1887

Abstract

The purpose of this study was to compare the molecular epidemiology of infectious bursal disease virus (IBDV) segments A and B of 50 natural or vaccine IBDV strains that were isolated or produced between 1972 and 2002 in 17 countries from four continents, with phenotypes ranging from attenuated to very virulent (vv). These strains were subjected to sequence and phylogenetic analysis based on partial sequences of genome segments A and B. Although there is co-evolution of the two genome segments (70 % of strains kept the same genetic relatives in the segment A- and B-defined consensus trees), several strains (26 %) were identified with the incongruence length difference test as exhibiting a significantly different phylogenetic relationship depending on which segment was analysed. This suggested that natural reassortment could have occurred. One of the possible naturally occurring reassortant strains, which exhibited a segment A related to the vvIBDV cluster whereas its segment B was not, was thoroughly sequenced (coding sequence of both segments) and submitted to a standardized experimental characterization of its acute pathogenicity. This strain induced significantly less mortality than typical vvIBDVs; however, the mechanisms for this reduced pathogenicity remain unknown, as no significant difference in the bursal lesions, post-infectious antibody response or virus production in the bursa was observed in challenged chickens.

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2006-01-01
2019-11-18
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References

  1. Bayliss, C. D., Spies, U., Shaw, K., Peters, R. W., Papageorgiou, A., Müller, H. & Boursnell, M. E. ( 1990; ). A comparison of the sequences of segment A of four infectious bursal disease virus strains and identification of a variable region in VP2. J Gen Virol 71, 1303–1312.[CrossRef]
    [Google Scholar]
  2. Boot, H. J., ter Huurne, A. A., Hoekman, A. J., Peeters, B. P. & Gielkens, A. L. ( 2000; ). Rescue of very virulent mosaic IBDV from cloned cDNA: VP2 is not the sole determinant of the very virulent phenotype. J Virol 74, 6701–6711.[CrossRef]
    [Google Scholar]
  3. Boot, H. J., Hoekman, A. J. & Gielkens, A. L. ( 2005; ). The enhanced virulence of very virulent infectious bursal disease virus is partly determined by its B segment. Arch Virol 150, 137–144.[CrossRef]
    [Google Scholar]
  4. Brandt, M., Yao, K., Meihong, L., 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.[CrossRef]
    [Google Scholar]
  5. Brown, M. D. & Skinner, M. A. ( 1996; ). Coding sequences of both genome segments of a European ‘very virulent’ infectious bursal disease virus. Virus Res 40, 1–15.[CrossRef]
    [Google Scholar]
  6. Bygrave, A. C. & Faragher, J. T. ( 1970; ). Mortality associated with Gumboro disease. Vet Rec 86, 758–759.
    [Google Scholar]
  7. Chettle, N. J., Stuart, J. C. & Wyeth, P. J. ( 1989; ). Outbreaks of virulent infectious bursal disease in East Anglia. Vet Rec 125, 271–272.[CrossRef]
    [Google Scholar]
  8. 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 C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger & L. A. Ball. London: Academic Press.
  9. Domanska, K., Mato, T., Rivallan, G. & 7 other authors ( 2004; ). Antigenic and genetic diversity of early European isolates of Infectious bursal disease virus prior to the emergence of the very virulent viruses: early European epidemiology of Infectious bursal disease virus revisited? Arch Virol 149, 465–480.[CrossRef]
    [Google Scholar]
  10. Eterradossi, N., Picault, J. P., Drouin, P., Guittet, M., L'Hospitalier, R. & Bennejean, G. ( 1992; ). Pathogenicity and preliminary antigenic characterization of six infectious bursal disease virus strains isolated in France from acute outbreaks. Zentralbl Veterinarmed B 39, 683–691.
    [Google Scholar]
  11. Eterradossi, N., Toquin, D., Rivallan, G. & Guittet, M. ( 1997a; ). Modified activity of a VP2-located neutralizing epitope on various vaccine, pathogenic and hypervirulent strains of infectious bursal disease virus. Arch Virol 142, 255–270.[CrossRef]
    [Google Scholar]
  12. Eterradossi, N., Rivallan, G., Toquin, D. & Guittet, M. ( 1997b; ). Limited antigenic variation among recent infectious bursal disease virus isolates from France. Arch Virol 142, 2079–2087.[CrossRef]
    [Google Scholar]
