Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Hepatitis E Virus Methyltransferase Inhibits Type I Interferon Induction by Targeting RIG-I

  • Kang, Sangmin (Korea Zoonosis Research Institute and Genetic Engineering Research Institute, Chonbuk National University) ;
  • Choi, Changsun (Department of Food and Nutrition, Chung-Ang University) ;
  • Choi, Insoo (Department of Infectious Disease, College of Veterinary Medicine, Konkuk University) ;
  • Han, Kwi-Nam (Biological Disaster Analysis Group, Korea Basic Science Research Institute) ;
  • Roh, Seong Woon (World Institute of Kimchi) ;
  • Choi, Jongsun (Biological Disaster Analysis Group, Korea Basic Science Research Institute) ;
  • Kwon, Joseph (Biological Disaster Analysis Group, Korea Basic Science Research Institute) ;
  • Park, Mi-Kyung (Food and Bio-industry Research Institute, Kyungpook National University) ;
  • Kim, Seong-Jun (Center for Convergent Research of Emerging Virus Infection, Korea Research Institute of Chemical Technology) ;
  • Myoung, Jinjong (Korea Zoonosis Research Institute and Genetic Engineering Research Institute, Chonbuk National University)
  • Received : 2018.08.29
  • Accepted : 2018.09.03
  • Published : 2018.09.28
Download PDF
⟨ Previous Next ⟩

Abstract

The type I interferons (IFNs) play a vital role in activation of innate immunity in response to viral infection. Accordingly, viruses have evolved to employ various survival strategies to evade innate immune responses induced by type I IFNs. For example, hepatitis E virus (HEV) encoded papain-like cysteine protease (PCP) has been shown to inhibit IFN activation signaling by suppressing K63-linked de-ubiquitination of retinoic acid-inducible gene I (RIG-I) and TANK-binding kinase 1 (TBK1), thus effectively inhibiting down-stream activation of IFN signaling. In the present study, we demonstrated that HEV inhibits polyinosinic-polycytidylic acid (poly(I:C))-induced $IFN-{\beta}$ transcriptional induction. Moreover, by using reporter assay with individual HEV-encoded gene, we showed that HEV methyltransferase (MeT), a non-structural protein, significantly decreases RIG-I-induced $IFN-{\beta}$ induction and $NF-{\kappa}B$ signaling activities in a dose-dependent manner. Taken together, we report here that MeT, along with PCP, is responsible for the inhibition of RIG-I-induced activation of type I IFNs, expanding the list of HEV-encoded antagonists of the host innate immunity.

Keywords

References

  1. Aggarwal R, Naik S. 2009. Epidemiology of hepatitis E: current status. J. Gastroenterol. Hepatol. 24: 1484-1493. https://doi.org/10.1111/j.1440-1746.2009.05933.x
  2. Arankalle VA, Chobe LP, Chadha MS. 2006. Type-IV Indian swine HEV infects rhesus monkeys. J. Viral Hepat. 13: 742-745. https://doi.org/10.1111/j.1365-2893.2006.00759.x
  3. Teshale EH, Hu DJ, Holmberg SD. 2010. The two faces of hepatitis E virus. Clin. Infect. Dis. 51: 328-334. https://doi.org/10.1086/653943
  4. Naik SR, Aggarwal R, Salunke PN, Mehrotra NN. 1992. A large waterborne viral hepatitis E epidemic in Kanpur, India. Bull. World Health Organ. 70: 597-604.
  5. Ricci A, Allende A, Bolton D, Chemaly M, Davies R, Escamez PSF, et al. 2017. Public health risks associated with hepatitis E virus (HEV) as a food-borne pathogen. EFSA J. 15.
