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Abstract

Infectious bursal disease virus (IBDV) causes an economically significant disease of chickens worldwide. The emergence of very virulent IBDV (vvIBDV) has brought more challenges for effective prevention of this disease. The molecular basis for the virulence of vvIBDV is not fully understood. In this study, 20 IBDV strains were analysed phylogenically and clustered in three branches based on their full-length B segments. The amino acid triplet located at positions 145/146/147 of VP1 was found highly conserved in branch I non-vvIBDVs as asparagine/glutamic acid/glycine (NEG), in branch II vvIBDVs as threonine/glutamic acid/glycine (TEG) and in branch III vvIBDVs as threonine/aspartic acid/asparagine (TDN). Further studies showed that the three amino acids play a critical role in the replication and pathogenicity of vvIBDV. Substitution of the TDN triplet with TEG or NEG reduced viral replication and pathogenicity of the vvIBDV HuB-1 strain in chickens. However, the replication of the attenuated IBDV Gt strain was reduced in chicken embryo fibroblast cells, whilst it was enhanced in the bursa by substituting NEG with TEG or TDN. The exchange of the three amino acids was also found to be capable of affecting the polymerase activity of VP1. The important role of segment B in the pathogenicity of IBDV was confirmed in this study. These results also provided new insights into the mechanism of the virulence of vvIBDVs and may offer new targets for their attenuation to develop potential vaccines using reverse genetics.

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2014-04-01
2024-04-23
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References

  1. Birghan C., Mundt E., Gorbalenya A. E. 2000; A non-canonical Lon proteinase lacking the ATPase domain employs the Ser-Lys catalytic dyad to exercise broad control over the life cycle of a double-stranded RNA virus. EMBO J 19:114–123 [View Article][PubMed]
    [Google Scholar]
  2. Boot H. J., ter Huurne A. A., Hoekman A. J., Peeters B. P., Gielkens A. L. 2000; Rescue of very virulent and mosaic infectious bursal disease virus from cloned cDNA: VP2 is not the sole determinant of the very virulent phenotype. J Virol 74:6701–6711 [View Article][PubMed]
    [Google Scholar]
  3. Boot H. J., Hoekman A. J. W., Gielkens A. L. J. 2005; The enhanced virulence of very virulent infectious bursal disease virus is partly determined by its B-segment. Arch Virol 150:137–144 [View Article][PubMed]
    [Google Scholar]
  4. Brandt M., Yao K., Liu M., Heckert R. A., Vakharia V. N. 2001; Molecular determinants of virulence, cell tropism, and pathogenic phenotype of infectious bursal disease virus. J Virol 75:11974–11982 [View Article][PubMed]
    [Google Scholar]
  5. Brown M. D., Green P., Skinner M. A. 1994; VP2 sequences of recent European ‘very virulent’ isolates of infectious bursal disease virus are closely related to each other but are distinct from those of ‘classical’ strains. J Gen Virol 75:675–680 [View Article][PubMed]
    [Google Scholar]
  6. Chettle N., Stuart J. C., Wyeth P. J. 1989; Outbreak of virulent infectious bursal disease in East Anglia. Vet Rec 125:271–272 [View Article][PubMed]
    [Google Scholar]
  7. Delmas B., Kibenge F. S. B., Leong J. C., Mundt E., Vakharia V. N., Wu J. L. 2004; Birnaviridae. In Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses pp. 561–569 Edited by Fauquet C. M., Mayo M. A., Maniloff J., Desselberger U., Ball L. A. London: Academic Press;
    [Google Scholar]