  13. Eterradossi, N., Arnauld, C., Toquin, D. & Rivallan, G. ( 1998; ). Critical amino acid changes in VP2 variable domain are associated with typical and atypical antigenicity in very virulent infectious bursal disease viruses. Arch Virol 143, 1627–1636.[CrossRef]
    [Google Scholar]
  14. Eterradossi, N., Arnaud, C., Tekaia, F. & 7 other authors ( 1999; ). Antigenic and genetic relationships between European very virulent infectious bursal disease viruses and an early West African isolate. Avian Pathol 28, 36–46.[CrossRef]
    [Google Scholar]
  15. Eterradossi, N., Gauthier, C., Reda, I. & 9 other authors ( 2004; ). Extensive antigenic changes in an atypical isolate of very virulent infectious bursal disease virus and experimental clinical control of this virus with an antigenically classical live vaccine. Avian Pathol 33, 423–431.[CrossRef]
    [Google Scholar]
  16. Farris, J. S., Källersjö, M., Kluge, A. G. & Bult, C. ( 1994; ). Testing significance of incongruence. Cladistics 10, 315–319.[CrossRef]
    [Google Scholar]
  17. Felsenstein, J. ( 1993; ). phylip (phylogeny inference package), version 3.5c. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle, USA.
  18. Guindon, S. & Gascuel, O. ( 2003; ). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52, 696–704.[CrossRef]
    [Google Scholar]
  19. Hoque, M. M., Omar, A. R., Chong, L. K., Hair-Bejo, M. & Aini, I. ( 2001; ). Pathogenicity of SspI-positive infectious bursal disease virus and molecular characterization of the VP2 hypervariable region. Avian Pathol 30, 369–380.[CrossRef]
    [Google Scholar]
  20. Ignjatovic, J. & Sapats, S. ( 2002; ). Confirmation of the existence of two distinct genetic groups of infectious bursal disease virus in Australia. Aust Vet J 80, 689–694.[CrossRef]
    [Google Scholar]
  21. Islam, M. R., Zierenberg, K. & Muller, 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.[CrossRef]
    [Google Scholar]
  22. Kibenge, F. S. B., Dhillon, A. S. & Russell, R. G. ( 1988; ). Biochemistry and immunology of infectious bursal disease virus. J Gen Virol 69, 1757–1775.[CrossRef]
    [Google Scholar]
  23. Kong, L. L., Omar, A. R., Hair-Bejo, M., Aini, I. & Seow, H. F. ( 2004; ). Sequence analysis of both genome segments of two very virulent infectious bursal disease virus field isolates with distinct pathogenicity. Arch Virol 149, 425–434.[CrossRef]
    [Google Scholar]
  24. Lasher, H. N. & Shane, S. M. ( 1994; ). Infectious bursal disease. World Poultry Sci J 50, 133–166.[CrossRef]
    [Google Scholar]
  25. Lecointre, G. L., Rachdi, P., Darlu, P. & Denamur, E. ( 1998; ). Escherichia coli molecular phylogeny using the incongruence length difference test. Mol Biol Evol 15, 1685–1695.[CrossRef]
    [Google Scholar]
  26. Le Nouën, C., Rivallan, G., Toquin, D. & Eterradossi, N. ( 2005; ). Significance of the genetic relationships deduced from partial nucleotide sequencing of infectious bursal disease virus genome segments A or B. Arch Virol 150, 313–325.[CrossRef]
    [Google Scholar]
  27. Lim, B. L., Cao, Y., Yu, T. & Mo, C. W. ( 1999; ). Adaptation of very virulent infectious bursal disease virus to chicken embryonic fibroblasts by site-directed mutagenesis of residues 279 and 284 of viral coat protein VP2. J Virol 73, 2854–2862.
    [Google Scholar]
  28. Liu, M. & Vakharia, V. N. ( 2004; ). VP1 protein of infectious bursal disease virus modulates the virulence in vivo. Virology 330, 62–73.[CrossRef]
    [Google Scholar]
  29. Lombardo, E., Maraver, A., Espinosa, I., Fernandez-Arias, A. & Rodriguez, F. J. ( 2000; ). VP5, the nonstructural polypeptide of infectious bursal disease virus, accumulates within the host plasma membrane and induces cell lysis. Virology 277, 345–357.[CrossRef]
    [Google Scholar]
  30. Macreadie, I. & Azad, A. A. ( 1993; ). Expression and RNA dependent RNA polymerase activity of birnavirus VP1 protein bacteria and yeast. Biochem Mol Biol Int 6, 1169–1178.
    [Google Scholar]
  31. Müller, H. & Nitschke, R. ( 1987; ). The two segments of the infectious bursal disease virus genome are circularized by a 90,000-Da protein. Virology 159, 174–177.[CrossRef]
    [Google Scholar]
  32. 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.
    [Google Scholar]
  33. Mundt, E. & Vakharia, V. N. ( 1996; ). Synthetic transcripts of double-stranded Birnavirus genome are infectious. Proc Natl Acad Sci U S A 93, 11131–11136.[CrossRef]
    [Google Scholar]
  34. Parede, L. H., Sapats, S., Gould, G., Rudd, M., Lowther, S. & Ignjatovic, J. ( 2003; ). Characterization of infectious bursal disease virus isolates from Indonesia indicates the existence of very virulent strains with unique genetic changes. Avian Pathol 32, 511–518.[CrossRef]