  6. Jilani N, Das BC, Husain SA, Baweja UK, Chattopadhya D, Gupta RK, et al. 2007. Hepatitis E virus infection and fulminant hepatic failure during pregnancy. J. Gastroenterol. Hepatol. 22: 676-682. https://doi.org/10.1111/j.1440-1746.2007.04913.x
  7. Navaneethan U, Al Mohajer M, Shata MT. 2008. Hepatitis E and pregnancy: understanding the pathogenesis. Liver Int. 28: 1190-1199. https://doi.org/10.1111/j.1478-3231.2008.01840.x
  8. 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
  9. 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
  10. 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
  11. Koonin EV, Gorbalenya AE, Purdy MA, Rozanov MN, Reyes GR, Bradley DW. 1992. Computer-assisted assignment of functional domains in the nonstructural polyprotein of hepatitis E virus: delineation of an additional group of positive-strand RNA plant and animal viruses. Proc. Natl. Acad. Sci. USA 89: 8259-8263. https://doi.org/10.1073/pnas.89.17.8259
  12. 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
  13. Ropp SL, Tam AW, Beames B, Purdy M, Frey TK. 2000. Expression of the hepatitis E virus ORF1. Arch. Virol. 145: 1321-1337. https://doi.org/10.1007/s007050070093
  14. 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
  15. 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
  16. 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
  17. 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
  18. 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
  19. Yamada K, Takahashi M, Hoshino Y, Takahashi H, Ichiyama K, Nagashima S, et al. 2009. ORF3 protein 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
  20. 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
  21. 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
  22. 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
  23. Theofilopoulos AN, Baccala R, Beutler B, Kono DH. 2005. Type I interferons (alpha/beta) in immunity and autoimmunity. Annu. Rev. Immunol. 23: 307-336. https://doi.org/10.1146/annurev.immunol.23.021704.115843
  24. Xi Y, Day SL, Jackson RJ, Ranasinghe C. 2012. Role of novel type I interferon epsilon in viral infection and mucosal immunity. Mucosal. Immunol. 5: 610-622. https://doi.org/10.1038/mi.2012.35
  25. 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
  26. Kang S, Myoung J. 2017. Primary lymphocyte infection models for KSHV and its putative tumorigenesis mechanisms in B cell lymphomas. J. Microbiol. 55: 319-329. https://doi.org/10.1007/s12275-017-7075-2
  27. Yarilina A, Ivashkiv LB. 2010. Type I interferon: a new player in TNF signaling. Curr. Dir. Autoimmun. 11: 94-104.
  28. 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
  29. Medzhitov R. 2007. Recognition of microorganisms and activation of the immune response. Nature 449: 819-826. https://doi.org/10.1038/nature06246
  30. 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
  31. 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
  32. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, Bartenschlager R, et al. 2005. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437: 1167-1172. https://doi.org/10.1038/nature04193
  33. 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
  34. Hardy MP, Mc GAF, 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
  35. 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
  36. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, Golenbock DT, et al. 2003. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4: 491-496.
  37. Chau TL, Gioia R, Gatot JS, Patrascu F, Carpentier I, Chapelle JP, et al. 2008. Are the IKKs and IKK-related kinases TBK1 and IKK-epsilon similarly activated? Trends Biochem. Sci. 33: 171-180. https://doi.org/10.1016/j.tibs.2008.01.002
  38. Hacker H, Karin M. 2006. Regulation and function of IKK and IKK-related kinases. Sci. STKE 2006: re13.
  39. 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
  40. Clement JF, Meloche S, Servant MJ. 2008. The IKK-related kinases: from innate immunity to oncogenesis. Cell Res. 18: 889-899. https://doi.org/10.1038/cr.2008.273
  41. 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
  42. Honda K, Taniguchi T. 2006. IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat. Rev. Immunol. 6: 644-658. https://doi.org/10.1038/nri1900
  43. Liu S, Cai X, Wu J, Cong Q, Chen X, Li T, et al. 2015. Phosphorylation of innate immune adaptor proteins MAVS, STING, and TRIF induces IRF3 activation. Science 347: aaa2630. https://doi.org/10.1126/science.aaa2630
  44. 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
  45. 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
  46. 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
  47. Song JW, Guan M, Zhao ZW, Zhang JJ. 2015. Type I interferons function as autocrine and paracrine factors to induce autotaxin in response to TLR activation. PLoS One 10.
  48. Hu J, Lou DH, Carow B, Winerdal ME, Rottenberg M, Wikstrom AC, et al. 2012. LPS Regulates SOCS2 transcription in a type I interferon dependent autocrine-paracrine loop. PLoS One 7.
