1887

Abstract

investigations have identified a variety of mechanisms by which herpesviruses evade interferon-stimulated antiviral effector mechanisms. However, these immune evasion mechanisms have not been evaluated during a bovine herpesvirus-1 (BHV-1) infection. This study investigated the transcription and secretion of type I and II interferons (IFNs) and the transcription of IFN-stimulated genes (ISGs) during a primary BHV-1 infection of the upper respiratory tract (URT) in naïve calves. IFN-α, -β and -γ transcription in nasal turbinates and protein levels in nasal secretions increased following infection. Increased IFN type I and II secretion was detected 3 days post-infection (p.i.) and IFN production increased in parallel with virus shedding. Expression of ISGs, including , and also increased significantly (<0.05) in nasal turbinates on day 3 p.i. and elevated ISG expression persisted throughout the period of viral shedding. In contrast, RNAase L gene expression was not induced during the BHV-1 infection in the nasal turbinates, but was induced on day 10 p.i. in the trachea. studies confirmed that recombinant bovine (rBo)IFN-α, -β and -γ induced expression of , and , but decreased transcript in bovine epithelial cells. Relative to vesicular stomatitisvirus (VSV), BHV-1 was resistant to the antiviral activity of rBoIFN-α and –γ, but treatment of epithelial cells with 10 ng rBoIFN-β ml effected an 80 % inhibition of BHV-1 replication and complete inhibition of VSV replication. These observations confirm that the transcription and translation of type I and II IFNs increase during BHV-1 infection, while the transcription of some ISGs is not inhibited.

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2017-07-01
2020-01-18
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References

  1. Chaplin PJ, Parsons KR, Collins RA. The cloning of cattle interferon-A subtypes isolated from the gut epithelium of rotavirus-infected calves. Immunogenetics 1996;44:143–145 [CrossRef][PubMed]
    [Google Scholar]
  2. Cerretti DP, Mckereghan K, Larsen A, Cosman D, Gillis S et al. Cloning, sequence, and expression of bovine interferon-gamma. J Immunol 1986;136:4561–4564[PubMed]
    [Google Scholar]
  3. Díaz-San Segundo F, Weiss M, Perez-Martín E, Koster MJ, Zhu J et al. Antiviral activity of bovine type III interferon against foot-and-mouth disease virus. Virology 2011;413:283–292 [CrossRef][PubMed]
    [Google Scholar]
  4. Fulton RW, Downing MM, Cummins JM. Antiviral effects of bovine interferons on bovine respiratory tract viruses. J Clin Microbiol 1984;19:492–497[PubMed]
    [Google Scholar]
  5. Schoggins JW, Rice CM. Interferon-stimulated genes and their antiviral effector functions. Curr Opin Virol 2011;1:519–525 [CrossRef][PubMed]
    [Google Scholar]
  6. Jones C. Alphaherpesvirus latency: its role in disease and survival of the virus in nature. Adv Virus Res 1998;51:81–133[PubMed][CrossRef]
    [Google Scholar]
  7. Reisinger L, Reimann H. Beitrag zur thiologie Des Bläschenausschlages Des Rindes. Wiener Tierärztl Wschr 1928;15:249–261
    [Google Scholar]
  8. Schroeder RJ, Moys MD. An acute upper respiratory infection of dairy cattle. J Am Vet Med Assoc 1954;125:471–472[PubMed]
    [Google Scholar]
  9. Schuh JC, Bielefeldt Ohmann H, Babiuk LA, Doige CE. Bovine herpesvirus-1-induced pharyngeal tonsil lesions in neonatal and weanling calves. J Comp Pathol 1992;106:243–253 [CrossRef][PubMed]
    [Google Scholar]
  10. Babiuk LA, Ohmann HB, Gifford G, Czarniecki CW, Scialli VT et al. Effect of bovine α1 interferon on bovine herpesvirus type 1-induced respiratory disease. J Gen Virol 1985;66:2383–2394 [CrossRef][PubMed]
