1887

Abstract

Chicken anaemia virus (CAV) is a lymphotropic virus that causes anaemia and immunosuppression in chickens. Previously, we proposed that CAV evades host antiviral responses by disrupting T-cell signalling, but the precise cellular targets and modes of action remain elusive. In this study, we examined gene expression in Marek’s disease virus-transformed chicken T-cell line MSB-1 after infection with CAV using both a custom 5K immune-focused microarray and quantitative real-time PCR at 24, 48 and 72 h post-infection. The data demonstrate an intricate equilibrium between CAV and the host gene expression, displaying subtle but significant modulation of transcripts involved in the T-cell, inflammation and NF-κB signalling cascades. CAV efficiently blocked the induction of type-I interferons and interferon-stimulated genes at 72 h. The cell expression pattern implies that CAV subverts host antiviral responses and that the transformed environment of MSB-1 cells offers an opportunistic advantage for virus growth.

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2018-03-01
2024-12-04
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References

  1. Todd D, McNulty MS. Circoviridae. In Pattison M, McMullin PF, Bradbury JM, Alexander DJ. (editors) Poultry Diseases Philadelphia, USA: Elsevier Health Sciences; 2008 pp. 398–404 [Crossref]
    [Google Scholar]
  2. Villiers E, Hausen HZ, Schat KA, Virus CA. Chicken anemia virus. In de Villiers EM, zur Hausen H. (editors) TT Viruses - Current Topics in Microbiology and Immunology Berlin Heidelberg: Springer; 2009 pp. 151–183
    [Google Scholar]
  3. Bullenkamp J, Cole D, Malik F, Alkhatabi H, Kulasekararaj A et al. Human gyrovirus apoptin shows a similar subcellular distribution pattern and apoptosis induction as the chicken anaemia virus derived VP3/Apoptin. Cell Death Dis 2012; 3:e296 [View Article][PubMed]
    [Google Scholar]
  4. Adair BM. Immunopathogenesis of chicken anemia virus infection. Dev Comp Immunol 2000; 24:247–255 [View Article][PubMed]
    [Google Scholar]
  5. Jeurissen SH, Wagenaar F, Pol JM, van der Eb AJ, Noteborn MH. Chicken anemia virus causes apoptosis of thymocytes after in vivo infection and of cell lines after in vitro infection. J Virol 1992; 66:7383–7388[PubMed]
    [Google Scholar]
  6. Giotis ES, Rothwell L, Scott A, Hu T, Talbot R et al. Transcriptomic profiling of virus-host cell interactions following chicken anaemia virus (CAV) infection in an in vivo model. PLoS One 2015; 10:e0134866 [View Article][PubMed]
    [Google Scholar]
  7. Todd D. Circoviruses: immunosuppressive threats to avian species: a review. Avian Pathol 2000; 29:373–394 [View Article][PubMed]
    [Google Scholar]
  8. Coombes AL, Crawford GR. Chicken anaemia virus: a short review. Worlds Poult Sci J 1996; 52:267–277 [View Article]
    [Google Scholar]
  9. McNulty MS. Chicken anaemia virus—a glimpse of the future?. Br Poult Sci 1997; 38:7–13 [View Article]
    [Google Scholar]
  10. Noteborn MH, Koch G. Chicken anaemia virus infection: molecular basis of pathogenicity. Avian Pathol 1995; 24:11–31 [View Article][PubMed]
    [Google Scholar]
  11. Zanella A, Dall'ara P, Lavazza A, Marchi R, Martin MA et al. Interaction between Marek's disease and chicken infectious anaemia viruses. Curr Prog Marek's Dis Res 200111–19
    [Google Scholar]
  12. Haridy M, Goryo M, Sasaki J, Okada K. Pathological and immunohistochemical study of chickens with co-infection of Marek's disease virus and chicken anaemia virus. Avian Pathol 2009; 38:469–483 [View Article][PubMed]
    [Google Scholar]
  13. Crowley TM, Haring VR, Moore R. Chicken anemia virus: an understanding of the in-vitro host response over time. Viral Immunol 2011; 24:3–9 [View Article][PubMed]
    [Google Scholar]
  14. Smith J, Speed D, Hocking PM, Talbot RT, Degen WG et al. Development of a chicken 5 K microarray targeted towards immune function. BMC Genomics 2006; 7:49 [View Article][PubMed]
    [Google Scholar]
