1887

Abstract

Previous research revealed the induction of chicken () in the lungs of chickens infected with highly pathogenic avian influenza viruses (HPAIVs). This activity was correlated with the degree of pathogenicity of the viruses to chickens. As mammalian ubiquitin-specific protease (USP18) is known to remove type I interferon (IFN I)-inducible ubiquitin-like molecules from conjugated proteins and block IFN I signalling, we explored the function of the chicken homologue of USP18 during avian influenza virus infection. With this aim, we cloned from cultured chicken cells and revealed that the putative ORF comprises 1137 bp. Comparative analysis of the predicted aa sequence of chUSP18 with those of human and mouse USP18 revealed relatively high sequence similarity among the sequences, including domains specific for the ubiquitin-specific processing protease family. Furthermore, we found that chUSP18 expression was induced by chicken IFN I, as observed for mammalian USP18. Experiments based on over-expression and depletion demonstrated that chUSP18 significantly enhanced the replication of a low-pathogenic avian influenza virus (LPAIV), but not an HPAIV. Our findings suggest that chUSP18, being similar to mammalian USP18, acts as a pro-viral factor during LPAIV replication .

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2017-09-01
2019-12-11
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References

  1. Sadler AJ, Williams BR. Interferon-inducible antiviral effectors. Nat Rev Immunol 2008;8:559–568 [CrossRef][PubMed]
    [Google Scholar]
  2. Liu AL, Li YF, Qi W, Ma XL, Yu KX et al. Comparative analysis of selected innate immune-related genes following infection of immortal DF-1 cells with highly pathogenic (H5N1) and low pathogenic (H9N2) avian influenza viruses. Virus Genes 2015;50:189–199 [CrossRef][PubMed]
    [Google Scholar]
  3. Watanabe C, Uchida Y, Ito H, Ito T, Saito T. Host immune-related gene responses against highly pathogenic avian influenza virus infection in vitro differ among chicken cell lines established from different organs. Vet Immunol Immunopathol 2011;144:187–199 [CrossRef][PubMed]
    [Google Scholar]
  4. Jiang H, Yang H, Kapczynski DR. Chicken interferon alpha pretreatment reduces virus replication of pandemic H1N1 and H5N9 avian influenza viruses in lung cell cultures from different avian species. Virol J 2011;8:447 [CrossRef][PubMed]
    [Google Scholar]
  5. Ngunjiri JM, Mohni KN, Sekellick MJ, Schultz-Cherry S, Webster RG et al. Lethal H5N1 influenza viruses are not resistant to interferon action in human, simian, porcine or chicken cells. Nat Med 2012;18:1456–1457 [CrossRef][PubMed]
    [Google Scholar]
  6. Uchida Y, Watanabe C, Takemae N, Hayashi T, Oka T et al. Identification of host genes linked with the survivability of chickens infected with recombinant viruses possessing H5N1 surface antigens from a highly pathogenic avian influenza virus. J Virol 2012;86:2686–2695 [CrossRef][PubMed]
    [Google Scholar]
  7. Chen L, Li S, Mcgilvray I. The ISG15/USP18 ubiquitin-like pathway (ISGylation system) in hepatitis C virus infection and resistance to interferon therapy. Int J Biochem Cell Biol 2011;43:1427–1431 [CrossRef][PubMed]
    [Google Scholar]
  8. Nakashima H, Nguyen T, Goins WF, Chiocca EA. Interferon-stimulated gene 15 (ISG15) and ISG15-linked proteins can associate with members of the selective autophagic process, histone deacetylase 6 (HDAC6) and SQSTM1/p62. J Biol Chem 2015;290:1485–1495 [CrossRef][PubMed]
    [Google Scholar]
  9. Malakhov MP, Malakhova OA, Kim KI, Ritchie KJ, Zhang DE. UBP43 (USP18) specifically removes ISG15 from conjugated proteins. J Biol Chem 2002;277:9976–9981 [CrossRef][PubMed]
    [Google Scholar]
  10. Zhao C, Hsiang TY, Kuo RL, Krug RM. ISG15 conjugation system targets the viral NS1 protein in influenza A virus-infected cells. Proc Natl Acad Sci USA 2010;107:2253–2258 [CrossRef][PubMed]
    [Google Scholar]
  11. Hsiang TY, Zhao C, Krug RM. Interferon-induced ISG15 conjugation inhibits influenza A virus gene expression and replication in human cells. J Virol 2009;83:5971–5977 [CrossRef][PubMed]
    [Google Scholar]
  12. Lenschow DJ, Lai C, Frias-Staheli N, Giannakopoulos NV, Lutz A et al. IFN-stimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses. Proc Natl Acad Sci USA 2007;104:1371–1376 [CrossRef][PubMed]
    [Google Scholar]
  13. Ketscher L, Hannß R, Morales DJ, Basters A, Guerra S et al. Selective inactivation of USP18 isopeptidase activity in vivo enhances ISG15 conjugation and viral resistance. Proc Natl Acad Sci USA 2015;112:1577–1582 [CrossRef][PubMed]
    [Google Scholar]
