1887

Abstract

Besides enormous economic losses to the poultry industry, recent H5N1 highly pathogenic avian influenza viruses (HPAIVs) originating in eastern Asia have posed serious threats to public health. Up to April 17, 2008, 381 human cases had been confirmed with a mortality of more than 60 %. Here, we attempt to identify potential progenitor genes for H5N1 HPAIVs since their first recognition in 1996; most were detected in the Eurasian landmass before 1996. Combinations among these progenitor genes generated at least 21 reassortants (named H5N1 progenitor reassortant, H5N1-PR1–21). H5N1-PR1 includes A/Goose/Guangdong/1/1996(H5N1). Only reassortants H5N1-PR2 and H5N1-PR7 were associated with confirmed human cases: H5N1-PR2 in the Hong Kong H5N1 outbreak in 1997 and H5N1-PR7 in laboratory confirmed human cases since 2003. H5N1-PR7 also contains a majority of the H5N1 viruses causing avian influenza outbreaks in birds, including the first wave of genotype Z, Qinghai-like and Fujian-like virus lineages. Among the 21 reassortants identified, 13 are first reported here. This study illustrates evolutionary patterns of H5N1 HPAIVs, which may be useful toward pandemic preparedness as well as avian influenza prevention and control.

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2008-09-01
2024-12-03
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References