  49. Draenert R, Frater J, Prado JG. 2012. Virus immune evasion: new mechanism and implications in disease outcome. Adv. Virol. 2012: 490549.
  50. Senba M, Mori N. 2012. Mechanisms of virus immune evasion lead to development from chronic inflammation to cancer formation associated with human papillomavirus infection. Oncol. Rev. 6: e17. https://doi.org/10.4081/oncol.2012.e17
  51. Wi J, Jeong MS, Hong HJ. 2017. Construction and Characterization of an anti-hepatitis B virus preS1 humanized antibody that binds to the essential receptor binding site. J. Microbiol. Biotechnol. 27: 1336-1344. https://doi.org/10.4014/jmb.1703.03066
  52. 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
  53. Lin W, Kim SS, Yeung E, Kamegaya Y, Blackard JT, Kim KA, et al. 2006. Hepatitis C virus core protein blocks interferon signaling by interaction with the STAT1 SH2 domain. J. Virol. 80: 9226-9235. https://doi.org/10.1128/JVI.00459-06
  54. Taylor DR, Shi ST, Romano PR, Barber GN, Lai MM. 1999. Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein. Science 285: 107-110. https://doi.org/10.1126/science.285.5424.107
  55. Li K, Foy E, Ferreon JC, Nakamura M, Ferreon AC, Ikeda M, et al. 2005. 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 102: 2992-2997. https://doi.org/10.1073/pnas.0408824102
  56. Li XD, Sun L, Seth RB, Pineda G, Chen ZJ. 2005. Hepatitis C virus protease NS3/4A cleaves mitochondrial antiviral signaling protein off the mitochondria to evade innate immunity. Proc. Natl. Acad. Sci. USA 102: 17717-17722. https://doi.org/10.1073/pnas.0508531102
  57. 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
  58. Lan KH, Lan KL, Lee WP, Sheu ML, Chen MY, Lee YL, et al. 2007. HCV NS5A inhibits interferon-alpha signaling through suppression of STAT1 phosphorylation in hepatocyte-derived cell lines. J. Hepatol. 46: 759-767.
  59. Kang S, Myoung J. 2017. Host innate immunity against hepatitis E virus and viral evasion mechanisms. J. Microbiol. Biotechnol. 27: 1727-1735. https://doi.org/10.4014/jmb.1708.08045
  60. 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
  61. Krain LJ, Nelson KE, Labrique AB. 2014. Host immune status and response to hepatitis E virus infection. Clin. Microbiol. Rev. 27: 139-165. https://doi.org/10.1128/CMR.00062-13
  62. 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
  63. 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
  64. 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
  65. Hamid FB, Kim J, Shin CG. 2017. Characterization of prototype foamy virus infectivity in transportin 3 knockdown human 293t cell line. J. Microbiol. Biotechnol. 27: 380-387. https://doi.org/10.4014/jmb.1606.06011
  66. Myoung J, Ganem D. 2011. Infection of lymphoblastoid cell lines by Kaposi's sarcoma-associated herpesvirus: critical role of cell-associated virus. J. Virol. 85: 9767-9777. https://doi.org/10.1128/JVI.05136-11
  67. Myoung J, Ganem D. 2011. Generation of a doxycycline-inducible KSHV producer cell line of endothelial origin: maintenance of tight latency with efficient reactivation upon induction. J. Virol. Methods. 174: 12-21. https://doi.org/10.1016/j.jviromet.2011.03.012
  68. Myoung J, Ganem D. 2011. Infection of primary human tonsillar lymphoid cells by KSHV reveals frequent but abortive infection of T cells. Virology 413: 1-11. https://doi.org/10.1016/j.virol.2010.12.036
  69. Myoung J, Ganem D. 2011. Active lytic infection of human primary tonsillar B cells by KSHV and its noncytolytic control by activated CD4+ T cells. J. Clin. Invest. 121: 1130-1140. https://doi.org/10.1172/JCI43755