    [Google Scholar]
  11. Hodgson PD, Aich P, Stookey J, Popowych Y, Potter A et al. Stress significantly increases mortality following a secondary bacterial respiratory infection. Vet Res 2012;43:21 [CrossRef][PubMed]
    [Google Scholar]
  12. Raggo C, Habermehl M, Babiuk LA, Griebel P. The in vivo effects of recombinant bovine herpesvirus-1 expressing bovine interferon-gamma. J Gen Virol 2000;81:2665–2673 [CrossRef][PubMed]
    [Google Scholar]
  13. Saira K, Zhou Y, Jones C. The infected cell protein 0 encoded by bovine herpesvirus 1 (bICP0) induces degradation of interferon response factor 3 and, consequently, inhibits beta interferon promoter activity. J Virol 2007;81:3077–3086 [CrossRef][PubMed]
    [Google Scholar]
  14. Henderson G, Zhang Y, Jones C. The bovine herpesvirus 1 gene encoding infected cell protein 0 (bICP0) can inhibit interferon-dependent transcription in the absence of other viral genes. J Gen Virol 2005;86:2697–2702 [CrossRef][PubMed]
    [Google Scholar]
  15. da Silva LF, Sinani D, Jones C. ICP27 protein encoded by bovine herpesvirus type 1 (bICP27) interferes with promoter activity of the bovine genes encoding beta interferon 1 (IFN-β1) and IFN-β3. Virus Res 2012;169:162–168 [CrossRef][PubMed]
    [Google Scholar]
  16. Paladino P, Mossman KL. Mechanisms employed by herpes simplex virus 1 to inhibit the interferon response. J Interferon Cytokine Res 2009;29:599–608 [CrossRef][PubMed]
    [Google Scholar]
  17. Ambagala AP, Cohen JI. Varicella-Zoster virus IE63, a major viral latency protein, is required to inhibit the alpha interferon-induced antiviral response. J Virol 2007;81:7844–7851 [CrossRef][PubMed]
    [Google Scholar]
  18. Zenner HL, Mauricio R, Banting G, Crump CM. Herpes simplex virus 1 counteracts tetherin restriction via its virion host shutoff activity. J Virol 2013;87:13115–13123 [CrossRef][PubMed]
    [Google Scholar]
  19. Kim MS, Min KS, Imakawa K. Regulation of Interferon-stimulated gene (ISG)12, ISG15, and MX1 and MX2 by conceptus interferons (IFNTs) in bovine uterine epithelial cells. Asian-Australas J Anim Sci 2013;26:795–803 [CrossRef][PubMed]
    [Google Scholar]
  20. Gupta KC, Kingsbury DW. Conserved polyadenylation signals in two negative-strand RNA virus families. Virology 1982;120:518–523 [CrossRef][PubMed]
    [Google Scholar]
  21. Ankel H, Westra DF, Welling-Wester S, Lebon P. Induction of interferon-alpha by glycoprotein D of herpes simplex virus: a possible role of chemokine receptors. Virology 1998;251:317–326 [CrossRef][PubMed]
    [Google Scholar]
  22. Abril C, Engels M, Liman A, Hilbe M, Albini S et al. Both viral and host factors contribute to neurovirulence of bovine herpesviruses 1 and 5 in interferon receptor-deficient mice. J Virol 2004;78:3644–3653 [CrossRef][PubMed]
    [Google Scholar]
  23. Hayden FG, Fritz R, Lobo MC, Alvord W, Strober W et al. Local and systemic cytokine responses during experimental human influenza A virus infection. Relation to symptom formation and host defense. J Clin Invest 1998;101:643–649 [CrossRef][PubMed]
    [Google Scholar]
  24. Bielefeldt Ohmann H, Campos M, Harland R, Griebel PJ, Babiuk LA. 2',5' Oligoadenylate synthetase activity in bovine peripheral blood mononuclear cells following bovine herpesvirus type-1-induced respiratory disease: a prognostic indicator?. J Interferon Res 1989;9:159–166 [CrossRef][PubMed]
    [Google Scholar]
  25. Perino LJ, Short EC, Burge LJ, Winter DA, Fulton RW. Interferon and 2',5'-oligo(A) synthetase activities in serum and blood mononuclear leukocytes of cattle after injection of bovine interferon-alpha 1. Am J Vet Res 1990;51:886–892[PubMed]
