1887

Abstract

Ferrets have become the model animal of choice for influenza pathology and transmission experiments as they are permissive and susceptible to human influenza A viruses. However, inoculation of ferrets with mumps virus (MuV) did not lead to successful infections. We evaluated the use of highly differentiated ferret tracheal epithelium cell cultures, FTE, for predicting the potential of ferrets to support respiratory viral infections. FTE cultures supported productive replication of human influenza A and B viruses but not of MuV, whereas analogous cells generated from human airways supported replication of all three viruses. We propose that strategies using these cultures might serve as a method of triaging viruses and potentially reducing the use of ferrets in viral studies.

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2015-08-01
2024-03-28
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References

  1. Afzal M.A., Dussupt V., Minor P.D., Pipkin P.A., Fleck R., Hockley D.J., Stacey G.N. 2005; Assessment of mumps virus growth on various continuous cell lines by virological, immunological, molecular and morphological investigations. J Virol Methods 126:149–56 [CrossRef]
    [Google Scholar]
  2. Belser J.A., Katz J.M., Tumpey T.M. 2011; The ferret as a model organism to study influenza A virus infection. Dis Model Mech 4:575–579 [View Article][PubMed]
    [Google Scholar]
  3. Bodewes R., Morick D., de Mutsert G., Osinga N., Bestebroer T., van der Vliet S., Smits S.L., Kuiken T., Rimmelzwaan G.F., other authors. 2013; Recurring influenza B virus infections in seals. Emerg Infect Dis 19:511–512 [View Article][PubMed]
    [Google Scholar]
  4. Bossart K.N., Zhu Z., Middleton D., Klippel J., Crameri G., Bingham J., McEachern J.A., Green D., Hancock T.J., other authors. 2009; A neutralizing human monoclonal antibody protects against lethal disease in a new ferret model of acute nipah virus infection. PLoS Pathog 5:e1000642 [CrossRef]
    [Google Scholar]
  5. Brookes D.W., Miah S., Lackenby A., Hartgroves L., Barclay W.S. 2010; Pandemic H1N1 2009 influenza virus with the H275Y oseltamivir resistance neuraminidase mutation shows a small compromise in enzyme activity and viral fitness. J Antimicrob Chemother
    [Google Scholar]
  6. Coates H.V., Chanock R.M. 1962; Experimental infection with respiratory syncytial virus in several species of animals. Am J Hyg 76:302–312[PubMed]
    [Google Scholar]
  7. Elderfield R.A., Watson S.J., Godlee A., Adamson W.E., Thompson C.I., Dunning J., Fernandez-Alonso M., Blumenkrantz D., Hussell T. other authors 2014; Accumulation of human-adapting mutations during circulation of A(H1N1)pdm09 influenza in humans in the UK. J Virol
    [Google Scholar]
  8. Herlocher M.L., Elias S., Truscon R., Harrison S., Mindell D., Simon C., Monto aS. 2001; Ferrets as a transmission model for influenza: sequence changes in HA1 of type A (H3N2) virus. J Infect Dis 184:542–546 [CrossRef]
    [Google Scholar]
  9. Huang S.S.H., Banner D., Fang Y., Ng D.C.K., Kanagasabai T., Kelvin D.J., Kelvin A.A. 2011; Comparative analyses of pandemic H1N1 and seasonal H1N1, H3N2, and influenza B infections depict distinct clinical pictures in ferrets. PLoS One 6:e27512 [View Article][PubMed]
    [Google Scholar]
  10. Huang S.S.H., Banner D., Paquette S.G., Leon A.J., Kelvin A.A., Kelvin D.J. 2014; Pathogenic influenza B virus in the ferret model establishes lower respiratory tract infection. J Gen Virol 95:2127–2139 [View Article][PubMed]
    [Google Scholar]
  11. Jackson D., Cadman A., Zurcher T., Barclay W.S. 2002; A reverse genetics approach for recovery of recombinant influenza B viruses entirely from cDNA. J Virol 76:11744–11747 [CrossRef]
    [Google Scholar]
  12. Jia N., Barclay W.S., Roberts K., Yen H.-L., Chan R.W.Y., Lam A.K.Y., Air G., Peiris J.S.M., Dell A., other authors. 2014; Glycomic characterization of respiratory tract tissues of ferrets: implications for its use in influenza virus infection studies. J Biol Chem 289:28489–28504 [View Article][PubMed]
