistic activity of HCV core protein involves induction of suppressor of cytokine signaling-3. FASEB J. 17: 488-490. https://doi.org/10.1096/fj.02-0664fje
  94. Shuai K, Liu B. 2003. Regulation of JAK-STAT signalling in the immune system. Nat. Rev. Immunol. 3: 900-911. https://doi.org/10.1038/nri1226
  95. Akhtar LN, Qin H, Muldowney MT, Yanagisawa LL, Kutsch O, Clements JE, et al. 2010. Suppressor of cytokine signaling 3 inhibits antiviral IFN-beta signaling to enhance HIV-1 replication in macrophages. J. Immunol. 185: 2393-2404. https://doi.org/10.4049/jimmunol.0903563
  96. Huang F, Yang C, Yu W, Bi Y, Long F, Wang J, et al. 2016. Hepatitis E virus infection activates signal regulator protein alpha to down-regulate type Iinterferon. Immunol. Res. 64: 115-122. https://doi.org/10.1007/s12026-015-8729-y
  97. Nan Y, Yu Y, Ma Z, Khattar SK, Fredericksen B, Zhang YJ. 2014. Hepatitis E virus inhibits type I interferon induction by ORF1 products. J. Virol. 88: 11924-11932. https://doi.org/10.1128/JVI.01935-14
  98. Karpe YA, Lole KS. 2011. Deubiquitination activity associated with hepatitis E virus putative papain-like cysteine protease. J. Gen. Virol. 92: 2088-2092. https://doi.org/10.1099/vir.0.033738-0
  99. Skaug B, Chen ZJ. 2010. Emerging role of ISG15 in antiviral immunity. Cell 143: 187-190. https://doi.org/10.1016/j.cell.2010.09.033
  100. Frias-Staheli N, Giannakopoulos NV, Kikkert M, Taylor SL, Bridgen A, Paragas J, et al. 2007. Ovarian tumor domaincontaining viral proteases evade ubiquitin- and ISG15-dependent innate immune responses. Cell Host Microbe 2: 404-416. https://doi.org/10.1016/j.chom.2007.09.014
  101. Sulea T, Lindner HA, Purisima EO, Menard R. 2005. Deubiquitination, a new function of the severe acute respiratory syndrome coronavirus papain-like protease? J. Virol. 79: 4550-4551. https://doi.org/10.1128/JVI.79.7.4550-4551.2005

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  2. Hepatitis E Virus Papain-Like Cysteine Protease Inhibits Type I Interferon Induction by Down-Regulating Melanoma Differentiation-Associated Gene 5 vol.28, pp.11, 2017, https://doi.org/10.4014/jmb.1809.09028
  3. Cell Type-Specific Interferon-γ-mediated Antagonism of KSHV Lytic Replication vol.9, pp.None, 2017, https://doi.org/10.1038/s41598-019-38870-7
  4. Metagenomic analysis of intestinal mucosa revealed a specific eukaryotic gut virome signature in early-diagnosed inflammatory bowel disease vol.10, pp.2, 2017, https://doi.org/10.1080/19490976.2018.1511664
  5. Zika Virus Proteins NS2A and NS4A Are Major Antagonists that Reduce IFN-β Promoter Activity Induced by the MDA5/RIG-I Signaling Pathway vol.29, pp.10, 2019, https://doi.org/10.4014/jmb.1909.09017
  6. Chikungunya Virus-Encoded nsP2, E2 and E1 Strongly Antagonize the Interferon-β Signaling Pathway vol.29, pp.11, 2017, https://doi.org/10.4014/jmb.1910.10014
  7. Methyltransferase of a cell culture-adapted hepatitis E inhibits the MDA5 receptor signaling pathway vol.57, pp.12, 2019, https://doi.org/10.1007/s12275-019-9478-8
  8. Identification of Hepatitis E Virus in Bovine and Porcine Raw Livers vol.29, pp.12, 2019, https://doi.org/10.4014/jmb.1910.10059
  9. Middle East Respiratory Syndrome Coronavirus-Encoded ORF8b Inhibits RIG-I-Like Receptors by a Differential Mechanism vol.29, pp.12, 2017, https://doi.org/10.4014/jmb.1911.11024
  10. Regulation of NF-Kappa B Signaling Pathway by Hepatitis Viruses vol.10, pp.3, 2017, https://doi.org/10.12677/hjbm.2020.103006
  11. Vertical transmission of hepatitis E virus in pregnant rhesus macaques vol.10, pp.1, 2020, https://doi.org/10.1038/s41598-020-74461-7