1887

Abstract

The current dogma of influenza accepts that feral aquatic birds are the reservoir for influenza A viruses. Although the genomic information of human influenza A viruses is increasing, little of this type of data is available for viruses circulating in feral waterfowl. This study presents the genetic characterization of 35 viruses isolated from wild Canadian ducks from 1983 to 2000, as the first attempt at a comprehensive genotypic analysis of influenza viruses isolated from feral ducks. This study demonstrates that influenza virus genes circulating in Canadian ducks have achieved evolutionary stasis. The majority of these duck virus genes are clustered in distinct North American clades; however, some H6 and H9 genes are clustered with those from Eurasian viruses. Genes appeared to reassort in a random fashion. None of the genotypes identified remained present throughout all of the years examined and most PA and PB2 genes that crossed over into swine were clustered in one phylogenetic grouping. Additionally, matrix genes were identified that branch very early in the evolutionary tree. These findings demonstrate the diversity of the influenza virus gene pool in Canadian ducks, and suggest that genes which cluster in specific phylogenetic groupings in the PB2 and PA genes can be used for markers of viruses with the potential for crossing the species barrier. A more comprehensive study of this important reservoir is needed to provide further insight into the genomic composition of viruses that crossover the species barrier, which would be a useful component to pandemic planning.

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2004-08-01
2019-10-23
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References

  1. Aymard-Henry, M., Coleman, M. T., Dowdle, W. R., Laver, W. G., Schild, G. C. & Webster, R. G. ( 1973; ). Influenza virus neuraminidase and neuraminidase-inhibition test procedures. Bull W H O 48, 199–202.
    [Google Scholar]
  2. Bourmakina, S. V. & Garcia-Sastre, A. ( 2003; ). Reverse genetics studies on the filamentous morphology of influenza A virus. J Gen Virol 84, 517–527.[CrossRef]
    [Google Scholar]
  3. Brammer, L., Postrma, A., Harper, S., Klimov, A. & Cox, N. ( 2003; ). Update: influenza activity-United States, 2002–2003 season. Morb Mortal Wkly Rep 52, 224–225.
    [Google Scholar]
  4. Brown, I. H., Ludwig, S., Olsen, C. W. & 7 other authors ( 1997; ). Antigenic and genetic analyses of H1N1 influenza A viruses from European pigs. J Gen Virol 78, 553–562.
    [Google Scholar]
  5. Brown, I. H., Harris, P. A., McCauley, J. W. & Alexander, D. J. ( 1998; ). Multiple genetic reassortment of avian and human influenza A viruses in European pigs, resulting in the emergence of an H1N2 virus of novel genotype. J Gen Virol 79, 2947–2955.
    [Google Scholar]
  6. Choi, Y. K., Goyal, S. M., Farnham, M. W. & Joo, H. S. ( 2002; ). Phylogenetic analysis of H1N2 isolates of influenza A virus from pigs in the United States. Virus Res 87, 173–179.[CrossRef]
    [Google Scholar]
  7. 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]
  8. 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]
  9. Del Hoyo, J., Elliot, A. & Sargatel, J. ( 1992; ). Handbook of the Birds of the World, vol. 1 & 3. Barcelona: Lynx Edicions.
  10. Endo, A., Pecoraro, R., Sugita, S. & Nerome, K. ( 1992; ). Evolutionary pattern of the H 3 haemagglutinin of equine influenza viruses: multiple evolutionary lineages and frozen replication. Arch Virol 123, 73–87.[CrossRef]
    [Google Scholar]
  11. Gorman, O. T., Donis, R. O., Kawaoka, Y. & Webster, R. G. ( 1990; ). Evolution of influenza A virus PB2 genes: implications for evolution of the ribonucleoprotein complex and origin of human influenza A virus. J Virol 64, 4893–4902.
    [Google Scholar]
  12. Gorman, O. T., Bean, W. J. & Webster, R. G. ( 1992; ). Evolutionary processes in influenza viruses: divergence, rapid evolution, and stasis. Curr Top Microbiol Immunol 176, 75–97.
    [Google Scholar]
  13. Grambas, S., Bennett, M. S. & Hay, A. J. ( 1992; ). Influence of amantadine resistance mutations on the pH regulatory function of the M2 protein of influenza A viruses. Virology 191, 541–549.[CrossRef]
    [Google Scholar]
  14. Guan, Y., Shortridge, K. F., Krauss, S., Chin, P. S., Dyrting, K. C., Ellis, T. M., Webster, R. G. & Peiris, M. ( 2000; ). H9N2 influenza viruses possessing H5N1-like internal genomes continue to circulate in poultry in southeastern China. J Virol 74, 9372–9380.[CrossRef]
    [Google Scholar]
  15. 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.[CrossRef]
    [Google Scholar]
  16. 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.[CrossRef]
    [Google Scholar]
  17. Hay, A. J., Wolstenholme, A. J., Skehel, J. J. & Smith, M. H. ( 1985; ). The molecular basis of the specific anti-influenza action of amantadine. EMBO J 4, 3021–3024.
