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Volume 96, Issue 7

New reassortant and enzootic European swine influenza viruses transmit efficiently through direct contact in the ferret model Free

Abstract

The reverse zoonotic events that introduced the 2009 pandemic influenza virus into pigs have drastically increased the diversity of swine influenza viruses in Europe. The pandemic potential of these novel reassortments is still unclear, necessitating enhanced surveillance of European pigs with additional focus on risk assessment of these new viruses. In this study, four European swine influenza viruses were assessed for their zoonotic potential. Two of the four viruses were enzootic viruses of subtype H1N2 (with avian-like H1) and H3N2, and two were new reassortants, one with avian-like H1 and human-like N2 and one with 2009 pandemic H1 and swine-like N2. All viruses replicated to high titres in nasal wash and nasal turbinate samples from inoculated ferrets and transmitted efficiently by direct contact. Only the H3N2 virus transmitted to naïve ferrets via the airborne route. Growth kinetics using a differentiated human bronchial epithelial cell line showed that all four viruses were able to replicate to high titres. Further, the viruses revealed preferential binding to the 2,6-α-silalylated glycans and investigation of the antiviral susceptibility of the viruses revealed that all were sensitive to neuraminidase inhibitors. These findings suggested that these viruses have the potential to infect humans and further underline the need for continued surveillance as well as biological characterization of new influenza A viruses.

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2015-07-01
2024-05-03
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References

