1887

Abstract

Genetic analysis of the M2 sequence of European porcine influenza A viruses reveals a high prevalence of amantadine resistance due to the substitution of serine 31 by asparagine in all three circulating subtypes, H1N1, H3N2 and H1N2. The M segment of all resistant strains belongs to a single genetic lineage. Whereas the first amantadine-resistant porcine strain was isolated in 1989, isolation of the last amantadine-susceptible strain dates to 1987, suggesting a displacement of amantadine-susceptible viruses by resistant strains soon after emergence of the mutation. Analysis of natural selection by codon-based tests indicates negative selection of codons 30, 31 and 34 which confer amantadine resistance. The codons 2, 11–28 and 54 of porcine and human strains exhibit differences in the patterns of substitution rates, suggesting different selection modes. Transfer of amantadine resistance by exchange of the M segment and viability of recombinant A/WSN/33 viruses with avian-like M segments raises concerns about the emergence of natural human reassortants.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.2008.007260-0
2009-04-01
2019-11-12
Loading full text...

Full text loading...

/deliver/fulltext/jgv/90/4/900.html?itemId=/content/journal/jgv/10.1099/vir.2008.007260-0&mimeType=html&fmt=ahah

References

  1. Abed, Y., Goyette, N. & Boivin, G. ( 2005; ). Generation and characterization of recombinant influenza A (H1N1) viruses harboring amantadine resistance mutations. Antimicrob Agents Chemother 49, 556–559.[CrossRef]
    [Google Scholar]
  2. Astrahan, P., Kass, I., Cooper, M. A. & Arkin, I. T. ( 2004; ). A novel method of resistance for influenza against a channel-blocking antiviral drug. Proteins 55, 251–257.[CrossRef]
    [Google Scholar]
  3. Bright, R. A., Medina, M. J., Xu, X., Perez-Oronoz, G., Wallis, T. R., Davis, X. R., Pavinelli, L., Cox, N. J. & Klimov, A. I. ( 2005; ). Incidence of adamantane resistance among influenza A (H3N2) viruses isolated worldwide from 1994 to 2005: a cause for concern. Lancet 366, 1175–1181.[CrossRef]
    [Google Scholar]
  4. Brown, I. H. ( 2000; ). The epidemiology and evolution of influenza viruses in pigs. Vet Microbiol 74, 29–46.[CrossRef]
    [Google Scholar]
  5. Brown, I. H., Ludwig, S., Olsen, C. W., Hannoun, C., Scholtissek, C., Hinshaw, V. S., Harris, P. A., McCauley, J. W., Strong, I. & Alexander, D. J. ( 1997; ). Antigenic and genetic analyses of H1N1 influenza A viruses from European pigs. J Gen Virol 78, 553–562.
    [Google Scholar]
  6. 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]
  7. Claas, E. C. J., Kawaoka, Y., De Jong, J. C., Masurel, N. & Webster, R. G. ( 1994; ). Infection of children with avian-human reassortant influenza virus from pigs in Europe. Virology 204, 453–457.[CrossRef]
    [Google Scholar]
  8. Deyde, V. M., Xu, X., Bright, R. A., Shaw, M., Smith, C. B., Zhang, Y., Shu, Y., Gubarewa, L. V., Cox, N. J. & Kimov, A. I. ( 2007; ). Surveillance of resistance to adamantanes among influenza A(H3N2) and A(H1N1) viruses isolated worldwide. J Infect Dis 196, 249–257.[CrossRef]
    [Google Scholar]
  9. Domingo, E. & Holland, J. J. ( 1997; ). RNA virus mutations and fitness for survival. Annu Rev Microbiol 51, 151–178.[CrossRef]
    [Google Scholar]
  10. Drummond, A. J. & Rambaut, A. ( 2007; ). beast: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7, 214 [CrossRef]
    [Google Scholar]
  11. Gregory, V., Lim, W., Cameron, K., Bennett, M., Klimov, A., Hall, H., Cox, N., Hay, A. J. & Lin, Y. ( 2001; ). Infection of a child in Hong Kong by an influenza A H3N2 virus closely related to viruses circulating in European pigs. J Gen Virol 82, 1397–1406.
    [Google Scholar]
  12. Gregory, V., Bennett, M., Thomas, Y., Kaiser, L., Wunderli, W., Matter, H., Hay, A. & Lin, Y. P. ( 2003; ). Human infection by a swine influenza A (H1N1) virus in Switzerland. Arch Virol 148, 793–802.[CrossRef]
    [Google Scholar]
  13. 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]
  14. Hayden, F. G. ( 2006; ). Antivirals for influenza: historical perspectives and lessons learned. Antiviral Res 71, 372–378.[CrossRef]
    [Google Scholar]
  15. Hoffmann, E., Neumann, G., Kawaoka, Y., Hobom, G. & Webster, R. G. ( 2000; ). A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci U S A 97, 6108–6113.[CrossRef]
    [Google Scholar]
  16. Hurt, A. C., Selleck, P., Komadina, N., Shaw, R., Brown, L. & Barr, I. G. ( 2007; ). Susceptibility of highly pathogenic A(H5N1) avian influenza viruses to the neuraminidase inhibitors and adamantanes. Antiviral Res 73, 228–231.[CrossRef]
    [Google Scholar]
  17. Kosakovsky Pond, S. L. & Frost, S. D. W. ( 2005; ). Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21, 2531–2533.[CrossRef]
    [Google Scholar]
  18. 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]
  19. 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.[CrossRef]