  8. Escaffre O., Le Nouën C., Amelot M., Ambroggio X., Ogden K. M., Guionie O., Toquin D., Müller H., Islam M. R., Eterradossi N. 2013; Both genome segments contribute to the pathogenicity of very virulent infectious bursal disease virus. J Virol 87:2767–2780 [View Article][PubMed]
    [Google Scholar]
  9. Eterradossi N., Saif Y. M. 2008; Infectious bursal disease. In Disease of Poultry, 12th edn. pp. 185–208. Edited by Saif Y. M., Fadly A. M., Glisson J. R., McDougald L. R., Nolan L. K., Swayne D. E. Ames, IA: Blackwell;
    [Google Scholar]
  10. Garriga D., Navarro A., Querol-Audí J., Abaitua F., Rodríguez J. F., Verdaguer N. 2007; Activation mechanism of a noncanonical RNA-dependent RNA polymerase. Proc Natl Acad Sci U S A 104:20540–20545 [View Article][PubMed]
    [Google Scholar]
  11. He C. Q., Ma L. Y., Wang D., Li G. R., Ding N. Z. 2009; Homologous recombination is apparent in infectious bursal disease virus. Virology 384:51–58 [View Article][PubMed]
    [Google Scholar]
  12. Ingrao F., Rauw F., Lambrecht B., van den Berg T. 2013; Infectious Bursal Disease: a complex host–pathogen interaction. Dev Comp Immunol 41:429–438 [View Article][PubMed]
    [Google Scholar]
  13. Islam M. R., Zierenberg K., Müller H. 2001; The genome segment B encoding the RNA-dependent RNA polymerase protein VP1 of very virulent infectious bursal disease virus (IBDV) is phylogenetically distinct from that of all other IBDV strains. Arch Virol 146:2481–2492 [View Article][PubMed]
    [Google Scholar]
  14. Jackwood D. J., Crossley B. M., Stoute S. T., Sommer-Wagner S., Woolcock P. R., Charlton B. R. 2012; Diversity of genome segment B from infectious bursal disease viruses in the United States. Avian Dis 56:165–172 [View Article][PubMed]
    [Google Scholar]
  15. Le Nouën C. L., Toquin D., Müller H., Raue R., Kean K. M., Langlois P., Cherbonnel M., Eterradossi N. 2012; Different domains of the RNA polymerase of infectious bursal disease virus contribute to virulence. PLoS ONE 7:e28064 [View Article][PubMed]
    [Google Scholar]
  16. Liu M., Vakharia V. N. 2004; VP1 protein of infectious bursal disease virus modulates the virulence in vivo. Virology 330:62–73 [View Article][PubMed]
    [Google Scholar]
  17. Lombardo E., Maraver A., Espinosa I., Fernández-Arias A., Rodriguez J. F. 2000; VP5, the nonstructural polypeptide of infectious bursal disease virus, accumulates within the host plasma membrane and induces cell lysis. Virology 277:345–357 [View Article][PubMed]
    [Google Scholar]
  18. Lucio B., Hitchner B. 1980; Immunosuppression and active response induced by infectious bursal disease virus in chickens with passive antibodies. Avian Dis 24:189–196 [View Article]
    [Google Scholar]
  19. Müller H., Islam M. R., Raue R. 2003; Research on infectious bursal disease – the past, the present and the future. Vet Microbiol 97:153–165 [View Article][PubMed]
    [Google Scholar]
  20. Mundt E. 1999; Tissue culture infectivity of different strains of infectious bursal disease virus is determined by distinct amino acids in VP2. J Gen Virol 80:2067–2076[PubMed]
    [Google Scholar]
  21. Niwa H., Yamamura K., Miyazaki J. 1991; Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193–199 [View Article][PubMed]
    [Google Scholar]
  22. Pan J., Vakharia V. N., Tao Y. J. 2007; The structure of a birnavirus polymerase reveals a distinct active site topology. Proc Natl Acad Sci U S A 104:7385–7390 [View Article][PubMed]
    [Google Scholar]
  23. Pan J., Lin L., Tao Y. J. 2009; Self-guanylylation of birnavirus VP1 does not require an intact polymerase activity site. Virology 395:87–96 [View Article][PubMed]