  14. Malakhova OA, Kim KI, Luo JK, Zou W, Kumar KG et al. UBP43 is a novel regulator of interferon signaling independent of its ISG15 isopeptidase activity. Embo J 2006;25:2358–2367 [CrossRef][PubMed]
    [Google Scholar]
  15. Aaronson DS, Horvath CM. A road map for those who don't know JAK-STAT. Science 2002;296:1653–1655 [CrossRef][PubMed]
    [Google Scholar]
  16. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. How cells respond to interferons. Annu Rev Biochem 1998;67:227–264 [CrossRef][PubMed]
    [Google Scholar]
  17. Schumacher B, Bernasconi D, Schultz U, Staeheli P. The chicken Mx promoter contains an ISRE motif and confers interferon inducibility to a reporter gene in chick and monkey cells. Virology 1994;203:144–148 [CrossRef][PubMed]
    [Google Scholar]
  18. Liu LQ, Ilaria R, Kingsley PD, Iwama A, van Etten RA et al. A novel ubiquitin-specific protease, UBP43, cloned from leukemia fusion protein AML1-ETO-expressing mice, functions in hematopoietic cell differentiation. Mol Cell Biol 1999;19:3029–3038 [CrossRef][PubMed]
    [Google Scholar]
  19. Magor KE, Miranzo Navarro D, Barber MR, Petkau K, Fleming-Canepa X et al. Defense genes missing from the flight division. Dev Comp Immunol 2013;41:377–388 [CrossRef][PubMed]
    [Google Scholar]
  20. Cormican P, Lloyd AT, Downing T, Connell SJ, Bradley D et al. The avian toll-Like receptor pathway-subtle differences amidst general conformity. Dev Comp Immunol 2009;33:967–973 [CrossRef][PubMed]
    [Google Scholar]
  21. Huang B, Qi ZT, Xu Z, Nie P. Global characterization of interferon regulatory factor (IRF) genes in vertebrates: glimpse of the diversification in evolution. BMC Immunol 2010;11:22 [CrossRef][PubMed]
    [Google Scholar]
  22. Brownlie R, Zhu J, Allan B, Mutwiri GK, Babiuk LA et al. Chicken TLR21 acts as a functional homologue to mammalian TLR9 in the recognition of CpG oligodeoxynucleotides. Mol Immunol 2009;46:3163–3170 [CrossRef][PubMed]
    [Google Scholar]
  23. Hayashi T, Watanabe C, Suzuki Y, Tanikawa T, Uchida Y et al. Chicken MDA5 senses short double-stranded RNA with implications for antiviral response against avian influenza viruses in chicken. J Innate Immun 2014;6:58–71 [CrossRef][PubMed]
    [Google Scholar]
  24. Zhang X, Bogunovic D, Payelle-Brogard B, Francois-Newton V, Speer SD et al. Human intracellular ISG15 prevents interferon-α/β over-amplification and auto-inflammation. Nature 2015;517:89–93 [CrossRef][PubMed]
    [Google Scholar]
  25. Zhao C, Sridharan H, Chen R, Baker DP, Wang S et al. Influenza B virus non-structural protein 1 counteracts ISG15 antiviral activity by sequestering ISGylated viral proteins. Nat Commun 2016;7:12754 [CrossRef][PubMed]
    [Google Scholar]
  26. Honke N, Shaabani N, Cadeddu G, Sorg UR, Zhang DE et al. Enforced viral replication activates adaptive immunity and is essential for the control of a cytopathic virus. Nat Immunol 2011;13:51–57 [CrossRef][PubMed]
    [Google Scholar]
  27. Reed LJ, Muench H. A simple method of estimating fifty per cent endpoints12. Am J Epidemiol 1938;27:493–497 [CrossRef]
    [Google Scholar]
  28. Kawakami E, Watanabe T, Fujii K, Goto H, Watanabe S et al. Strand-specific real-time RT-PCR for distinguishing influenza vRNA, cRNA, and mRNA. J Virol Methods 2011;173:1–6 [CrossRef][PubMed]
    [Google Scholar]
  29. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT Method. Methods 2001;25:402–408 [CrossRef][PubMed]
    [Google Scholar]
  30. Larkin MA, Blackshields G, Brown NP, Chenna R, Mcgettigan PA et al. CLUSTAL W and CLUSTAL X version 2.0. Bioinformatics 2007;23:2947–2948 [CrossRef][PubMed]
    [Google Scholar]
  31. Nicholas KB, Nicholas Jr HB. GeneDoc: a tool for editing and annotating multiple sequence alignments. , Pittsburgh Supercomputing Center’s National Resource for Biomedical Supercomputing, ver. 2.7. 000. 1997
  32. Burkart C, Fan JB, Zhang DE. Two independent mechanisms promote expression of an N-terminal truncated USP18 isoform with higher DeISGylation activity in the nucleus. J Biol Chem 2012;287:4883–4893 [CrossRef][PubMed]
    [Google Scholar]
  33. Li YP, Handberg KJ, Juul-Madsen HR, Zhang MF, Jørgensen PH. Transcriptional profiles of chicken embryo cell cultures following infection with infectious bursal disease virus. Arch Virol 2007;152:463–478 [CrossRef][PubMed]
    [Google Scholar]
  34. Brahmakshatriya VR, Lupiani B, Reddy SM. Characterization and evaluation of avian influenza NS1 mutant virus as a potential live and killed DIVA (differentiating between infected and vaccinated animals) vaccine for chickens. Vaccine 2010;28:2388–2396 [CrossRef][PubMed]
    [Google Scholar]
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