  70. Johne R, Trojnar E, Filter M, Hofmann J. 2016. Thermal stability of hepatitis E virus as estimated by a cell culture method. Appl. Environ. Microbiol. 82: 4225-4231. https://doi.org/10.1128/AEM.00951-16
  71. Kang HS, Myoung J, So EY, Bahk YY, Kim BS. 2016. Transgenic expression of non-structural genes of Theiler's virus suppresses initial viral replication and pathogenesis of demyelination. J. Neuroinflammation 13: 133. https://doi.org/10.1186/s12974-016-0597-4
  72. Ha S, Choi IS, Choi C, Myoung J. 2016. Infection models of human norovirus: challenges and recent progress. Arch. Virol. 161: 779-788. https://doi.org/10.1007/s00705-016-2748-4
  73. Cho M, Myoung J. 2015. OX40 and 4-1BB downregulate Kaposi's sarcoma-associated herpesvirus replication in lymphatic endothelial cells, but 4-1BB and not OX40 inhibits viral replication in B-cells. J. Gen. Virol. 96: 3635-3645. https://doi.org/10.1099/jgv.0.000312
  74. Lee JM, Kim J, Ryu I, Woo HM, Lee TG, Jung W, et al. 2017. An aptamer-based electrochemical sensor that can distinguish influenza virus subtype H1 from H5. J. Microbiol. Biotechnol. 27: 2037-2043. https://doi.org/10.4014/jmb.1708.08015
  75. Lee JM, Cho JB, Ahn HC, Jung W, Jeong YJ. 2017. A novel chemical compound for inhibition of SARS coronavirus helicase. J. Microbiol. Biotechnol. 27: 2070-2073. https://doi.org/10.4014/jmb.1707.07073
  76. Choi S, Park H, Minelko M, Kim EK, Cho MR, Nam JH. 2017. Recombinant adeno-associated virus expressing truncated IK cytokine diminishes the symptoms of inflammatory arthritis. J. Microbiol. Biotechnol. 27: 1892-1895. https://doi.org/10.4014/jmb.1705.05018
  77. Yoo JE, Lee C, Park S, Ko G. 2017. Evaluation of various real-time reverse transcription quantitative PCR assays for norovirus detection. J. Microbiol. Biotechnol. 27: 816-824. https://doi.org/10.4014/jmb.1612.12026
  78. Shin JS, Ku KB, Jang Y, Yoon YS, Shin D, Kwon OS, et al. 2017. Comparison of anti-influenza virus activity and pharmacokinetics of oseltamivir free base and oseltamivir phosphate. J. Microbiol. 55: 979-983. https://doi.org/10.1007/s12275-017-7371-x
  79. Jeong H, Seong BL. 2017. Exploiting virus-like particles as innovative vaccines against emerging viral infections. J. Microbiol. 55: 220-230. https://doi.org/10.1007/s12275-017-7058-3
  80. Kim JH, Lee CH, Lee SW. 2016. Hepatitis C virus infection stimulates transforming growth factor-beta1 expression through up-regulating miR-192. J. Microbiol. 54: 520-526. https://doi.org/10.1007/s12275-016-6240-3
  81. Elkholy YS, Hegab AS, Ismail DK, Hassan RM. 2016. Evaluation of a novel commercial quaternary ammonium compound for eradication of Mycobacteria, HCV and HBV in Egypt. J. Microbiol. 54: 39-43. https://doi.org/10.1007/s12275-016-5530-0
  82. Kim MJ, Lee SY, Kim HJ, Lee JS, Joo IS, Kwak HS, et al. 2016. Development of a one-step duplex RT-PCR method for the simultaneous detection of VP3/VP1 and VP1/P2B regions of the hepatitis A virus. J. Microbiol. Biotechnol. 26: 1398-1403. https://doi.org/10.4014/jmb.1604.04047
  83. Ahn HS, Han SH, Kim YH, Park BJ, Kim DH, Lee JB, et al. 2017. Adverse fetal outcomes in pregnant rabbits experimentally infected with rabbit hepatitis E virus. Virology 512: 187-193. https://doi.org/10.1016/j.virol.2017.09.020