    [Google Scholar]
  35. Reed, L. J. & Muench, H. ( 1938; ). A simple method of estimation of fifty per cent end-points. Am J Hyg 27, 493–497.
    [Google Scholar]
  36. Roner, M. R., Bassett, K. & Roehr, J. ( 2004; ). Identification of the 5′ sequences required for incorporation of an engineered ssRNA into the Reovirus genome. Virology 329, 348–360.[CrossRef]
    [Google Scholar]
  37. Sapats, S. I., Ashton, F., Wright, P. J. & Ignjatovic, J. ( 1996; ). Sequence analysis of the S1 glycoprotein of infectious bronchitis viruses: identification of a novel genotypic group in Australia. J Gen Virol 77, 413–418.[CrossRef]
    [Google Scholar]
  38. Schnitzler, D., Bernstein, F., Müller, H. & Becht, H. ( 1993; ). The genetic basis for the antigenicity of the VP2 protein of the infectious bursal disease virus. J Gen Virol 74, 1563–1571.[CrossRef]
    [Google Scholar]
  39. Skeeles, J. K., Luckert, P. D., Fletcher, O. J. & Leonard, D. J. ( 1979; ). Immunization studies with a cell culture adapted infectious bursal disease virus. Avian Dis 23, 456–465.[CrossRef]
    [Google Scholar]
  40. Spies, U., Müller, H. & Becht, H. ( 1989; ). Nucleotide sequence of infectious bursal disease virus genome segment A delineates two major open reading frames. Nucleic Acids Res 17, 7982.[CrossRef]
    [Google Scholar]
  41. Sun, J. H., Lu, P., Yan, Y. X., Hua, X. G., Jiang, J. & Zhao, Y. ( 2003; ). Sequence and analysis of genomic segment A and B of very virulent infectious bursal disease virus isolated from China. J Vet Med B Infect Dis Vet Public Health 50, 148–154.[CrossRef]
    [Google Scholar]
  42. Swofford, D. L. ( 2002; ). paup* Phylogenetic Analysis Using Parsimony. Sunderland, MA: Sinauer Associates.
  43. Tacken, M. G., Rottier, P. J., Gielkens, A. L. & Peeters, B. P. ( 2000; ). Interactions in vivo between the proteins of infectious bursal disease virus: capsid protein VP3 interacts with the RNA-dependent RNA polymerase, VP1. J Gen Virol 81, 209–218.
    [Google Scholar]
  44. 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.[CrossRef]
    [Google Scholar]
  45. Vakharia, V. N., He, J., Ahamed, B. & Snyder, D. B. ( 1994; ). Molecular basis of antigenic variation in infectious bursal disease virus. Virus Res 31, 265–273.[CrossRef]
    [Google Scholar]
  46. 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, 409–421.[CrossRef]
    [Google Scholar]
  47. van den Berg, T. P., Morales, D. N., Eterradossi, N. & 12 other authors ( 2004; ). Assessment of genetic, antigenic and pathotypic criteria for the characterization of IBDV strains. Avian Pathol 33, 470–476.[CrossRef]
    [Google Scholar]
  48. van Loon, A. A. W. M., 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.
    [Google Scholar]
  49. 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.[CrossRef]
    [Google Scholar]
  50. Yamaguchi, T., Ogawa, M., Miyoshi, M., Inoshima, Y., Fukushi, H. & Hirai, K. ( 1997; ). Sequence and phylogenetic analyses of highly virulent infectious bursal disease virus. Arch Virol 142, 1441–1458.[CrossRef]
    [Google Scholar]
  51. Yao, K. & Vakharia, N. V. ( 2001; ). Induction of apoptosis in vitro by the 17-kDa nonstructural protein of infectious bursal disease virus: possible role in viral pathogenesis. Virology 285, 50–58.[CrossRef]
    [Google Scholar]
  52. Yao, K., Goodwin, M. A. & Vakharia, V. N. ( 1998; ). Generation of a mutant infectious bursal disease virus that do not cause bursal lesions. J Virol 72, 2647–2654.
    [Google Scholar]
  53. Zierenberg, K., Nieper, H., van den Berg, T. P., Ezeokoli, C. D., Voss, M. & Muller, H. ( 2000; ). The VP2 variable region of African and German isolates of infectious bursal disease virus: comparison with very virulent, “classical” virulent, and attenuated tissue culture-adapted strains. Arch Virol 145, 113–125.[CrossRef]
    [Google Scholar]
  54. Zierenberg, K., Raue, R., Nieper, H., Islam, M. R., Eterradossi, N., Toquin, D. & Müller, H. ( 2004; ). Generation of serotype 1/serotype 2 reassortant viruses of the infectious bursal disease virus and their investigation in vitro and in vivo. Virus Res 105, 23–34.[CrossRef]
    [Google Scholar]
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vol. , part 1, pp. 209 - 216

Virus strains included in the molecular epidemiology studies.

Oligonucleotide primers used in this study.

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