1887

Abstract

Borna disease virus (BDV) is a neurotropic, negative-stranded RNA virus causing persistent infection and progressive neurological disorders in a wide range of warm-blooded animals. The role of the small non-structural X protein in viral pathogenesis is not completely understood. Here we investigated whether the X protein of BDV and avian bornavirus (ABV) interferes with the type I interferon (IFN) system, similar to other non-structural proteins of negative-stranded RNA viruses. In luciferase reporter assays, we found that the X protein of various bornaviruses interfered with the type I IFN system at all checkpoints investigated, in contrast to previously reported findings, resulting in reduced type I IFN secretion.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.047175-0
2013-02-01
2020-07-07
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/2/263.html?itemId=/content/journal/jgv/10.1099/vir.0.047175-0&mimeType=html&fmt=ahah

References

  1. Andrejeva J., Childs K. S., Young D. F., Carlos T. S., Stock N., Goodbourn S., Randall R. E. 2004; The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-β promoter. Proc Natl Acad Sci U S A 101:17264–17269 [CrossRef][PubMed]
    [Google Scholar]
  2. Basler C. F., Amarasinghe G. K. 2009; Evasion of interferon responses by Ebola and Marburg viruses. J Interferon Cytokine Res 29:511–520 [CrossRef][PubMed]
    [Google Scholar]
  3. Baum A., García-Sastre A. 2010; Induction of type I interferon by RNA viruses: cellular receptors and their substrates. Amino Acids 38:1283–1299 [CrossRef][PubMed]
    [Google Scholar]
  4. Baum A., García-Sastre A. 2011; Differential recognition of viral RNA by RIG-I. Virulence 2:166–169 [CrossRef][PubMed]
    [Google Scholar]
  5. Berg M., Ehrenborg C., Blomberg J., Pipkorn R., Berg A. L. 1998; Two domains of the Borna disease virus p40 protein are required for interaction with the p23 protein. J Gen Virol 79:2957–2963[PubMed]
    [Google Scholar]
  6. Briese T., de la Torre J. C., Lewis A., Ludwig H., Lipkin W. I. 1992; Borna disease virus, a negative-strand RNA virus, transcribes in the nucleus of infected cells. Proc Natl Acad Sci U S A 89:11486–11489 [CrossRef][PubMed]
    [Google Scholar]
  7. Chawla-Sarkar M., Lindner D. J., Liu Y. F., Williams B. R., Sen G. C., Silverman R. H., Borden E. C. 2003; Apoptosis and interferons: role of interferon-stimulated genes as mediators of apoptosis. Apoptosis 8:237–249 [CrossRef][PubMed]
    [Google Scholar]
  8. Childs K., Stock N., Ross C., Andrejeva J., Hilton L., Skinner M., Randall R., Goodbourn S. 2007; mda-5, but not RIG-I, is a common target for paramyxovirus V proteins. Virology 359:190–200 [CrossRef][PubMed]
    [Google Scholar]
  9. Cubitt B., Oldstone C., Valcarcel J., de la Torre J. C. 1994; RNA splicing contributes to the generation of mature mRNAs of Borna disease virus, a non-segmented negative strand RNA virus. Virus Res 34:69–79 [CrossRef][PubMed]
    [Google Scholar]
  10. Ehrhardt C., Kardinal C., Wurzer W. J., Wolff T., von Eichel-Streiber C., Pleschka S., Planz O., Ludwig S. 2004; Rac1 and PAK1 are upstream of IKK-epsilon and TBK-1 in the viral activation of interferon regulatory factor-3. FEBS Lett 567:230–238 [CrossRef][PubMed]
    [Google Scholar]
  11. Fernandez-Sesma A. 2007; The influenza virus NS1 protein: inhibitor of innate and adaptive immunity. Infect Disord Drug Targets 7:336–343 [CrossRef][PubMed]
    [Google Scholar]
  12. García-Sastre A., Biron C. A. 2006; Type 1 interferons and the virus–host relationship: a lesson in détente. Science 312:879–882 [CrossRef][PubMed]
    [Google Scholar]
  13. Gitlin L., Benoit L., Song C., Cella M., Gilfillan S., Holtzman M. J., Colonna M. 2010; Melanoma differentiation-associated gene 5 (MDA5) is involved in the innate immune response to Paramyxoviridae infection in vivo. PLoS Pathog 6:e1000734 [CrossRef][PubMed]
    [Google Scholar]
  14. Goodbourn S., Randall R. E. 2009; The regulation of type I interferon production by paramyxoviruses. J Interferon Cytokine Res 29:539–548 [CrossRef][PubMed]
    [Google Scholar]
  15. Habjan M., Andersson I., Klingström J., Schümann M., Martin A., Zimmermann P., Wagner V., Pichlmair A., Schneider U.other authors 2008; Processing of genome 5′ termini as a strategy of negative-strand RNA viruses to avoid RIG-I-dependent interferon induction. PLoS ONE 3:e2032 [CrossRef][PubMed]
    [Google Scholar]
  16. Hallensleben W., Staeheli P. 1999; Inhibition of Borna disease virus multiplication by interferon: cell line differences in susceptibility. Arch Virol 144:1209–1216 [CrossRef][PubMed]
    [Google Scholar]
  17. Haller O., Kochs G., Weber F. 2006; The interferon response circuit: induction and suppression by pathogenic viruses. Virology 344:119–130 [CrossRef][PubMed]
    [Google Scholar]