    [Google Scholar]
  18. Hinshaw, V. S., Webster, R. G. & Turner, B. ( 1979; ). Water-borne transmission of influenza A viruses? Intervirology 11, 66–68.[CrossRef]
    [Google Scholar]
  19. Hinshaw, V. S., Webster, R. G. & Turner, B. ( 1980; ). The perpetuation of orthomyxoviruses and paramyxoviruses in Canadian waterfowl. Can J Microbiol 26, 622–629.[CrossRef]
    [Google Scholar]
  20. 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.[CrossRef]
    [Google Scholar]
  21. Hoffmann, E., Stech, J., Guan, Y., Webster, R. G. & Perez, D. R. ( 2001; ). Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol 146, 2275–2289.[CrossRef]
    [Google Scholar]
  22. Horimoto, T. & Kawaoka, Y. ( 2001; ). Pandemic threat posed by avian influenza A viruses. Clin Microbiol Rev 14, 129–149.[CrossRef]
    [Google Scholar]
  23. Ito, T., Gorman, O. T., Kawaoka, Y., Bean, W. J. & Webster, R. G. ( 1991; ). Evolutionary analysis of the influenza A virus M gene with comparison of the M1 and M2 proteins. J Virol 65, 5491–5498.
    [Google Scholar]
  24. Ito, T., Okazaki, K., Kawaoka, Y., Takada, A., Webster, R. G. & Kida, H. ( 1995; ). Perpetuation of influenza A viruses in Alaskan waterfowl reservoirs. Arch Virol 140, 1163–1172.[CrossRef]
    [Google Scholar]
  25. Karasin, A. I., Brown, I. H., Carman, S. & Olsen, C. W. ( 2000; ). Isolation and characterization of H4N6 avian influenza viruses from pigs with pneumonia in Canada. J Virol 74, 9322–9327.[CrossRef]
    [Google Scholar]
  26. Karasin, A. I., Landgraf, J., Swenson, S., Erickson, G., Goyal, S., Woodruff, M., Scherba, G., Anderson, G. & Olsen, C. W. ( 2002; ). Genetic characterization of H1N2 influenza A viruses isolated from pigs throughout the United States. J Clin Microbiol 40, 1073–1079.[CrossRef]
    [Google Scholar]
  27. Kawaoka, Y., Chambers, T. M., Sladen, W. L. & Webster, R. G. ( 1988; ). Is the gene pool of influenza viruses in shorebirds and gulls different from that in wild ducks? Virology 163, 247–250.[CrossRef]
    [Google Scholar]
  28. Kawaoka, Y., Krauss, S. & Webster, R. G. ( 1989; ). Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. J Virol 63, 4603–4608.
    [Google Scholar]
  29. Lin, Y. P., Shu, L. L., Wright, S., Bean, W. J., Sharp, G. B., Shortridge, K. F. & Webster, R. G. ( 1994; ). Analysis of the influenza virus gene pool of avian species from southern China. Virology 198, 557–566.[CrossRef]
    [Google Scholar]
  30. Lindstrom, S., Endo, A., Sugita, S., Pecoraro, M., Hiromoto, Y., Kamada, M., Takahashi, T. & Nerome, K. ( 1998; ). Phylogenetic analyses of the matrix and non-structural genes of equine influenza viruses. Arch Virol 143, 1585–1598.[CrossRef]
    [Google Scholar]
  31. Liu, M., He, S., Walker, D. & 7 other authors ( 2003; ). The influenza virus gene pool in a poultry market in South Central China. Virology 305, 267–275.[CrossRef]
    [Google Scholar]
  32. Macken, C., Lu, H., Goodman, J. & Boykin, L. ( 2001; ). The value of a database in surveillance and vaccine selection. In Options for the Control of Influenza IV, pp. 103–106. Edited by A. D. M. E. Osterhaus, N. Cox & A. W. Hampson. Amsterdam: Elsevier Science.
  33. Makarova, N. V., Kaverin, N. V., Krauss, S., Senne, D. & Webster, R. G. ( 1999; ). Transmission of Eurasian avian H2 influenza virus to shorebirds in North America. J Gen Virol 80, 3167–3171.
