1887

Abstract

Highly pathogenic avian H5N1 viruses have circulated in South-east Asia for more than a decade and have now spread to more than 60 countries. The evolution of these viruses is characterized by frequent reassortment of the so-called ‘internal’ genes, creating novel genotypes. Additionally, over time, the surface glycoprotein, haemagglutinin (HA), which is the primary target of the adaptive immune response, has evolved by point mutation into 20 genetically and potentially antigenically distinct clades. To investigate the evolution of avian H5N1 influenza viruses, we undertook a high-resolution analysis of the reassortment of internal genes and evolution of HA of 651 avian H5N1 viruses from 2000 to 2008. Our analysis suggested: (i) all current H5N1 genotypes were derived from a single, clearly defined sequence of initial reassortment events; (ii) reassortment of just three of the internal genes had the most importance in avian H5N1 virus evolution; (iii) HA and the constellation of internal genes may be jointly important in the emergence of dominant variants. Further, our analysis led to the identification of evolutionarily significant molecular changes in the internal genes that may be significant for the emergence of these dominant variants.

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2010-08-01
2024-03-29
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References

  1. Benson D. A., Karsch-Mizrachi I., Lipman D. J., Ostell J., Wheeler D. L. 2008; GenBank. Nucleic Acids Res 36:D25–D30
    [Google Scholar]
  2. Chen W., Calvo P. A., Malide D., Gibbs J., Schubert U., Bacik I., Basta S., O’Neill R., Schickli J. other authors 2001; A novel influenza A virus mitochondrial protein that induces cell death. Nat Med 7:1306–1312
    [Google Scholar]
  3. 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
    [Google Scholar]
  4. 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
    [Google Scholar]
  5. Chen H., Li Y., Li Z., Shi J., Shinya K., Deng G., Qi Q., Tian G., Fan S. & other authors (2006a). Properties and dissemination of H5N1 viruses isolated during an influenza outbreak in migratory waterfowl in western China. J Virol 80:5976–5983
    [Google Scholar]
  6. 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 2006b; Establishment of multiple sublineages of H5N1 influenza virus in Asia: implications for pandemic control. Proc Natl Acad Sci U S A 103:2845–2850
    [Google Scholar]
  7. Cheung C. L., Vijaykrishna D., Smith G. J., Fan X. H., Zhang J. X., Bahl J., Duan L., Huang K., Tai H. other authors 2007; Establishment of influenza A virus (H6N1) in minor poultry species in southern China. J Virol 81:10402–10412
    [Google Scholar]
  8. Claas E. C., de Jong J. C., Van Beek R., Rimmelzwaan G. F., Osterhaus A. D. 1998a; Human influenza virus A/HongKong/156/97 (H5N1) infection. Vaccine 16:977–978
    [Google Scholar]
  9. 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. 1998b; Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 351:472–477
    [Google Scholar]
  10. Crescenzo-Chaigne B., Naffakh N., van der Werf S. 1999; Comparative analysis of the ability of the polymerase complexes of influenza viruses type A, B and C to assemble into functional RNPs that allow expression and replication of heterotypic model RNA templates in vivo . Virology 265:342–353
    [Google Scholar]
  11. de Jong J. C., Claas E. C., Osterhaus A. D., Webster R. G., Lim W. L. 1997; A pandemic warning?. Nature 389:554
    [Google Scholar]
  12. Duan L., Bahl J., Smith G. J., Wang J., Vijaykrishna D., Zhang L. J., Zhang J. X., Li K. S., Fan X. H. other authors 2008; The development and genetic diversity of H5N1 influenza virus in China, 1996–2006. Virology 380:243–254
    [Google Scholar]
  13. Dugan V. G., Chen R., Spiro D. J., Sengamalay N., Zaborsky J., Ghedin E., Nolting J., Swayne D. E., Runstadler J. A. other authors 2008; The evolutionary genetics and emergence of avian influenza viruses in wild birds. PLoS Pathog 4:e1000076
    [Google Scholar]
  14. Felsenstein J. 2004 Inferring Phylogenies Sunderland, MA: Sinauer Associates;
  15. Gabriel G., Dauber B., Wolff T., Planz O., Klenk H. D., Stech J. 2005; The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host. Proc Natl Acad Sci U S A 102:18590–18595
    [Google Scholar]