  15. Yuasa N. Propagation and infectivity titration of the Gifu-1 strain of chicken anemia agent in a cell-Line (MDCC-MSB1) derived from Mareks-disease lymphoma. Natl Inst Anim Health Q 1983; 23:13–20
    [Google Scholar]
  16. Yuasa N, Taniguchi T, Goda M, Shibatani M, Imada T et al. Isolation of chicken anemia agent with MDCC-MSB1 cells from chickens in the field. Natl Inst Anim Health Q 1983; 23:75–77[PubMed]
    [Google Scholar]
  17. Vonbulow V, Fuchs B, Bertram M. Investigations on chicken infectious anemia agent (CAA) in vitro - propagation, titration, serum neutralization tests, and indirect immunofluorescence assays. J Vet Med B Infect Dis Vet Public Health 1985; 32:679–693
    [Google Scholar]
  18. Kikkawa U, Matsuzaki H, Yamamoto T. Protein kinase C delta (PKC delta): activation mechanisms and functions. J Biochem 2002; 132:831–839 [View Article][PubMed]
    [Google Scholar]
  19. Hiscott J, Kwon H, Génin P. Hostile takeovers: viral appropriation of the NF-κB pathway. J Clin Invest 2001; 107:143–151 [View Article][PubMed]
    [Google Scholar]
  20. Rhiza HJ, Bauer B. Persistence of viral DNA in Marek’s disease virus-transformed lymphoblastoid cell lines. In Wittmann G, Gaskell RM, Rhiza HJ. (editors) Latent Herpesvirus Infections in Veterinary Medicine Boston, MA: Martinus Nijhoff; 1984 pp. 481–488
    [Google Scholar]
  21. Xie Q, Anderson AS, Morgan RW. Marek's disease virus (MDV) ICP4, pp38, and meq genes are involved in the maintenance of transformation of MDCC-MSB1 MDV-transformed lymphoblastoid cells. J Virol 1996; 70:1125–1131[PubMed]
    [Google Scholar]
  22. Parnas O, Corcoran DL, Cullen BR. Analysis of the mRNA targetome of microRNAs expressed by Marek's disease virus. MBio 2014; 5:e01060-13 [View Article][PubMed]
    [Google Scholar]
  23. Kumar S, Kunec D, Buza JJ, Chiang HI, Zhou H et al. Nuclear Factor kappa B is central to Marek's disease herpesvirus induced neoplastic transformation of CD30 expressing lymphocytes in-vivo . BMC Syst Biol 2012; 6:123 [View Article][PubMed]
    [Google Scholar]
  24. Didelot C, Schmitt E, Brunet M, Maingret L, Parcellier A et al. Heat shock proteins: endogenous modulators of apoptotic cell death. Handb Exp Pharmacol 2006; 172:171–198[PubMed] [Crossref]
    [Google Scholar]
  25. Rohn JL, Zhang YH, Aalbers RI, Otto N, den Hertog J et al. A tumor-specific kinase activity regulates the viral death protein Apoptin. J Biol Chem 2002; 277:50820–50827 [View Article][PubMed]
    [Google Scholar]
  26. Shen Y, Shenk TE. Viruses and apoptosis. Curr Opin Genet Dev 1995; 5:105–111 [View Article][PubMed]
    [Google Scholar]
  27. Jeurissen SH, Wagenaar F, Pol JM, van der Eb AJ, Noteborn MH. Chicken anemia virus causes apoptosis of thymocytes after in vivo infection and of cell lines after in vitro infection. J Virol 1992; 66:7383–7388[PubMed]
    [Google Scholar]
  28. Kaffashi A, Pagel CN, Noormohammadi AH, Browning GF. Evidence of apoptosis induced by viral protein 2 of chicken anaemia virus. Arch Virol 2015; 160:2557–2563 [View Article][PubMed]
    [Google Scholar]
  29. Myers MD, Dragone LL, Weiss A. Src-like adaptor protein down-regulates T cell receptor (TCR)-CD3 expression by targeting TCRzeta for degradation. J Cell Biol 2005; 170:285–294 [View Article][PubMed]
    [Google Scholar]
  30. Giotis ES, Robey RC, Skinner NG, Tomlinson CD, Goodbourn S et al. Chicken interferome: avian interferon-stimulated genes identified by microarray and RNA-seq of primary chick embryo fibroblasts treated with a chicken type I interferon (IFN-α). Vet Res 2016; 47:75 [View Article][PubMed]
    [Google Scholar]
  31. Röll S, Härtle S, Lütteke T, Kaspers B, Härtle S. Tissue and time specific expression pattern of interferon regulated genes in the chicken. BMC Genomics 2017; 18:264 [View Article][PubMed]
    [Google Scholar]
  32. Giotis ES, Ross CS, Robey RC, Nohturfft A, Goodbourn S et al. Constitutively elevated levels of SOCS1 suppress innate responses in DF-1 immortalised chicken fibroblast cells. Sci Rep 2017; 7:17485 [View Article][PubMed]
    [Google Scholar]
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