1887

Abstract

Revealing the frequency and determinants of reassortment among RNA genome segments is fundamental to understanding basic aspects of the biology and evolution of the influenza virus. To estimate the extent of genomic reassortment in influenza viruses circulating in North American swine, we performed a phylogenetic analysis of 139 whole-genome viral sequences sampled during 1998–2011 and representing seven antigenically distinct viral lineages. The highest amounts of reassortment were detected between the H3 and the internal gene segments (PB2, PB1, PA, NP, M and NS), while the lowest reassortment frequencies were observed among the H1γ, H1pdm and neuraminidase segments, particularly N1. Less reassortment was observed among specific haemagglutinin–neuraminidase combinations that were more prevalent in swine, suggesting that some genome constellations may be evolutionarily more stable.

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2012-12-01
2021-08-04
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References

  1. Bao Y., Bolotov P., Dernovoy D., Kiryutin B., Zaslavsky L., Tatusova T., Ostell J., Lipman D. 2008; The influenza virus resource at the National Center for Biotechnology Information. J Virol 82:596–601 [View Article][PubMed]
    [Google Scholar]
  2. Centers for Disease Control and Prevention 2012; Evaluation of rapid influenza diagnostic tests for influenza A (H3N2)v virus and updated case count – United States, 2012. MMWR Morb Mortal Wkly Rep 61:619–621[PubMed]
    [Google Scholar]
  3. Chen L. M., Davis C. T., Zhou H., Cox N. J., Donis R. O. 2008; Genetic compatibility and virulence of reassortants derived from contemporary avian H5N1 and human H3N2 influenza A viruses. PLoS Pathog 4:e1000072 [View Article][PubMed]
    [Google Scholar]
  4. Djikeng A., Halpin R., Kuzmickas R., Depasse J., Feldblyum J., Sengamalay N., Afonso C., Zhang X., Anderson N. G.other authors 2008; Viral genome sequencing by random priming methods. BMC Genomics 9:5 [View Article][PubMed]
    [Google Scholar]
  5. Ducatez M. F., Hause B., Stigger-Rosser E., Darnell D., Corzo C., Juleen K., Simonson R., Brockwell-Staats C., Rubrum A.other authors 2011; Multiple reassortment between pandemic (H1N1) 2009 and endemic influenza viruses in pigs, United States. Emerg Infect Dis 17:1624–1629 [View Article][PubMed]
    [Google Scholar]
  6. Gao Q., Palese P. 2009; Rewiring the RNAs of influenza virus to prevent reassortment. Proc Natl Acad Sci U S A 106:15891–15896 [View Article][PubMed]
    [Google Scholar]
  7. 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 [View Article][PubMed]
    [Google Scholar]
  8. Huelsenbeck J. P., Ronquist F. 2001; mrbayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755 [View Article][PubMed]
    [Google Scholar]
  9. Imai M., Kawaoka Y. 2012; The role of receptor binding specificity in interspecies transmission of influenza viruses. Curr Opin Virol 2:160–167 [View Article][PubMed]
    [Google Scholar]
  10. Karasin A. I., Carman S., Olsen C. W. 2006; Identification of human H1N2 and human-swine reassortant H1N2 and H1N1 influenza A viruses among pigs in Ontario, Canada (2003 to 2005). J Clin Microbiol 44:1123–1126 [View Article][PubMed]
    [Google Scholar]
  11. Kimble J. B., Sorrell E., Shao H., Martin P. L., Perez D. R. 2011; Compatibility of H9N2 avian influenza surface genes and 2009 pandemic H1N1 internal genes for transmission in the ferret model. Proc Natl Acad Sci U S A 108:12084–12088 [View Article][PubMed]
    [Google Scholar]
  12. Lekcharoensuk P., Lager K. M., Vemulapalli R., Woodruff M., Vincent A. L., Richt J. A. 2006; Novel swine influenza virus subtype H3N1, United States. Emerg Infect Dis 12:787–794 [View Article][PubMed]
    [Google Scholar]
  13. Li C., Hatta M., Nidom C. A., Muramoto Y., Watanabe S., Neumann G., Kawaoka Y. 2010; Reassortment between avian H5N1 and human H3N2 influenza viruses creates hybrid viruses with substantial virulence. Proc Natl Acad Sci U S A 107:4687–4692 [View Article][PubMed]
    [Google Scholar]