  16. Garten R. J., Davis C. T., Russell C. A., Shu B., Lindstrom S., Balish A., Sessions W. M., Xu X., Skepner E. other authors 2009; Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325:197–201
    [Google Scholar]
  17. Guan Y., Shortridge K. F., Krauss S., Webster R. G. 1999; Molecular characterization of H9N2 influenza viruses: were they the donors of the “internal” genes of H5N1 viruses in Hong Kong?. Proc Natl Acad Sci U S A 96:9363–9367
    [Google Scholar]
  18. 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. 2002a; Emergence of multiple genotypes of H5N1 avian influenza viruses in Hong Kong SAR. Proc Natl Acad Sci U S A 99:8950–8955
    [Google Scholar]
  19. Guan Y., Peiris M., Kong K. F., Dyrting K. C., Ellis T. M., Sit T., Zhang L. J., Shortridge K. F. 2002b; H5N1 influenza viruses isolated from geese in Southeastern China: evidence for genetic reassortment and interspecies transmission to ducks. Virology 292:16–23
    [Google Scholar]
  20. 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
    [Google Scholar]
  21. Guindon S., Gascuel O. 2003; A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
    [Google Scholar]
  22. Hatta M., Gao P., Halfmann P., Kawaoka Y. 2001; Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293:1840–1842
    [Google Scholar]
  23. Hoffmann E., Stech J., Leneva I., Krauss S., Scholtissek C., Chin P. S., Peiris M., Shortridge K. F., Webster R. G. 2000; Characterization of the influenza A virus gene pool in avian species in southern China: was H6N1 a derivative or a precursor of H5N1?. J Virol 74:6309–6315
    [Google Scholar]
  24. Jackson D., Hossain M. J., Hickman D., Perez D. R., Lamb R. A. 2008; A new influenza virus virulence determinant: the NS1 protein four C-terminal residues modulate pathogenicity. Proc Natl Acad Sci U S A 105:4381–4386
    [Google Scholar]
  25. 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
    [Google Scholar]
  26. Li Z., Chen H., Jiao P., Deng G., Tian G., Li Y., Hoffmann E., Webster R. G., Matsuoka Y., Yu K. 2005; Molecular basis of replication of duck H5N1 influenza viruses in a mammalian mouse model. J Virol 79:12058–12064
    [Google Scholar]
  27. 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
    [Google Scholar]
  28. Lu G., Rowley T., Garten R., Donis R. O. 2007; FluGenome: a web tool for genotyping influenza A virus. Nucleic Acids Res 35:W275–W279
    [Google Scholar]
  29. Macken C. A., Webby R. J., Bruno W. J. 2006; Genotype turnover by reassortment of replication complex genes from avian influenza A virus. J Gen Virol 87:2803–2815
    [Google Scholar]
  30. Massin P., van der Werf S., Naffakh N. 2001; Residue 627 of PB2 is a determinant of cold sensitivity in RNA replication of avian influenza viruses. J Virol 75:5398–5404
    [Google Scholar]
  31. Mazur I., Anhlan D., Mitzner D., Wixler L., Schubert U., Ludwig S. 2008; The proapoptotic influenza A virus protein PB1-F2 regulates viral polymerase activity by interaction with the PB1 protein. Cell Microbiol 10:1140–1152
    [Google Scholar]
  32. McAuley J. L., Hornung F., Boyd K. L., Smith A. M., McKeon R., Bennink J., Yewdell J. W., McCullers J. A. 2007; Expression of the 1918 influenza A virus PB1-F2 enhances the pathogenesis of viral and secondary bacterial pneumonia. Cell Host Microbe 2:240–249
    [Google Scholar]
  33. Naffakh N., Massin P., Escriou N., Crescenzo-Chaigne B., van der Werf S. 2000; Genetic analysis of the compatibility between polymerase proteins from human and avian strains of influenza A viruses. J Gen Virol 81:1283–1291
    [Google Scholar]
  34. Nelson M. I., Viboud C., Simonsen L., Bennett R. T., Griesemer S. B., St George K., Taylor J., Spiro D. J., Sengamalay N. A. other authors 2008; Multiple reassortment events in the evolutionary history of H1N1 influenza A virus since 1918. PLoS Pathog 4:e1000012
    [Google Scholar]
  35. Neumann G., Noda T., Kawaoka Y. 2009; Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459:931–939
    [Google Scholar]
  36. Novel Swine-Origin Influenza A (H1N1) Virus Investigation Team; 2009; Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med 360:2605–2615
    [Google Scholar]
  37. Obenauer J. C., Denson J., Mehta P. K., Su X., Mukatira S., Finkelstein D. B., Xu X., Wang J., Ma J. other authors 2006; Large-scale sequence analysis of avian influenza isolates. Science 311:1576–1580