    [Google Scholar]
  34. Nei, M. & Kumar, S. ( 2000; ). Accuracies and statistical tests of phylogenetic trees. In Molecular Evolution and Phylogenetics, pp. 165–186. Edited by M. Nei & S. Kumar. New York: Oxford University Press.
  35. Okazaki, K., Takada, A., Ito, T. & 13 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]
  36. Palmer, D. F., Coleman, W. R., Dowdle, W. R. & Schild, G. C. ( 1975; ). Advanced Laboratory Techniques for Influenza Diagnosis. Washington, DC, USA: Department of Health, Education and Welfare.
  37. Perez, D. R., Lim, W., Seiler, J. P., Yi, G., Peiris, M., Shortridge, K. F. & Webster, R. G. ( 2003; ). Role of quail in the interspecies transmission of H9 influenza A viruses: molecular changes on HA that correspond to adaptation from ducks to chickens. J Virol 77, 3148–3156.[CrossRef]
    [Google Scholar]
  38. Schafer, J. R., Kawaoka, Y., Bean, W. J., Suss, J., Senne, D. & Webster, R. G. ( 1993; ). Origin of the pandemic 1957 H2 influenza A virus and the persistence of its possible progenitors in the avian reservoir. Virology 194, 781–788.[CrossRef]
    [Google Scholar]
  39. Scholtissek, C. & Naylor, E. ( 1988; ). Fish farming and influenza pandemics. Nature 331, 215.[CrossRef]
    [Google Scholar]
  40. Scholtissek, C., Rohde, W., Von Hoyningen., V. & Rott, R. ( 1978; ). On the origin of the human influenza virus subtypes H2N2 and H3N2. Virology 87, 13–20.[CrossRef]
    [Google Scholar]
  41. Scholtissek, C., Burger, H., Bachmann, P. A. & Hannoun, C. ( 1983; ). Genetic relatedness of hemagglutinins of the H1 subtype of influenza A viruses isolated from swine and birds. Virology 129, 521–523.[CrossRef]
    [Google Scholar]
  42. Sharp, G. B., Kawaoka, Y., Wright, S. M., Turner, B., Hinshaw, V. & Webster, R. G. ( 1993; ). Wild ducks are the reservoir for only a limited number of influenza A subtypes. Epidemiol Infect 110, 161–176.[CrossRef]
    [Google Scholar]
  43. Sharp, G. B., Kawaoka, Y., Jones, D. J., Bean, W. J., Pryor, S. P., Hinshaw, V. & Webster, R. G. ( 1997; ). Coinfection of wild ducks by influenza A viruses: distribution patterns and biological significance. J Virol 71, 6128–6135.
    [Google Scholar]
  44. Suarez, D. L. & Perdue, M. L. ( 1998; ). Multiple alignment comparison of the non-structural genes of influenza A viruses. Virus Res 54, 59–69.[CrossRef]
    [Google Scholar]
  45. Subbarao, K., Klimov, A., Katz, J. & 13 other authors ( 1998; ). Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279, 393–396.[CrossRef]
    [Google Scholar]
  46. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. & Higgins, D. G. ( 1997; ). The clustal x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876–4882.[CrossRef]
    [Google Scholar]
  47. Webby, R. J., Woolcock, P. R., Krauss, S. L. & Webster, R. G. ( 2002; ). Reassortment and interspecies transmission of North American H6N2 influenza viruses. Virology 295, 44–53.[CrossRef]
    [Google Scholar]
  48. 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.
    [Google Scholar]
  49. Webster, R. G., Guan, Y., Peiris, M. & 9 other authors ( 2002; ). Characterization of H5N1 influenza viruses that continue to circulate in geese in southeastern China. J Virol 76, 118–126.[CrossRef]
    [Google Scholar]
  50. Ye, Z., Robinson, D. & Wagner, R. R. ( 1995; ). Nucleus-targeting domain of the matrix protein (M1) of influenza virus. J Virol 69, 1964–1970.
    [Google Scholar]
  51. Zhou, N. N., Senne, D. A., Landgraf, J. S. & 7 other authors ( 1999a; ). Genetic reassortment of avian, swine, and human influenza A viruses in American pigs. J Virol 73, 8851–8856.
    [Google Scholar]
  52. Zhou, N. N., Shortridge, K. F., Claas, E. C., Krauss, S. L. & Webster, R. G. ( 1999b; ). Rapid evolution of H5N1 influenza viruses in chickens in Hong Kong. J Virol 73, 3366–3374.
    [Google Scholar]
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