  84. Lee M, Seo DJ, Seo J, Oh H, Jeon SB, Ha SD, et al. 2015. Detection of viable murine norovirus using the plaque assay and propidium-monoazide-combined real-time reverse transcription-polymerase chain reaction. J. Virol. Methods 221: 57-61. https://doi.org/10.1016/j.jviromet.2015.04.018
  85. Gillen J, Li W, Liang Q, Avey D, Wu J, Wu F, et al. 2015. A survey of the interactome of Kaposi's sarcoma-associated herpesvirus ORF45 revealed its binding to viral ORF33 and cellular USP7, resulting in stabilization of ORF33 that is required for production of progeny viruses. J. Virol. 89: 4918-4931. https://doi.org/10.1128/JVI.02925-14
  86. Fu B, Kuang E, Li W, Avey D, Li X, Turpin Z, et al. 2015. Activation of p90 ribosomal S6 kinases by ORF45 of Kaposi's sarcoma-associated herpesvirus is critical for optimal production of infectious viruses. J. Virol. 89: 195-207. https://doi.org/10.1128/JVI.01937-14
  87. Lim S, Cha S, Jang JH, Yang D, Choe J, Seo T. 2016. Alterations in acetylation of histone H4 lysine 8 and trimethylation of lysine 20 associated with lytic gene promoters during Kaposi's sarcoma-associated herpesvirus reactivation. J. Microbiol. Biotechnol.
  88. Schemmerer M, Apelt S, Trojnar E, Ulrich RG, Wenzel JJ, Johne R. 2016. Enhanced replication of hepatitis E virus strain 47832c in an A549-derived subclonal cell line. Viruses 8.
  89. 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
  90. Malmgaard L. 2004. Induction and regulation of IFNs during viral infections. J. Interferon. Cytokine Res. 24: 439-454. https://doi.org/10.1089/1079990041689665
  91. Loo YM, Fornek J, Crochet N, Bajwa G, Perwitasari O, Martinez-Sobrido L, et al. 2008. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J. Virol. 82: 335-345. https://doi.org/10.1128/JVI.01080-07
  92. Takeuchi O, Akira S. 2010. Pattern recognition receptors and inflammation. Cell 140: 805-820. https://doi.org/10.1016/j.cell.2010.01.022

Cited by

  1. The Amino-Terminal Region of Hepatitis E Virus ORF1 Containing a Methyltransferase (Met) and a Papain-Like Cysteine Protease (PCP) Domain Counteracts Type I Interferon Response vol.10, pp.12, 2018, https://doi.org/10.3390/v10120726
  2. Cell culture systems for the study of hepatitis E virus vol.163, pp.None, 2018, https://doi.org/10.1016/j.antiviral.2019.01.007
  3. Immunocontraceptive Effects in Male Rats Vaccinated with Gonadotropin-Releasing Hormone-I and -II Protein Complex vol.29, pp.4, 2019, https://doi.org/10.4014/jmb.1901.01067
  4. 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
  5. Chikungunya Virus-Encoded nsP2, E2 and E1 Strongly Antagonize the Interferon-β Signaling Pathway vol.29, pp.11, 2018, https://doi.org/10.4014/jmb.1910.10014
  6. 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
  7. Identification of Hepatitis E Virus in Bovine and Porcine Raw Livers vol.29, pp.12, 2019, https://doi.org/10.4014/jmb.1910.10059
  8. Middle East Respiratory Syndrome Coronavirus-Encoded ORF8b Inhibits RIG-I-Like Receptors by a Differential Mechanism vol.29, pp.12, 2018, https://doi.org/10.4014/jmb.1911.11024
  9. Chikungunya Virus nsP2 Impairs MDA5/RIG-I-Mediated Induction of NF-κB Promoter Activation: A Potential Target for Virus-Specific Therapeutics vol.30, pp.12, 2020, https://doi.org/10.4014/jmb.2012.12005
  10. Interplay between Hepatitis E Virus and Host Cell Pattern Recognition Receptors vol.22, pp.17, 2018, https://doi.org/10.3390/ijms22179259
  11. Hepatitis E virus‐encoded microRNA promotes viral replication by inhibiting type I interferon vol.36, pp.1, 2022, https://doi.org/10.1096/fj.202101042r