  18. Honkavuori K. S., Shivaprasad H. L., Williams B. L., Quan P. L., Hornig M., Street C., Palacios G., Hutchison S. K., Franca M.other authors 2008; Novel Borna virus in psittacine birds with proventricular dilatation disease. Emerg Infect Dis 14:1883–1886 [CrossRef][PubMed]
    [Google Scholar]
  19. Johansson M., Berg M., Berg A. L. 2002; Humoral immune response against Borna disease virus (BDV) in experimentally and naturally infected cats. Vet Immunol Immunopathol 90:23–33 [CrossRef][PubMed]
    [Google Scholar]
  20. Kistler A. L., Gancz A., Clubb S., Skewes-Cox P., Fischer K., Sorber K., Chiu C. Y., Lublin A., Mechani S.other authors 2008; Recovery of divergent avian bornaviruses from cases of proventricular dilatation disease: identification of a candidate etiologic agent. Virol J 5:88 [CrossRef][PubMed]
    [Google Scholar]
  21. Koonin E. V., Senkevich T. G., Dolja V. V. 2006; The ancient Virus World and evolution of cells. Biol Direct 1:29 [CrossRef][PubMed]
    [Google Scholar]
  22. Lipkin W. I., Briese T. 2006; Bornaviridae. In Fields Virology, 5th edn. vol. II pp. 1829–1851 Edited by Knipe D., Howley P., Griffin D. E., Lamb R. A., Martin M., Roizman B., Straus S. Philadelphia, PA: Lippincott Williams & Wilkins;
    [Google Scholar]
  23. Ludwig H., Bode L. 2000; Borna disease virus: new aspects on infection, disease, diagnosis and epidemiology. Rev Sci Tech 19:259–288[PubMed]
    [Google Scholar]
  24. Munir M. 2010; TRIM proteins: another class of viral victims. Sci Signal 3:jc2 [CrossRef][PubMed]
    [Google Scholar]
  25. Munir M., Zohari S., Metreveli G., Baule C., Belák S., Berg M. 2011; Alleles A and B of non-structural protein 1 of avian influenza A viruses differentially inhibit beta interferon production in human and mink lung cells. J Gen Virol 92:2111–2121 [CrossRef][PubMed]
    [Google Scholar]
  26. Nowotny N., Kolodziejek J., Jehle C. O., Suchy A., Staeheli P., Schwemmle M. 2000; Isolation and characterization of a new subtype of Borna disease virus. J Virol 74:5655–5658 [CrossRef][PubMed]
    [Google Scholar]
  27. Poenisch M., Burger N., Staeheli P., Bauer G., Schneider U. 2009; Protein X of Borna disease virus inhibits apoptosis and promotes viral persistence in the central nervous systems of newborn-infected rats. J Virol 83:4297–4307 [CrossRef][PubMed]
    [Google Scholar]
  28. Pringle C. R. 2005; Mononegavirales. In Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses pp. 609–614 Edited by Fauquet C. M., Mayo M. A., Maniloff J., Desselberger U., Ball L. A. London: Elsevier Academic Press;
    [Google Scholar]
  29. Reuter A., Ackermann A., Kothlow S., Rinder M., Kaspers B., Staeheli P. 2010; Avian bornaviruses escape recognition by the innate immune system. Viruses 2:927–938 [CrossRef][PubMed]
    [Google Scholar]
  30. Sato M., Suemori H., Hata N., Asagiri M., Ogasawara K., Nakao K., Nakaya T., Katsuki M., Noguchi S.other authors 2000; Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-α/β gene induction. Immunity 13:539–548 [CrossRef][PubMed]
    [Google Scholar]
  31. Schneider P. A., Schneemann A., Lipkin W. I. 1994; RNA splicing in Borna disease virus, a nonsegmented, negative-strand RNA virus. J Virol 68:5007–5012[PubMed]
    [Google Scholar]
  32. Schneider U., Schwemmle M., Staeheli P. 2005; Genome trimming: a unique strategy for replication control employed by Borna disease virus. Proc Natl Acad Sci U S A 102:3441–3446 [CrossRef][PubMed]
    [Google Scholar]
  33. Schwardt M., Mayer D., Frank R., Schneider U., Eickmann M., Planz O., Wolff T., Schwemmle M. 2005; The negative regulator of Borna disease virus polymerase is a non-structural protein. J Gen Virol 86:3163–3169 [CrossRef][PubMed]
    [Google Scholar]
  34. Sen G. C. 2001; Viruses and interferons. Annu Rev Microbiol 55:255–281 [CrossRef][PubMed]
    [Google Scholar]
  35. Stark G. R., Kerr I. M., Williams B. R., Silverman R. H., Schreiber R. D. 1998; How cells respond to interferons. Annu Rev Biochem 67:227–264 [CrossRef][PubMed]
    [Google Scholar]
  36. Unterstab G., Ludwig S., Anton A., Planz O., Dauber B., Krappmann D., Heins G., Ehrhardt C., Wolff T. 2005; Viral targeting of the interferon-β-inducing Traf family member-associated NF-κB activator (TANK)-binding kinase-1. Proc Natl Acad Sci U S A 102:13640–13645 [CrossRef][PubMed]
    [Google Scholar]
  37. Wehner T., Ruppert A., Herden C., Frese K., Becht H., Richt J. A. 1997; Detection of a novel Borna disease virus-encoded 10 kDa protein in infected cells and tissues. J Gen Virol 78:2459–2466[PubMed]
    [Google Scholar]
  38. Wensman J. J., Berg M., Berg A. L. 2008; Experiences of Borna disease virus infection in Sweden. APMIS Suppl 116:46–49 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.047175-0
Loading
/content/journal/jgv/10.1099/vir.0.047175-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error