1887

Abstract

The first confirmed outbreak of highly pathogenic avian influenza (HPAI) virus infections in North America was caused by A/turkey/Ontario/7732/1966 (H5N9); however, the phylogeny of this virus is largely unknown. This study performed genomic sequence analysis of 11 avian influenza isolates from 1956 to 1979 for comparison with A/turkey/Ontario/7732/1966 (H5N9). Phylogenetic and genetic analyses included these viruses in combination with all known full-genome sequences of avian viruses isolated before 1981. It was shown that a low-pathogenic avian influenza virus, A/turkey/Ontario/6213/1966 (H5N1), that had been isolated 3 months previously, was the closest known genetic relative with six genome segments of common lineage encoding the polymerase subunits PB2, PB1 and PA, nucleoprotein (NP), haemagglutinin (HA) and non-structural (NS) proteins. The lineages of these genome segments included reassortment with other North American turkey viruses that were all rooted in North American wild waterfowl with the HA gene originating from the H5N2 serotype. The phylogenies demonstrated adaptation from North American wild birds to turkeys with the possible involvement of domestic waterfowl. The turkey isolate, A/turkey/Wisconsin/1968 (H5N9), was the second most closely related poultry isolate to A/turkey/Ontario/7732/1966 (H5N9), possessing five common lineage genome segments (PB2, PB1, PA, HA and neuraminidase). The A/turkey/Ontario/6213/1966 (H5N1) virus was more virulent than A/turkey/Wisconsin/68 (H5N9) for chicken embryos and mice, indicating a greater biological similarity to A/turkey/Ontario/7732/1966 (H5N9). Thus, A/turkey/Ontario/6213/1966 (H5N1) was identified as the closest known ancestral relative of HPAI A/turkey/Ontario/7732/1966 (H5N9), which will serve as a useful reference virus for characterizing the early genetic and biological properties associated with the emergence of pathogenic avian influenza strains.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.042895-0
2012-08-01
2021-08-03
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/8/1649.html?itemId=/content/journal/jgv/10.1099/vir.0.042895-0&mimeType=html&fmt=ahah