  1. Abusugra I. A., Linné T., Klingeborn B. (1987). The provenance of the Swedish swine influenza H1N1 virus of 1983. Zentralbl Veterinarmed B 34, 566–572.[PubMed] [Google Scholar]
  2. Barman S., Krylov P. S., Fabrizio T. P., Franks J., Turner J. C., Seiler P., Wang D., Rehg J. E., Erickson G. A. et al. (2012). Pathogenicity and transmissibility of North American triple reassortant swine influenza A viruses in ferrets. PLoS Pathog 8, e1002791. [View Article][PubMed] [Google Scholar]
  3. Baum L. G., Paulson J. C. (1990). Sialyloligosaccharides of the respiratory epithelium in the selection of human influenza virus receptor specificity. Acta Histochem Suppl 40, 35–38.[PubMed] [Google Scholar]
  4. Breum S. Ø., Hjulsager C. K., Trebbien R., Larsen L. E. (2013). Influenza A virus with a human-like N2 gene is circulating in pigs. Genome Announc 1, e00712-13. [View Article][PubMed] [Google Scholar]
  5. Campbell P. J., Danzy S., Kyriakis C. S., Deymier M. J., Lowen A. C., Steel J. (2014). The M segment of the 2009 pandemic influenza virus confers increased neuraminidase activity, filamentous morphology, and efficient contact transmissibility to A/Puerto Rico/8/1934-based reassortant viruses. J Virol 88, 3802–3814. [View Article][PubMed] [Google Scholar]
  6. Castrucci M. R., Donatelli I., Sidoli L., Barigazzi G., Kawaoka Y., Webster R. G. (1993). Genetic reassortment between avian and human influenza A viruses in Italian pigs. Virology 193, 503–506. [View Article][PubMed] [Google Scholar]
  7. Chou H. H., Takematsu H., Diaz S., Iber J., Nickerson E., Wright K. L., Muchmore E. A., Nelson D. L., Warren S. T., Varki A. (1998). A mutation in human CMP-sialic acid hydroxylase occurred after the Homo–Pan divergence. Proc Natl Acad Sci U S A 95, 11751–11756. [View Article][PubMed] [Google Scholar]
  8. De Vleeschauwer A., Atanasova K., Van Borm S., van den Berg T., Rasmussen T. B., Uttenthal Å., Van Reeth K. (2009). Comparative pathogenesis of an avian H5N2 and a swine H1N1 influenza virus in pigs. PLoS One 4, e6662. [View Article][PubMed] [Google Scholar]
  9. Dunham E. J., Dugan V. G., Kaser E. K., Perkins S. E., Brown I. H., Holmes E. C., Taubenberger J. K. (2009). Different evolutionary trajectories of European avian-like and classical swine H1N1 influenza A viruses. J Virol 83, 5485–5494. [View Article][PubMed] [Google Scholar]
  10. Gamblin S. J., Haire L. F., Russell R. J., Stevens D. J., Xiao B., Ha Y., Vasisht N., Steinhauer D. A., Daniels R. S. et al. (2004). The structure and receptor binding properties of the 1918 influenza hemagglutinin. Science 303, 1838–1842. [View Article][PubMed] [Google Scholar]
  11. Glaser L., Stevens J., Zamarin D., Wilson I. A., García-Sastre A., Tumpey T. M., Basler C. F., Taubenberger J. K., Palese P. (2005). A single amino acid substitution in 1918 influenza virus hemagglutinin changes receptor binding specificity. J Virol 79, 11533–11536. [View Article][PubMed] [Google Scholar]
  12. 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. [View Article][PubMed] [Google Scholar]
  13. Hooper K. A., Bloom J. D. (2013). A mutant influenza virus that uses an N1 neuraminidase as the receptor-binding protein. J Virol 87, 12531–12540. [View Article][PubMed] [Google Scholar]
  14. Ilyushina N. A., Seiler J. P., Rehg J. E., Webster R. G., Govorkova E. A. (2010). Effect of neuraminidase inhibitor-resistant mutations on pathogenicity of clade 2.2 A/Turkey/15/06 (H5N1) influenza virus in ferrets. PLoS Pathog 6, e1000933. [View Article][PubMed] [Google Scholar]
  15. Jones J. C., Baranovich T., Marathe B. M., Danner A. F., Seiler J. P., Franks J., Govorkova E. A., Krauss S., Webster R. G. (2014). Risk assessment of H2N2 influenza viruses from the avian reservoir. J Virol 88, 1175–1188. [View Article][PubMed] [Google Scholar]
  16. Lednicky J. A., Croutch C. R., Lawrence S. J., Hamilton S. B., Daniels D. E., Astroff B. (2010). A nonlethal young domesticated ferret (Mustela putorius furo) model for studying pandemic influenza virus A/California/04/2009 (H1N1). Comp Med 60, 364–368.[PubMed] [Google Scholar]
  17. Lewis N. S., Anderson T. K., Kitikoon P., Skepner E., Burke D. F., Vincent A. L. (2014). Substitutions near the hemagglutinin receptor-binding site determine the antigenic evolution of influenza A H3N2 viruses in U.S. swine. J Virol 88, 4752–4763. [View Article][PubMed] [Google Scholar]
  18. Maher J. A., DeStefano J. (2004). The ferret: an animal model to study influenza virus. Lab Anim (NY) 33, 50–53. [View Article][PubMed] [Google Scholar]
  19. Matrosovich M. N., Gambaryan A. S. (2012). Solid-phase assays of receptor-binding specificity. Methods Mol Biol 865, 71–94. [View Article][PubMed] [Google Scholar]
  20. Matrosovich M., Tuzikov A., Bovin N., Gambaryan A., Klimov A., Castrucci M. R., Donatelli I., Kawaoka Y. (2000). Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J Virol 74, 8502–8512. [View Article][PubMed] [Google Scholar]
  21. Matrosovich M. N., Matrosovich T. Y., Gray T., Roberts N. A., Klenk H.-D. (2004). Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc Natl Acad Sci U S A 101, 4620–4624. [View Article][PubMed] [Google Scholar]
  22. Moreno A., Di Trani L., Faccini S., Vaccari G., Nigrelli D., Boniotti M. B., Falcone E., Boni A., Chiapponi C. et al. (2011). Novel H1N2 swine influenza reassortant strain in pigs derived from the pandemic H1N1/2009 virus. Vet Microbiol 149, 472–477. [View Article][PubMed] [Google Scholar]
  23. Munster V. J., de Wit E., van den Brand J. M. A., Herfst S., Schrauwen E. J. A., Bestebroer T. M., van de Vijver D., Boucher C. A., Koopmans M. et al. (2009). Pathogenesis and transmission of swine-origin 2009 A(H1N1) influenza virus in ferrets. Science 325, 481–483.[PubMed] [Google Scholar]