    [Google Scholar]
  24. Qi X., Gao Y., Gao H., Deng X., Bu Z., Wang X., Fu C., Wang X. 2007; An improved method for infectious bursal disease virus rescue using RNA polymerase II system. J Virol Methods 142:81–88 [View Article][PubMed]
    [Google Scholar]
  25. Schröder A., van Loon A. A., Goovaerts D., Mundt E. 2000; Chimeras in noncoding regions between serotypes I and II of segment A of infectious bursal disease virus are viable and show pathogenic phenotype in chickens. J Gen Virol 81:533–540[PubMed]
    [Google Scholar]
  26. Shi L., Li H., Ma G., Zhou J., Hong L., Zheng X., Wu Y., Wang Y., Yan Y. 2009; Competitive replication of different genotypes of infectious bursal disease virus on chicken embryo fibroblasts. Virus Genes 39:46–52 [View Article][PubMed]
    [Google Scholar]
  27. Stricker R. L., Behrens S. E., Mundt E. 2010; Nuclear factor NF45 interacts with viral proteins of infectious bursal disease virus and inhibits viral replication. J Virol 84:10592–10605 [View Article][PubMed]
    [Google Scholar]
  28. Tacken M. G., Peeters B. P., Thomas A. A., Rottier P. J., Boot H. J. 2002; Infectious bursal disease virus capsid protein VP3 interacts both with VP1, the RNA-dependent RNA polymerase, and with viral double-stranded RNA. J Virol 76:11301–11311 [View Article][PubMed]
    [Google Scholar]
  29. Tamura K., Dudley J., Nei M., Kumar S. 2007; MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599 [View Article][PubMed]
    [Google Scholar]
  30. van den Berg T. P. 2000; Acute infectious bursal disease in poultry: a review. Avian Pathol 29:175–194 [View Article][PubMed]
    [Google Scholar]
  31. van den Berg T. P., Gonze M., Meulemans G. 1991; Acute infectious bursal disease in poultry: isolation and characterisation of a highly virulent strain. Avian Pathol 20:133–143 [View Article][PubMed]
    [Google Scholar]
  32. van Loon A. A., de Haas N., Zeyda I., Mundt E. 2002; Alteration of amino acids in VP2 of very virulent infectious bursal disease virus results in tissue culture adaptation and attenuation in chickens. J Gen Virol 83:121–129[PubMed]
    [Google Scholar]
  33. von Einem U. I., Gorbalenya A. E., Schirrmeier H., Behrens S. E., Letzel T., Mundt E. 2004; VP1 of infectious bursal disease virus is an RNA-dependent RNA polymerase. J Gen Virol 85:2221–2229 [View Article][PubMed]
    [Google Scholar]
  34. Wang Y., Qi X., Gao H., Gao Y., Lin H., Song X., Pei L., Wang X. 2009; Comparative study of the replication of infectious bursal disease virus in DF-1 cell line and chicken embryo fibroblasts evaluated by a new real-time RT-PCR. J Virol Methods 157:205–210 [View Article][PubMed]
    [Google Scholar]
  35. Yu F., Qi X., Yuwen Y., Wang Y., Gao H., Gao Y., Qin L., Wang X. 2010; Molecular characteristics of segment B of seven very virulent infectious bursal disease viruses isolated in China. Virus Genes 41:246–249 [View Article][PubMed]
    [Google Scholar]
  36. Yu F., Qi X., Gao L., Wang Y., Gao Y., Qin L., Gao H., Wang X. 2012; A simple and efficient method to rescue very virulent infectious bursal disease virus using SPF chickens. Arch Virol 157:969–973 [View Article][PubMed]
    [Google Scholar]
  37. Yu F., Ren X., Wang Y., Qi X., Song J., Gao Y., Qin L., Gao H., Wang X. 2013; A single amino acid V4I substitution in VP1 attenuates virulence of very virulent infectious bursal disease virus (vvIBDV) in SPF chickens and increases replication in CEF cells. Virology 440:204–209 [View Article][PubMed]
    [Google Scholar]
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