    [Google Scholar]
  38. Palese P., Shaw M. 2007; Orthomyxoviridae : The viruses and their replication. In Fields Virology , 5th edn. pp 1647–1689 Edited by Knipe D. M., Howley P. M., Griffin D. E., Lamb R. A., Martin M. A., Roizman B., Straus S. E. Philadelphia, PA: Wolters Kluwer, Lippincott Williams & Wilkins;
    [Google Scholar]
  39. Salomon R., Franks J., Govorkova E. A., Ilyushina N. A., Yen H. L., Hulse-Post D. J., Humberd J., Trichet M., Rehg J. E. other authors 2006; The polymerase complex genes contribute to the high virulence of the human H5N1 influenza virus isolate A/Vietnam/1203/04. J Exp Med 203:689–697
    [Google Scholar]
  40. Shinya K., Hamm S., Hatta M., Ito H., Ito T., Kawaoka Y. 2004; PB2 amino acid at position 627 affects replicative efficiency, but not cell tropism, of Hong Kong H5N1 influenza A viruses in mice. Virology 320:258–266
    [Google Scholar]
  41. 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 2006a; Emergence and predominance of an H5N1 influenza variant in China. Proc Natl Acad Sci U S A 103:16936–16941
    [Google Scholar]
  42. Smith G. J., Naipospos T. S., Nguyen T. D., de Jong M. D., Vijaykrishna D., Usman T. B., Hassan S. S., Nguyen T. V., Dao T. V. other authors 2006b; Evolution and adaptation of H5N1 influenza virus in avian and human hosts in Indonesia and Vietnam. Virology 350:258–268
    [Google Scholar]
  43. Smith G. J., Vijaykrishna D., Ellis T. M., Ellis T. M., Dyrting K. C., Leung Y. H., Bahl J., Wong C. W., Kai H. other authors 2009; Characterization of avian influenza viruses A (H5N1) from wild birds, Hong Kong, 2004–2008. Emerg Infect Dis 15:402–407
    [Google Scholar]
  44. Subbarao K., Klimov A., Katz J., Regnery H., Lim W., Hall H., Perdue M., Swayne D., Bender C. other authors 1998; Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279:393–396
    [Google Scholar]
  45. Sweet T. M., Maassab H. F., Herlocher M. L. 2004; Reverse genetics studies of attenuation of the ca A/AA/6/60 influenza virus: the role of the matrix gene. Biomed Pharmacother 58:509–515
    [Google Scholar]
  46. Van Hoeven N., Pappas C., Belser J. A., Maines T. R., Zeng H., Garcia-Sastre A., Sasisekharan R., Katz J. M., Tumpey T. M. 2009; Human HA and polymerase subunit PB2 proteins confer transmission of an avian influenza virus through the air. Proc Natl Acad Sci U S A 106:3366–3371
    [Google Scholar]
  47. Vijaykrishna D., Bahl J., Riley S., Duan L., Zhang J. X., Chen H., Peiris J. S., Smith G. J., Guan Y. 2008; Evolutionary dynamics and emergence of panzootic H5N1 influenza viruses. PLoS Pathog 4:e1000161
    [Google Scholar]
  48. Wan X. F., Nguyen T., Davis C. T., Smith C. B., Zhao Z. M., Carrel M., Inui K., Do H. T., Mai D. T. other authors 2008; Evolution of highly pathogenic H5N1 avian influenza viruses in Vietnam between 2001 and 2007. PLoS One 3:e3462
    [Google Scholar]
  49. Watanabe T., Watanabe S., Shinya K., Kim J. H., Hatta M., Kawaoka Y. 2009; Viral RNA polymerase complex promotes optimal growth of 1918 virus in the lower respiratory tract of ferrets. Proc Natl Acad Sci U S A 106:588–592
    [Google Scholar]
  50. WHO 2008; Toward a unified nomenclature system for highly pathogenic avian influenza virus (H5N1. Emerg Infect Dis 14:e1
    [Google Scholar]
  51. WHO Global Influenza Program Surveillance Network 2005; Evolution of H5N1 avian influenza viruses in Asia. Emerg Infect Dis 11:1515–1521
    [Google Scholar]
  52. Wright P. F., Neumann G., Kawaoka Y. 2007; Orthomyxoviruses. In Fields Virology , 5th edn. pp 1691–1740 Edited by Knipe D. M., Howley P. M., Griffin D. E., Lamb R. A., Martin M. A., Roizman B., Straus. Philadelphia, PA: Wolters Kluwer, Lippincott Williams & Wilkins;
    [Google Scholar]
  53. 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
    [Google Scholar]
  54. Xu K. M., Smith G. J., Bahl J., Duan L., Tai H., Vijaykrishna D., Wang J., Zhang J. X., Li K. S. other authors 2007; The genesis and evolution of H9N2 influenza viruses in poultry from southern China; 2000 to 2005 J Virol 81:10389–10401
    [Google Scholar]
  55. Zamarin D., Garcia-Sastre A., Xiao X., Wang R., Palese P. 2005; Influenza virus PB1-F2 protein induces cell death through mitochondrial ANT3 and VDAC1. PLoS Pathog 1:e4
    [Google Scholar]
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