1887

Abstract

An avian-like H3N2 influenza A virus (IAV) has recently caused sporadic canine influenza outbreaks in China and Korea, but the molecular mechanisms involved in the interspecies transmission of H3N2 IAV from avian to canine species are not well understood. Sequence analysis showed that residue 222 in haemagglutinin (HA) is predominantly tryptophan (W) in the closely related avian H3N2 IAV, but was leucine (L) in canine H3N2 IAV. In this study, reassortant viruses rH3N2-222L (canine-like) and rH3N2-222W (avian-like) with HA mutation L222W were generated using reverse genetics to evaluate the significance of the L222W mutation on receptor binding and host tropism of H3N2 IAV. Compared with rH3N2-222W, rH3N2-222L grew more rapidly in MDCK cells and had significantly higher infectivity in primary canine tracheal epithelial cells. Tissue-binding assays demonstrated that rH3N2-222L had a preference for canine tracheal tissues rather avian tracheal tissues, whereas rH3N2-222W favoured slightly avian rather canine tracheal tissues. Glycan microarray analysis suggested both rH3N2-222L and rH3N2-222W bound preferentially to α2,3-linked sialic acids. However, the rH3N2-222W had more than twofold less binding affinity than rH3N2-222L to a set of glycans with Neu5Aca2–3Galb1–4(Fuca-)-like or Neu5Aca2–3Galb1–3(Fuca-)-like structures. These data suggest the W to L mutation at position 222 of the HA could facilitate infection of H3N2 IAV in dogs, possibly by increasing the binding affinities of the HA to specific receptors with Neu5Aca2–3Galb1–4(Fuca-) or Neu5Aca2–3Galb1–3(Fuca-)-like structures that are present in dogs.

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2013-12-01
2024-03-29
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References

  1. Bateman A. C., Busch M. G., Karasin A. I., Bovin N., Olsen C. W. 2008; Amino acid 226 in the hemagglutinin of H4N6 influenza virus determines binding affinity for alpha2,6-linked sialic acid and infectivity levels in primary swine and human respiratory epithelial cells. J Virol 82:8204–8209 [View Article][PubMed]
    [Google Scholar]
  2. Blixt O., Head S., Mondala T., Scanlan C., Huflejt M. E., Alvarez R., Bryan M. C., Fazio F., Calarese D. other authors 2004; Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc Natl Acad Sci U S A 101:17033–17038 [View Article][PubMed]
    [Google Scholar]
  3. Bochner B. S., Alvarez R. A., Mehta P., Bovin N. V., Blixt O., White J. R., Schnaar R. L. 2005; Glycan array screening reveals a candidate ligand for Siglec-8. J Biol Chem 280:4307–4312 [View Article][PubMed]
    [Google Scholar]
  4. Bradley K. C., Jones C. A., Tompkins S. M., Tripp R. A., Russell R. J., Gramer M. R., Heimburg-Molinaro J., Smith D. F., Cummings R. D., Steinhauer D. A. 2011a; Comparison of the receptor binding properties of contemporary swine isolates and early human pandemic H1N1 isolates (Novel 2009 H1N1). Virology 413:169–182 [View Article][PubMed]
    [Google Scholar]
  5. Bradley K. C., Galloway S. E., Lasanajak Y., Song X., Heimburg-Molinaro J., Yu H., Chen X., Talekar G. R., Smith D. F. other authors 2011b; Analysis of influenza virus hemagglutinin receptor binding mutants with limited receptor recognition properties and conditional replication characteristics. J Virol 85:12387–12398 [View Article][PubMed]
    [Google Scholar]
  6. Busch M. G., Bateman A. C., Landolt G. A., Karasin A. I., Brockman-Schneider R. A., Gern J. E., Suresh M., Olsen C. W. 2008; Identification of amino acids in the HA of H3 influenza viruses that determine infectivity levels in primary swine respiratory epithelial cells. Virus Res 133:269–279 [View Article][PubMed]
    [Google Scholar]
  7. Chen L. M., Rivailler P., Hossain J., Carney P., Balish A., Perry I., Davis C. T., Garten R., Shu B. other authors 2011; Receptor specificity of subtype H1 influenza A viruses isolated from swine and humans in the United States. Virology 412:401–410 [View Article][PubMed]