    [Google Scholar]
  20. Ludwig, S., Stitz, L., Planz, O., Van, H., Fitch, W. M. & Scholtissek, S. ( 1995; ). European swine virus as a possible source for the next influenza pandemic? Virology 212, 555–561.[CrossRef]
    [Google Scholar]
  21. Marozin, S., Gregory, V., Cameron, K., Bennett, M., Valette, M., Aymard, M., Foni, E., Barigazzi, G., Lin, Y. & Hay, A. ( 2002; ). Antigenic and genetic diversity among swine influenza A H1N1 and H1N2 viruses in Europe. J Gen Virol 83, 735–745.
    [Google Scholar]
  22. Masuda, H., Suzuki, H., Oshitani, H., Saito, R., Kawasaki, S., Nishikawa, M. & Satoh, H. ( 2000; ). Incidence of amantadine-resistant influenza A viruses in sentinel surveillance sites and nursing homes in Niigata, Japan. Microbiol Immunol 44, 833–839.[CrossRef]
    [Google Scholar]
  23. Nardelli, L., Pascucci, S., Gualandi, G. L. & Loda, P. ( 1978; ). Outbreaks of classical swine influenza in Italy in 1976. Zentralbl Veterinarmed B 25, 853–857.
    [Google Scholar]
  24. Page, R. D. M. ( 1996; ). TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12, 357–358.
    [Google Scholar]
  25. Pensaert, M., Ottis, K., Vandeputte, J., Kaplan, M. M. & Bachmann, P. A. ( 1981; ). Evidence for the natural transmission of influenza A virus from wild ducks to swine and its potential importance for man. Bull World Health Organ 59, 75–78.
    [Google Scholar]
  26. Poon, A. F. Y., Lewis, F. I., Kosakovsky Pond, S. L. & Frost, S. D. W. ( 2007; ). An evolutionary-network model reveals stratified interactions in the V3 loop of the HIV-1 envelope. PLoS Comput Biol 3, e231 [CrossRef]
    [Google Scholar]
  27. Posada, D. & Crandall, K. A. ( 1998; ). modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.[CrossRef]
    [Google Scholar]
  28. Rimmelzwaan, G. F., de Jong, J. C., Bestebroer, T. M., van Loon, A. M., Claas, E. C. J., Fouchier, R. A. M. & Osterhaus, A. D. M. E. ( 2001; ). Antigenic and genetic characterization of swine influenza A (H1N1) viruses isolated from pneumonia patients in the Netherlands. Virology 282, 301–308.[CrossRef]
    [Google Scholar]
  29. Ronquist, F. & Huelsenbeck, J. P. ( 2003; ). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.[CrossRef]
    [Google Scholar]
  30. Schmidtke, M., Zell, R., Bauer, K., Krumbholz, A., Schrader, C., Süss, J. & Wutzler, P. ( 2006; ). Amantadine resistance among porcine H1N1, H1N2, and H3N2 influenza A viruses isolated in Germany between 1981 and 2001. Intervirology 49, 286–293.[CrossRef]
    [Google Scholar]
  31. Schmidtke, M., Bauer, K., Ludwig, N. & Wutzler, P. ( 2008; ). Emergence and phylogenetic relationships of amantadine-resistant human H3N2 influenza A viruses in Germany in the season 2005/2006. Int J Antimicrob Agents 32, 192–198.[CrossRef]
    [Google Scholar]
  32. Schnell, J. R. & Chou, J. J. ( 2008; ). Structure and mechanism of the M2 proton channel of influenza A virus. Nature 451, 591–595.[CrossRef]
    [Google Scholar]
  33. Shiraishi, K., Mitamura, K., Sakai-Tagawa, Y., Goto, H., Sugaya, N. & Kawaoka, Y. ( 2003; ). High frequency of resistant viruses harboring different mutations in amantadine-treated children with influenza. J Infect Dis 188, 57–61.[CrossRef]
    [Google Scholar]
  34. Simonsen, L., Viboud, C., Grenfell, B. T., Dushoff, J., Jennings, L., Smit, M., Macken, C., Hata, M., Gog, J. & other authors ( 2007; ). The genesis and spread of reassortment human influenza A/H3N2 viruses conferring adamantane resistance. Mol Biol Evol 24, 1811–1820.[CrossRef]
    [Google Scholar]
  35. Stouffer, A. L., Acharya, R., Salom, D., Levine, A. S., Di Constanzo, L., Soto, C. S., Tereshko, V., Nanda, V., Stayrock, S. & DeGrado, W. F. ( 2008; ). Structural basis for the function and inhibition of an influenza virus proton channel. Nature 451, 596–599.[CrossRef]
    [Google Scholar]
  36. Tamura, K., Dudley, J., Nei, M. & Kumar, S. ( 2007; ). mega4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. Mol Biol Evol 24, 1596–1599.[CrossRef]
    [Google Scholar]
  37. Zell, R., Motzke, S., Krumbholz, A., Wutzler, P., Herwig, V. & Dürrwald, R. ( 2008; ). Novel reassortant of swine influenza H1N2 virus in Germany. J Gen Virol 89, 271–276.[CrossRef]
    [Google Scholar]
  38. Ziegler, T., Hemphill, M. L., Ziegler, M. L., Perez-Oronoz, G., Klimov, A. I., Hampson, A. W., Regnery, H. L. & Cox, N. J. ( 1999; ). Low incidence of rimantadine resistance in field isolates of influenza A viruses. J Infect Dis 180, 935–939.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.2008.007260-0
Loading
/content/journal/jgv/10.1099/vir.2008.007260-0
Loading

Data & Media loading...

Supplements

vol. , part 4, pp. 900–908

List of influenza A virus strains used in this study

Natural selection acting on the M2 open reading frame of porcine and human influenza viruses

[Single PDF](41 KB)



PDF

Most Cited This Month

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