    [Google Scholar]
  13. Kim Y.H., Kim H.S., Cho S.H., Seo S.H. 2009; Influenza B virus causes milder pathogenesis and weaker inflammatory responses in ferrets than influenza A virus. Viral Immunol 22:423–430 [View Article][PubMed]
    [Google Scholar]
  14. Margine I., Krammer F. 2014; Animal models for influenza viruses: implications for universal vaccine development. Pathogens 3:845–874 [View Article][PubMed]
    [Google Scholar]
  15. Markwell M.A.K. 1991; New Frontiers Opened by the Exploration of Host Cell Receptors. In The Paramyxoviruses pp. 407–425 Edited by Kingsbury D. W. Boston, MA: Springer US; [View Article]
    [Google Scholar]
  16. Martina B.E.E., Haagmans B.L., Kuiken T., Fouchier R.A.M., Rimmelzwaan G.F., VanAmerongen G., Peiris J.S.M., Lim W., Osterhaus A.D.M.E. 2003; Virology: SARS virus infection of cats and ferrets. Nature 425:915 [View Article][PubMed]
    [Google Scholar]
  17. 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]
  18. Ohishi K., Ninomiya A., Kida H., Park C.-H., Maruyama T., Arai T., Katsumata E., Tobayama T., Boltunov A.N., other authors. 2002; Serological evidence of transmission of human influenza A and B viruses to Caspian seals (Phoca caspica). Microbiol Immunol 46:639–644 [View Article][PubMed]
    [Google Scholar]
  19. Osterhaus A.D., Rimmelzwaan G.F., Martina B.E., Bestebroer T.M., Fouchier R.A. 2000; Influenza B virus in seals. Science 288:1051–1053 [View Article][PubMed]
    [Google Scholar]
  20. Parker L., Gilliland S.M., Minor P., Schepelmann S. 2013; Assessment of the ferret as an in vivo model for mumps virus infection. J Gen Virol 94:1200–1205 [View Article][PubMed]
    [Google Scholar]
  21. Pillet S., Svitek N., von Messling V. 2009; Ferrets as a model for morbillivirus pathogenesis, complications, and vaccines. Curr Top Microbiol Immunol 330:73–87[PubMed]
    [Google Scholar]
  22. Ran Z., Shen H., Lang Y., Kolb E.A., Turan N., Zhu L., Ma J., Bawa B., Liu Q., other authors. 2015; Domestic pigs are susceptible to infection with influenza B viruses. J Virol 89:4818–4826 [View Article][PubMed]
    [Google Scholar]
  23. Roberts K.L., Shelton H., Scull M., Pickles R., Barclay W.S. 2011; Lack of transmission of a human influenza virus with avian receptor specificity between ferrets is not due to decreased virus shedding but rather a lower infectivity in vivo. J Gen Virol 92:1822–1831 [View Article][PubMed]
    [Google Scholar]
  24. Roberts K.L., Shelton H., Stilwell P., Barclay W.S. 2012; Transmission of a 2009 H1N1 pandemic influenza virus occurs before fever is detected, in the ferret model. PLoS One 7:e43303 [CrossRef]
    [Google Scholar]
  25. Thangavel R.R., Bouvier N.M. 2014; Animal models for influenza virus pathogenesis, transmission, and immunology. J Immunol Methods 410:60–79 [View Article][PubMed]
    [Google Scholar]
  26. Thompson C.I., Barclay W.S., Zambon M.C., Pickles R.J. 2006; Infection of human airway epithelium by human and avian strains of influenza a virus. J Virol 80:8060–8068 [View Article][PubMed]
    [Google Scholar]
  27. 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]
  28. Wang Y.F., Chang C.F., Chi C.Y., Wang H.C., Wang J.R., Su I.J. 2012; Characterization of glycan binding specificities of influenza B viruses with correlation with hemagglutinin genotypes and clinical features. J Med Virol 84:679–685 [View Article][PubMed]
    [Google Scholar]
  29. Xu P., Huang Z., Gao X., Michel F.J., Hirsch G., Hogan R.J., Sakamoto K., Ho W., Wu J., He B. 2013; Infection of mice, ferrets, and rhesus macaques with a clinical mumps virus isolate. J Virol 87:8158–8168 [View Article][PubMed]
    [Google Scholar]
  30. Zeng H., Goldsmith C.S., Maines T.R., Belser J.A., Gustin K.M., Pekosz A., Zaki S.R., Katz J.M., Tumpey T.M. 2013; Tropism and infectivity of influenza virus, including highly pathogenic avian H5N1 virus, in ferret tracheal differentiated primary epithelial cell cultures. J Virol 87:2597–2607 [View Article][PubMed]
    [Google Scholar]
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