    [Google Scholar]
  26. Liu SY, Sanchez DJ, Aliyari R, Lu S, Cheng G. Systematic identification of type I and type II interferon-induced antiviral factors. Proc Natl Acad Sci USA 2012;109:4239–4244 [CrossRef][PubMed]
    [Google Scholar]
  27. Marié I, Durbin JE, Levy DE. Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7. EMBO J 1998;17:6660–6669 [CrossRef][PubMed]
    [Google Scholar]
  28. Ku CC, Che XB, Reichelt M, Rajamani J, Schaap-Nutt A et al. Herpes simplex virus-1 induces expression of a novel MxA isoform that enhances viral replication. Immunol Cell Biol 2011;89:173182 [CrossRef][PubMed]
    [Google Scholar]
  29. Floyd-Smith G, Slattery E, Lengyel P. Interferon action: RNA cleavage pattern of a (2'-5')oligoadenylate-dependent endonuclease. Science 1981;212:1030–1032 [CrossRef]
    [Google Scholar]
  30. Mori S, Jewett A, Cavalcanti M, Murakami-Mori K, Nakamura S et al. Differential regulation of human NK cell-associated gene expression following activation by IL-2, IFN-alpha and PMA/ionomycin. Int J Oncol 1998;12:1165–1170 [CrossRef][PubMed]
    [Google Scholar]
  31. Pak-Wittel MA, Yang L, Sojka DK, Rivenbark JG, Yokoyama WM. Interferon-γ mediates chemokine-dependent recruitment of natural killer cells during viral infection. Proc Natl Acad Sci USA 2013;110:E50E59 [CrossRef][PubMed]
    [Google Scholar]
  32. Campos M, Griebel P, Bielefeldt Ohmann H, Babiuk LA. Cell-mediated cytotoxic responses in lungs following a primary bovine herpes virus type 1 infection. Immunology 1992;75:47–52[PubMed]
    [Google Scholar]
  33. Braun RBL, van Drunen Littel-van den Hurk S. Compatibility of plasmids expressing different antigens in a single DNA vaccine formulation. J Gen Virol 1998;79:2965–2970 [CrossRef][PubMed]
    [Google Scholar]
  34. Kaushik RS, Begg AA, Wilson HL, Aich P, Abrahamsen MS et al. Establishment of fetal bovine intestinal epithelial cell cultures susceptible to bovine rotavirus infection. J Virol Methods 2008;148:182–196 [CrossRef][PubMed]
    [Google Scholar]
  35. Capon DJ, Shepard HM, Goeddel DV. Two distinct families of human and bovine interferon-alpha genes are coordinately expressed and encode functional polypeptides. Mol Cell Biol 1985;5:768–779 [CrossRef][PubMed]
    [Google Scholar]
  36. Babiuk LA, Rouse BT. Immune interferon production by lymphoid cells: role in the inhibition of herpesviruses. Infect Immun 1976;13:1567–1578[PubMed]
    [Google Scholar]
  37. Manoj S, Griebel PJ, Babiuk LA, van Drunen Littel-van den Hurk S. Modulation of immune responses to bovine herpesvirus-1 in cattle by immunization with a DNA vaccine encoding glycoprotein D as a fusion protein with bovine CD154. Immunology 2004;112:328–338 [CrossRef][PubMed]
    [Google Scholar]
  38. Mirabzadeh-Ardakani A, Solie J, Gonzalez-Cano P, Schmutz SM, Griebel PJ. Tissue- and age-dependent expression of the bovine DEFB103 gene and protein. Cell Tissue Res 2016;363:479–490 [CrossRef][PubMed]
    [Google Scholar]
  39. González-Cano P, Arsic N, Popowych YI, Griebel PJ. Two functionally distinct myeloid dendritic cell subpopulations are present in bovine blood. Dev Comp Immunol 2014;44:378–388 [CrossRef][PubMed]
    [Google Scholar]
  40. Malmuthuge N, Li M, Fries P, Griebel PJ, Guan LL. Regional and age dependent changes in gene expression of Toll-like receptors and key antimicrobial defence molecules throughout the gastrointestinal tract of dairy calves. Vet Immunol Immunopathol 2012;146:18–26 [CrossRef][PubMed]
    [Google Scholar]
  41. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T method. Methods 2001;25:402–408 [CrossRef][PubMed]
    [Google Scholar]
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