References

  1. Alexander D. J., Parsons G., Manvell R. J. 1986; Experimental assessment of the pathogenicity of eight avian influenza A viruses of H5 subtype for chickens, turkeys, ducks and quail. Avian Pathol 15:647–662 [View Article][PubMed]
    [Google Scholar]
  2. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410[PubMed] [CrossRef]
    [Google Scholar]
  3. Basler C. F., Aguilar P. V. 2008; Progress in identifying virulence determinants of the 1918 H1N1 and the Southeast Asian H5N1 influenza A viruses. Antiviral Res 79:166–178 [View Article][PubMed]
    [Google Scholar]
  4. Brown E. G., Liu H., Kit L. C., Baird S., Nesrallah M. 2001; Pattern of mutation in the genome of influenza A virus on adaptation to increased virulence in the mouse lung: identification of functional themes. Proc Natl Acad Sci U S A 98:6883–6888 [View Article][PubMed]
    [Google Scholar]
  5. Brown E. G., Sattar S. A., Tetro J. A., Liu J. 2008; Trends in influenza A virus genetics: can we predict the natural evolution of a H5N1 Z?. Curr Top Virol 7:99–113
    [Google Scholar]
  6. Canadian Council on Animal Care 1993 Guide to Care and Use of Experimental Animals, 2nd edn. vol. 1 Ottowa, ON: Canadian Council on Animal Care;
    [Google Scholar]
  7. Forbes N. E., Ping J., Dankar S. K., Jia J. J., Selman M., Keleta L., Zhou Y., Brown E. G. 2012; Multifunctional adaptive NS1 mutations are selected upon human influenza virus evolution in the mouse. PLoS ONE 7:e31839 [View Article][PubMed]
    [Google Scholar]
  8. Ghedin E., Sengamalay N. A., Shumway M., Zaborsky J., Feldblyum T., Subbu V., Spiro D. J., Sitz J., Koo H. other authors 2005; Large-scale sequencing of human influenza reveals the dynamic nature of viral genome evolution. Nature 437:1162–1166 [View Article][PubMed]
    [Google Scholar]
  9. Guan Y., Peiris J. S., Poon L. L., Dyrting K. C., Ellis T. M., Sims L., Webster R. G., Shortridge K. F. 2003; Reassortants of H5N1 influenza viruses recently isolated from aquatic poultry in Hong Kong SAR. Avian Dis 47:Suppl.911–913 [View Article][PubMed]
    [Google Scholar]
  10. Hwang J., Lief F. S., Miller C. W., Mallinson E. T. 1970; An epornitic of type A influenza virus infection in ducks. J Am Vet Med Assoc 157:2106–2108[PubMed]
    [Google Scholar]
  11. Jadhao S. J., Nguyen D. C., Uyeki T. M., Shaw M., Maines T., Rowe T., Smith C., Huynh L. P., Nghiem H. K. other authors 2009; Genetic analysis of avian influenza A viruses isolated from domestic waterfowl in live-bird markets of Hanoi, Vietnam, preceding fatal H5N1 human infections in 2004. Arch Virol 154:1249–1261 [View Article][PubMed]
    [Google Scholar]
  12. Keleta L., Ibricevic A., Bovin N. V., Brody S. L., Brown E. G. 2008; Experimental evolution of human influenza virus H3 hemagglutinin in the mouse lung identifies adaptive regions in HA1 and HA2. J Virol 82:11599–11608 [View Article][PubMed]
    [Google Scholar]
  13. Lang G., Ferguson A. E. 1981; The extent and control of avian influenza in Canada. Can Vet J 22:377–381[PubMed]
    [Google Scholar]
  14. Lang G., Narayan O., Rouse B. T., Ferguson A. E., Connell M. C. 1968a; A new influenza A virus infection in turkeys II. A highly pathogenic variant, A/turkey/Ontario 772/66. Can Vet J 9:151–160[PubMed]
    [Google Scholar]
  15. Lang G., Rouse B. T., Narayan O., Ferguson A. E., Connell M. C. 1968b; A new influenza virus infection in turkeys. I. Isolation and characterization of virus 6213. Can Vet J 9:22–29[PubMed]
    [Google Scholar]
  16. Li K. S., Guan Y., Wang J., Smith G. J., Xu K. M., Duan L., Rahardjo A. P., Puthavathana P., Buranathai C. other authors 2004; Genesis of a highly pathogenic and potentially pandemic H5N1 influenza virus in eastern Asia. Nature 430:209–213 [View Article][PubMed]
    [Google Scholar]
  17. Lupiani B., Reddy S. M. 2009; The history of avian influenza. Comp Immunol Microbiol Infect Dis 32:311–323 [View Article][PubMed]
    [Google Scholar]
  18. Mukhtar M. M., Rasool S. T., Song D., Zhu C., Hao Q., Zhu Y., Wu J. 2007; Origin of highly pathogenic H5N1 avian influenza virus in China and genetic characterization of donor and recipient viruses. J Gen Virol 88:3094–3099 [View Article][PubMed]
    [Google Scholar]
  19. Narayan O., Lang G., Rouse B. T. 1969a; A new influenza A virus infection in turkeys. IV. Experimental susceptibility of domestic birds to virus strain turkey/Ontario 7732/1966. Arch Gesamte Virusforsch 26:149–165 [View Article][PubMed]
    [Google Scholar]
  20. Narayan O., Lang G., Rouse B. T. 1969b; A new influenza A virus infection in turkeys. V. Pathology of the experimental disease by strain turkey/Ontario 7732/66. Arch Gesamte Virusforsch 26:166–182 [View Article][PubMed]
    [Google Scholar]
  21. Philpott M., Hioe C., Sheerar M., Hinshaw V. S. 1990; Hemagglutinin mutations related to attenuation and altered cell tropism of a virulent avian influenza A virus. J Virol 64:2941–2947[PubMed]
    [Google Scholar]
  22. Ping J., Dankar S. K., Forbes N. E., Keleta L., Zhou Y., Tyler S., Brown E. G. 2010; PB2 and hemagglutinin mutations are major determinants of host range and virulence in mouse-adapted influenza A virus. J Virol 84:10606–10618 [View Article][PubMed]
    [Google Scholar]
  23. Ping J., Keleta L., Forbes N. E., Dankar S., Stecho W., Tyler S., Zhou Y., Babiuk L., Weingartl H. other authors 2011; Genomic and protein structural maps of adaptive evolution of human influenza A virus to increased virulence in the mouse. PLoS ONE 6:e21740 [View Article][PubMed]
    [Google Scholar]
  24. Rouse B. T., Lang G., Narayan O. 1968; A new influenza A virus infection in turkeys. 3. Pathology of the experimental disease by virus strain turkey/Ontario/6213/66. J Comp Pathol 78:525–533 [View Article][PubMed]
    [Google Scholar]
  25. Sandhu T. H., Hinshaw V. 2003; Influenza A virus infection of domestic ducks. Avian Dis 47:93–99
    [Google Scholar]
  26. Shaw M., Cooper L., Xu X., Thompson W., Krauss S., Guan Y., Zhou N., Klimov A., Cox N. other authors 2002; Molecular changes associated with the transmission of avian influenza a H5N1 and H9N2 viruses to humans. J Med Virol 66:107–114 [View Article][PubMed]
    [Google Scholar]
  27. Smithies L. K., Emerson F. G., Robertson S. M., Ruedy D. D. 1969; Two different type A influenza virus infections in turkeys in Wisconsin. II. 1968 outbreak. Avian Dis 13:606–610 [View Article][PubMed]
    [Google Scholar]
  28. Swayne D. E. 2009; High pathogenicity avian influenza in the Americas. In Avian Influenza pp. 191–216 Edited by Swayne D. E. Oxford, UK: Blackwell; [View Article]
    [Google Scholar]
  29. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [View Article][PubMed]
    [Google Scholar]
  30. Walker R. V., Bannister G. L. 1953; A filterable agent in ducks. Can J Comp Med Vet Sci 17:248–250[PubMed]
    [Google Scholar]
  31. Webster R. G., Bean W. J., Gorman O. T., Chambers T. M., Kawaoka Y. 1992; Evolution and ecology of influenza A viruses. Microbiol Rev 56:152–179[PubMed]
    [Google Scholar]
  32. Zhao Z.-M., Shortridge K. F., Garcia M., Guan Y., Wan X.-F. 2008; Genotypic diversity of H5N1 highly pathogenic avian influenza viruses. J Gen Virol 89:2182–2193 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.042895-0
Loading
/content/journal/jgv/10.1099/vir.0.042895-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

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