  1. Bao Y., Federhen S., Leipe D., Pham V., Resenchuk S., Rozanov M., Tatusov R., Tatusova T. 2004; National center for biotechnology information viral genomes project. J Virol 78:7291–7298 [CrossRef]
    [Google Scholar]
  2. Chen H., Deng G., Li Z., Tian G., Li Y., Jiao P., Zhang L., Liu Z., Webster R. G., Yu K. 2004; The evolution of H5N1 influenza viruses in ducks in southern China. Proc Natl Acad Sci U S A 101:10452–10457 [CrossRef]
    [Google Scholar]
  3. Chen H., Smith G. J., Zhang S. Y., Qin K., Wang J., Li K. S., Webster R. G., Peiris J. S., Guan Y. 2005; Avian flu: H5N1 virus outbreak in migratory waterfowl. Nature 436:191–192 [CrossRef]
    [Google Scholar]
  4. Chen H., Smith G. J., Li K. S., Wang J., Fan X. H., Rayner J. M., Vijaykrishna D., Zhang J. X., Zhang L. J. other authors 2006; Establishment of multiple sublineages of H5N1 influenza virus in Asia: implications for pandemic control. Proc Natl Acad Sci U S A 103:2845–2850 [CrossRef]
    [Google Scholar]
  5. Claas E. C., Osterhaus A. D., van Beek R., De Jong J. C., Rimmelzwaan G. F., Senne D. A., Krauss S., Shortridge K. F., Webster R. G. 1998; Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 351:472–477 [CrossRef]
    [Google Scholar]
  6. Drummond A. J., Rambaut A. 2007; beast: bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214 [CrossRef]
    [Google Scholar]
  7. Duan L., Campitelli L., Fan X. H., Leung Y. H., Vijaykrishna D., Zhang J. X., Donatelli I., Delogu M., Li K. S. other authors 2007; Characterization of low-pathogenic H5 subtype influenza viruses from Eurasia: implications for the origin of highly pathogenic H5N1 viruses. J Virol 81:7529–7539 [CrossRef]
    [Google Scholar]
  8. Edgar R. C. 2004; muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797 [CrossRef]
    [Google Scholar]
  9. Guan Y., Peiris J. S., Lipatov A. S., Ellis T. M., Dyrting K. C., Krauss S., Zhang L. J., Webster R. G., Shortridge K. F. 2002; Emergence of multiple genotypes of H5N1 avian influenza viruses in Hong Kong SAR. Proc Natl Acad Sci U S A 99:8950–8955 [CrossRef]
    [Google Scholar]
  10. Guan Y., Poon L. L., Cheung C. Y., Ellis T. M., Lim W., Lipatov A. S., Chan K. H., Sturm-Ramirez K. M., Cheung C. L. other authors 2004; H5N1 influenza: a protean pandemic threat. Proc Natl Acad Sci U S A 101:8156–8161 [CrossRef]
    [Google Scholar]
  11. Guo Y., Xu X., Wan X. 1998; Genetic characterization of an avian influenza A (H5N1) virus isolated from a sick goose in China. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi 12:322–325 (in Chinese
    [Google Scholar]
  12. 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 [CrossRef]
    [Google Scholar]
  13. Li Y., Lin Z., Shi J., Qi Q., Deng G., Li Z., Wang X., Tian G., Chen H. 2006; Detection of Hong Kong 97-like H5N1 influenza viruses from eggs of Vietnamese waterfowl. Arch Virol 151:1615–1624 [CrossRef]
    [Google Scholar]
  14. Liu J., Xiao H., Lei F., Zhu Q., Qin K., Zhang X. W., Zhang X. L., Zhao D., Wang G. other authors 2005; Highly pathogenic H5N1 influenza virus infection in migratory birds. Science 309:1206 [CrossRef]
    [Google Scholar]
  15. Long J. X., Xue F., Peng Y., Gu M., Liu X. F. 2006; The deletion of nucleotides of NS gene from 263 to 277 of H5N1 increases viral virulence in chicken. Wei Sheng Wu Xue Bao 46:301–305 (in Chinese
    [Google Scholar]
  16. 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 [CrossRef]
    [Google Scholar]
  17. Okazaki K., Takada A., Ito T., Imai M., Takakuwa H., Hatta M., Ozaki H., Tanizaki T., Nagano T. other authors 2000; Precursor genes of future pandemic influenza viruses are perpetuated in ducks nesting in Siberia. Arch Virol 145:885–893 [CrossRef]
    [Google Scholar]
  18. Posada D., Crandall K. A. 1998; modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818 [CrossRef]
    [Google Scholar]
  19. Seo S. H., Hoffmann E., Webster R. G. 2002; Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat Med 8:950–954 [CrossRef]
    [Google Scholar]
  20. Shortridge K. F. 1992; Pandemic influenza: a zoonosis?. Semin Respir Infect 7:11–25
    [Google Scholar]
  21. Shortridge K. F., Stuart-Harris C. H. 1982; An influenza epicentre?. Lancet 2:812–813
    [Google Scholar]
  22. Shortridge K. F., Zhou N. N., Guan Y., Gao P., Ito T., Kawaoka Y., Kodihalli S., Krauss S., Markwell D. other authors 1998; Characterization of avian H5N1 influenza viruses from poultry in Hong Kong. Virology 252:331–342 [CrossRef]
    [Google Scholar]
  23. Sims L. D., Ellis T. M., Liu K. K., Dyrting K., Wong H., Peiris M., Guan Y., Shortridge K. F. 2003; Avian influenza in Hong Kong 1997–2002. Avian Dis 47:832–838 [CrossRef]
    [Google Scholar]
  24. Smith G. J., Fan X. H., Wang J., Li K. S., Qin K., Zhang J. X., Vijaykrishna D., Cheung C. L., Huang K. other authors 2006; Emergence and predominance of an H5N1 influenza variant in China. Proc Natl Acad Sci U S A 103:16936–16941 [CrossRef]
    [Google Scholar]
  25. Swofford D. L. 1998 paup*: phylogenetic analysis using parsimony (*and other methods Sunderland, MA: Sinauer Associates;
    [Google Scholar]
  26. Twu K. Y., Kuo R. L., Marklund J., Krug R. M. 2007; The H5N1 influenza virus NS genes selected after 1998 enhance virus replication in mammalian cells. J Virol 81:8112–8121 [CrossRef]
    [Google Scholar]
  27. Wan X.-F. 1998; Isolation and characterization of avian influenza viruses in China . Master thesis South China Agricultural University;
  28. Wan X. F., Ren T., Luo K. J., Liao M., Zhang G. H., Chen J. D., Cao W. S., Li Y., Jin N. Y. other authors 2005; Genetic characterization of H5N1 avian influenza viruses isolated in southern China during the 2003–04 avian influenza outbreaks. Arch Virol 150:1257–1266 [CrossRef]
    [Google Scholar]
  29. Wan X.-F., Wu X., Lin G., Holton S. B., Desmone R. A., Shyu C. R., Guan Y., Emch M. 2007a; Computational identification of reassortments in avian influenza viruses. Avian Dis 51:434–439 [CrossRef]
    [Google Scholar]
  30. Wan X. F., Chen G., Luo F., Emch M., Donis R. 2007b; A quantitative genotype algorithm reflecting H5N1 avian influenza niches. Bioinformatics 23:2368–2375 [CrossRef]
    [Google Scholar]
  31. Xu X., Subbarao K., Cox N. J., Guo Y. 1999; Genetic characterization of the pathogenic influenza A/Goose/Guangdong/1/96 (H5N1) virus: similarity of its hemagglutinin gene to those of H5N1 viruses from the 1997 outbreaks in Hong Kong. Virology 261:15–19 [CrossRef]
    [Google Scholar]
  32. Zwickl D. J. 2006; Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion . PhD thesis University of Texas at Austin;
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