    [Google Scholar]
  8. Claas E. C. J., Osterhaus A. D. M. E., 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 [View Article][PubMed]
    [Google Scholar]
  9. Connor R. J., Kawaoka Y., Webster R. G., Paulson J. C. 1994; Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 205:17–23 [View Article][PubMed]
    [Google Scholar]
  10. Crawford P. C., Dubovi E. J., Castleman W. L., Stephenson I., Gibbs E. P., Chen L., Smith C., Hill R. C., Ferro P. other authors 2005; Transmission of equine influenza virus to dogs. Science 310:482–485 [View Article][PubMed]
    [Google Scholar]
  11. Gamblin S. J., Haire L. F., Russell R. J., Stevens D. J., Xiao B., Ha Y., Vasisht N., Steinhauer D. A., Daniels R. S. other authors 2004; The structure and receptor binding properties of the 1918 influenza hemagglutinin. Science 303:1838–1842 [View Article][PubMed]
    [Google Scholar]
  12. Gray T. E., Guzman K., Davis C. W., Abdullah L. H., Nettesheim P. 1996; Mucociliary differentiation of serially passaged normal human tracheobronchial epithelial cells. Am J Respir Cell Mol Biol 14:104–112 [View Article][PubMed]
    [Google Scholar]
  13. Ha Y., Stevens D. J., Skehel J. J., Wiley D. C. 2003; X-ray structure of the hemagglutinin of a potential H3 avian progenitor of the 1968 Hong Kong pandemic influenza virus. Virology 309:209–218 [View Article][PubMed]
    [Google Scholar]
  14. Hoelzer K., Murcia P. R., Baillie G. J., Wood J. L., Metzger S. M., Osterrieder N., Dubovi E. J., Holmes E. C., Parrish C. R. 2010; Intrahost evolutionary dynamics of canine influenza virus in naive and partially immune dogs. J Virol 84:5329–5335 [View Article][PubMed]
    [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 [View Article][PubMed]
    [Google Scholar]
  16. Horimoto T., Kawaoka Y. 2005; Influenza: lessons from past pandemics, warnings from current incidents. Nat Rev Microbiol 3:591–600 [View Article][PubMed]
    [Google Scholar]
  17. Ito T. 2000; Interspecies transmission and receptor recognition of influenza A viruses. Microbiol Immunol 44:423–430[PubMed] [CrossRef]
    [Google Scholar]
  18. Ito T., Suzuki Y., Mitnaul L., Vines A., Kida H., Kawaoka Y. 1997; Receptor specificity of influenza A viruses correlates with the agglutination of erythrocytes from different animal species. Virology 227:493–499 [View Article][PubMed]
    [Google Scholar]
  19. Ito T., Couceiro J. N. S. S., Kelm S., Baum L. G., Krauss S., Castrucci M. R., Donatelli I., Kida H., Paulson J. C. other authors 1998; Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J Virol 72:7367–7373[PubMed]
    [Google Scholar]
  20. Kumari K., Gulati S., Smith D. F., Gulati U., Cummings R. D., Air G. M. 2007; Receptor binding specificity of recent human H3N2 influenza viruses. Virol J 4:42 [View Article][PubMed]
    [Google Scholar]
  21. Lee C., Song D., Kang B., Kang D., Yoo J., Jung K., Na G., Lee K., Park B., Oh J. 2009; A serological survey of avian origin canine H3N2 influenza virus in dogs in Korea. Vet Microbiol 137:359–362 [View Article][PubMed]
    [Google Scholar]
  22. Li S., Shi Z., Jiao P., Zhang G., Zhong Z., Tian W., Long L.-P., Cai Z., Zhu X. other authors 2010; Avian-origin H3N2 canine influenza A viruses in Southern China. Infect Genet Evol 10:1286–1288 [View Article][PubMed]
    [Google Scholar]
  23. Liu J., Stevens D. J., Haire L. F., Walker P. A., Coombs P. J., Russell R. J., Gamblin S. J., Skehel J. J. 2009; Structures of receptor complexes formed by hemagglutinins from the Asian Influenza pandemic of 1957. Proc Natl Acad Sci U S A 106:17175–17180 [View Article][PubMed]
    [Google Scholar]
  24. Ma W., Kahn R. E., Richt J. A. 2008; The pig as a mixing vessel for influenza viruses: human and veterinary implications. J Mol Genet Med 3:158–166[PubMed]
    [Google Scholar]
  25. Masurel N., Ophof P., de Jong P. 1981; Antibody response to immunization with influenza A/USSR/77 (H1N1) virus in young individuals primed or unprimed for A/New Jersey/76 (H1N1) virus. J Hyg (Lond) 87:201–209 [View Article][PubMed]