  14. Lindstrom S., Garten R., Balish A., Shu B., Emery S., Berman L., Barnes N., Sleeman K., Gubareva L.other authors 2012; Human infections with novel reassortant influenza A(H3N2)v viruses, United States, 2011. Emerg Infect Dis 18:834–837 [View Article][PubMed]
    [Google Scholar]
  15. Lorusso A., Vincent A. L., Harland M. L., Alt D., Bayles D. O., Swenson S. L., Gramer M. R., Russell C. A., Smith D. J.other authors 2011; Genetic and antigenic characterization of H1 influenza viruses from United States swine from 2008. J Gen Virol 92:919–930 [View Article][PubMed]
    [Google Scholar]
  16. Ma W., Lager K. M., Lekcharoensuk P., Ulery E. S., Janke B. H., Solórzano A., Webby R. J., García-Sastre A., Richt J. A. 2010; Viral reassortment and transmission after co-infection of pigs with classical H1N1 and triple-reassortant H3N2 swine influenza viruses. J Gen Virol 91:2314–2321 [View Article][PubMed]
    [Google Scholar]
  17. Mitnaul L. J., Matrosovich M. N., Castrucci M. R., Tuzikov A. B., Bovin N. V., Kobasa D., Kawaoka Y. 2000; Balanced hemagglutinin and neuraminidase activities are critical for efficient replication of influenza A virus. J Virol 74:6015–6020 [View Article][PubMed]
    [Google Scholar]
  18. Nelson M. I., Lemey P., Tan Y., Vincent A., Lam T. T., Detmer S., Viboud C., Suchard M. A., Rambaut A.other authors 2011; Spatial dynamics of human-origin H1 influenza A virus in North American swine. PLoS Pathog 7:e1002077 [View Article][PubMed]
    [Google Scholar]
  19. Nelson M. I., Vincent A. L., Kitikoon P., Holmes E. C., Gramer M. R. 2012; Evolution of novel reassortant A/H3N2 influenza viruses in North American swine and humans, 2009–2011. J Virol 86:8872–8878 [View Article][PubMed]
    [Google Scholar]
  20. Parker J., Rambaut A., Pybus O. G. 2008; Correlating viral phenotypes with phylogeny: accounting for phylogenetic uncertainty. Infect Genet Evol 8:239–246 [View Article][PubMed]
    [Google Scholar]
  21. Posada D., Crandall K. A. 1998; modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818 [View Article][PubMed]
    [Google Scholar]
  22. Rambaut, A. (2002 Sequence alignment editor, version 2.0. Available http://tree.bio.ed.ac.uk/software/seal/ Accessed 11 December 2011
  23. Smith G. J., Vijaykrishna D., Bahl J., Lycett S. J., Worobey M., Pybus O. G., Ma S. K., Cheung C. L., Raghwani J.other authors 2009; Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459:1122–1125 [View Article][PubMed]
    [Google Scholar]
  24. Sorrell E. M., Wan H., Araya Y., Song H., Perez D. R. 2009; Minimal molecular constraints for respiratory droplet transmission of an avian-human H9N2 influenza A virus. Proc Natl Acad Sci U S A 106:7565–7570 [View Article][PubMed]
    [Google Scholar]
  25. Swofford D. L. 2003; paup*: Phylogenetic analysis using parsimony (and other methods), version 4. Sunderland, MA: Sinauer Associates;
  26. Vijaykrishna D., Smith G. J., Pybus O. G., Zhu H., Bhatt S., Poon L. L., Riley S., Bahl J., Ma S. K.other authors 2011; Long-term evolution and transmission dynamics of swine influenza A virus. Nature 473:519–522 [View Article][PubMed]
    [Google Scholar]
  27. Vincent A. L., Ma W., Lager K. M., Janke B. H., Richt J. A. 2008; Swine influenza viruses a North American perspective. Adv Virus Res 72:127–154 [View Article][PubMed]
    [Google Scholar]
  28. Xu R., Zhu X., McBride R., Nycholat C. M., Yu W., Paulson J. C., Wilson I. A. 2012; Functional balance of the hemagglutinin and neuraminidase activities accompanies the emergence of the 2009 H1N1 influenza pandemic. J Virol 86:9221–9232 [View Article][PubMed]
    [Google Scholar]
  29. Zhou N. N., Senne D. A., Landgraf J. S., Swenson S. L., Erickson G., Rossow K., Liu L., Yoon K., Krauss S., Webster R. G. 1999; Genetic reassortment of avian, swine, and human influenza A viruses in American pigs. J Virol 73:8851–8856[PubMed]
    [Google Scholar]
  30. Zhou B., Donnelly M. E., Scholes D. T., St George K., Hatta M., Kawaoka Y., Wentworth D. E. 2009; Single-reaction genomic amplification accelerates sequencing and vaccine production for classical and swine origin human influenza A viruses. J Virol 83:10309–10313 [View Article][PubMed]
    [Google Scholar]
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