  24. Nobusawa E., Ishihara H., Morishita T., Sato K., Nakajima K. (2000). Change in receptor-binding specificity of recent human influenza A viruses (H3N2): a single amino acid change in hemagglutinin altered its recognition of sialyloligosaccharides. Virology 278, 587–596. [View Article][PubMed] [Google Scholar]
  25. Pascua P. N. Q., Song M.-S., Lee J. H., Baek Y. H., Kwon H. I., Park S.-J., Choi E. H., Lim G.-J., Lee O.-J. et al. (2012). Virulence and transmissibility of H1N2 influenza virus in ferrets imply the continuing threat of triple-reassortant swine viruses. Proc Natl Acad Sci U S A 109, 15900–15905. [View Article][PubMed] [Google Scholar]
  26. Pascua P. N. Q., Lim G. J., Kwon H. I., Park S. J., Kim E. H., Song M. S., Kim C. J., Choi Y. K. (2013). Emergence of H3N2pM-like and novel reassortant H3N1 swine viruses possessing segments derived from the A (H1N1)pdm09 influenza virus, Korea. Influenza Other Respi Viruses 7, 1283–1291. [View Article][PubMed] [Google Scholar]
  27. Pearce M. B., Jayaraman A., Pappas C., Belser J. A., Zeng H., Gustin K. M., Maines T. R., Sun X., Raman R. et al. (2012). Pathogenesis and transmission of swine origin A(H3N2)v influenza viruses in ferrets. Proc Natl Acad Sci U S A 109, 3944–3949. [View Article][PubMed] [Google Scholar]
  28. Potier M., Mameli L., Belisle M., Dallaire L., Melancon S. B. (1979). Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl-α-N-acetylneuraminate) substrate. Anal Biochem 94, 287–296. [CrossRef] [Google Scholar]
  29. Reed L. J., Muench H. (1938). A simple method of estimating fifty per cent endpoints. Am J Epidemiol 27, 493–497. [Google Scholar]
  30. Rogers G. N., Paulson J. C., Daniels R. S., Skehel J. J., Wilson I. A., Wiley D. C. (1983). Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity. Nature 304, 76–78. [View Article][PubMed] [Google Scholar]
  31. Schultz U., Fitch W. M., Ludwig S., Mandler J., Scholtissek C. (1991). Evolution of pig influenza viruses. Virology 183, 61–73. [View Article][PubMed] [Google Scholar]
  32. Smith G. J. D., Vijaykrishna D., Bahl J., Lycett S. J., Worobey M., Pybus O. G., Ma S. K., Cheung C. L., Raghwani J. et al. (2009). Origins and evolutionary genomics of the 2009 swine-origin H1N1 influenza A epidemic. Nature 459, 1122–1125. [View Article][PubMed] [Google Scholar]
  33. Starick E., Lange E., Fereidouni S., Bunzenthal C., Höveler R., Kuczka A., grosse Beilage E., Hamann H. P., Klingelhöfer I. et al. (2011). Reassorted pandemic (H1N1) 2009 influenza A virus discovered from pigs in Germany. J Gen Virol 92, 1184–1188. [View Article][PubMed] [Google Scholar]
  34. Starick E., Lange E., Grund C., Grosse Beilage E., Döhring S., Maas A., Noé T., Beer M., Harder T. C. (2012). Reassortants of pandemic influenza A virus H1N1/2009 and endemic porcine HxN2 viruses emerge in swine populations in Germany. J Gen Virol 93, 1658–1663. [View Article][PubMed] [Google Scholar]
  35. Stark G. V., Long J. P., Ortiz D. I., Gainey M., Carper B. A., Feng J., Miller S. M., Bigger J. E., Vela E. M. (2013). Clinical profiles associated with influenza disease in the ferret model. PLoS One 8, e58337. [View Article][PubMed] [Google Scholar]
  36. Stevens J., Blixt O., Glaser L., Taubenberger J. K., Palese P., Paulson J. C., Wilson I. A. (2006). Glycan microarray analysis of the hemagglutinins from modern and pandemic influenza viruses reveals different receptor specificities. J Mol Biol 355, 1143–1155. [View Article][PubMed] [Google Scholar]
  37. Takahashi T., Hashimoto A., Maruyama M., Ishida H., Kiso M., Kawaoka Y., Suzuki Y., Suzuki T. (2009). Identification of amino acid residues of influenza A virus H3 HA contributing to the recognition of molecular species of sialic acid. FEBS Lett 583, 3171–3174. [View Article][PubMed] [Google Scholar]
  38. Trebbien R., Bragstad K., Larsen L. E., Nielsen J., Bøtner A., Heegaard P. M. H., Fomsgaard A., Viuff B., Hjulsager C. K. (2013). Genetic and biological characterisation of an avian-like H1N2 swine influenza virus generated by reassortment of circulating avian-like H1N1 and H3N2 subtypes in Denmark. Virol J 10, 290. [View Article][PubMed] [Google Scholar]
  39. Tremblay D., Allard V., Doyon J. F., Bellehumeur C., Spearman J. G., Harel J., Gagnon C. A. (2011). Emergence of a new swine H3N2 and pandemic (H1N1) 2009 influenza A virus reassortant in two Canadian animal populations, mink and swine. J Clin Microbiol 49, 4386–4390. [View Article][PubMed] [Google Scholar]
  40. van Riel D., Munster V. J., de Wit E., Rimmelzwaan G. F., Fouchier R. A. M., Osterhaus A. D. M. E., Kuiken T. (2007). Human and avian influenza viruses target different cells in the lower respiratory tract of humans and other mammals. Am J Pathol 171, 1215–1223. [View Article][PubMed] [Google Scholar]
  41. Yen H.-L., Liang C.-H., Wu C.-Y., Forrest H. L., Ferguson A., Choy K.-T., Jones J., Wong D. D.-Y., Cheung P. P.-H. et al. (2011). Hemagglutinin-neuraminidase balance confers respiratory-droplet transmissibility of the pandemic H1N1 influenza virus in ferrets. Proc Natl Acad Sci U S A 108, 14264–14269. [View Article][PubMed] [Google Scholar]
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New reassortant and enzootic European swine influenza viruses transmit efficiently through direct contact in the ferret model
J. Gen. Virol. 96, 1603 (2015); https://doi.org/10.1099/vir.0.000094
/content/journal/jgv/10.1099/vir.0.000094
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