    [Google Scholar]
  26. Meisner J., Szretter K. J., Bradley K. C., Langley W. A., Li Z. N., Lee B. J., Thoennes S., Martin J., Skehel J. J. other authors 2008; Infectivity studies of influenza virus hemagglutinin receptor binding site mutants in mice. J Virol 82:5079–5083 [View Article][PubMed]
    [Google Scholar]
  27. Myers K. P., Olsen C. W., Gray G. C. 2007; Cases of swine influenza in humans: a review of the literature. Clin Infect Dis 44:1084–1088 [View Article][PubMed]
    [Google Scholar]
  28. Nobusawa E., Nakajima K. 1988; Amino acid substitution at position 226 of the hemagglutinin molecule of influenza (H1N1) virus affects receptor binding activity but not fusion activity. Virology 167:8–14 [View Article][PubMed]
    [Google Scholar]
  29. Oshansky C. M., Pickens J. A., Bradley K. C., Jones L. P., Saavedra-Ebner G. M., Barber J. P., Crabtree J. M., Steinhauer D. A., Tompkins S. M., Tripp R. A. 2011; Avian influenza viruses infect primary human bronchial epithelial cells unconstrained by sialic acid α2,3 residues. PLoS ONE 6:e21183 [View Article][PubMed]
    [Google Scholar]
  30. Payungporn S., Crawford P. C., Kouo T. S., Chen L. M., Pompey J., Castleman W. L., Dubovi E. J., Katz J. M., Donis R. O. 2008; Influenza A virus (H3N8) in dogs with respiratory disease, Florida. Emerg Infect Dis 14:902–908 [View Article][PubMed]
    [Google Scholar]
  31. Quintana A. M., Hussey S. B., Burr E. C., Pecoraro H. L., Annis K. M., Rao S., Landolt G. A. 2011; Evaluation of infectivity of a canine lineage H3N8 influenza A virus in ponies and in primary equine respiratory epithelial cells. Am J Vet Res 72:1071–1078 [View Article][PubMed]
    [Google Scholar]
  32. Rogers G. N., D’Souza B. L. 1989; Receptor binding properties of human and animal H1 influenza virus isolates. Virology 173:317–322 [View Article][PubMed]
    [Google Scholar]
  33. Rogers G. N., Paulson J. C. 1983; Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 127:361–373 [View Article][PubMed]
    [Google Scholar]
  34. Rogers G. N., Pritchett T. J., Lane J. L., Paulson J. C. 1983; Differential sensitivity of human, avian, and equine influenza A viruses to a glycoprotein inhibitor of infection: selection of receptor specific variants. Virology 131:394–408 [View Article][PubMed]
    [Google Scholar]
  35. Scholtissek C., Bürger H., Kistner O., Shortridge K. F. 1985; The nucleoprotein as a possible major factor in determining host specificity of influenza H3N2 viruses. Virology 147:287–294 [View Article][PubMed]
    [Google Scholar]
  36. Schroth M. K., Grimm E., Frindt P., Galagan D. M., Konno S.-I., Love R., Gern J. E. 1999; Rhinovirus replication causes RANTES production in primary bronchial epithelial cells. Am J Respir Cell Mol Biol 20:1220–1228 [View Article][PubMed]
    [Google Scholar]
  37. Shen C.-I., Wang C.-H., Shen S.-C., Lee H.-C., Liao J.-W., Su H.-L. 2011; The infection of chicken tracheal epithelial cells with a H6N1 avian influenza virus. PLoS ONE 6:e18894 [View Article][PubMed]
    [Google Scholar]
  38. Shibeshi W., Abraham G., Kneuer C., Ellenberger C., Seeger J., Schoon H.-A., Ungemach F. R. 2008; Isolation and culture of primary equine tracheal epithelial cells. In Vitro Cell Dev Biol Anim 44:179–184 [View Article][PubMed]
    [Google Scholar]
  39. Shinde V., Bridges C. B., Uyeki T. M., Shu B., Balish A., Xu X., Lindstrom S., Gubareva L. V., Deyde V. other authors 2009; Triple-reassortant swine influenza A (H1) in humans in the United States, 2005-2009. N Engl J Med 360:2616–2625 [View Article][PubMed]
    [Google Scholar]
  40. Sime A., McKellar Q., Nolan A. 1997; Method for the growth of equine airway epithelial cells in culture. Res Vet Sci 62:30–33 [View Article][PubMed]
    [Google Scholar]
  41. Skehel J. J., Wiley D. C. 2000; Receptor binding and membrane fusion in virus entry: the influenza hemagglutinin. Annu Rev Biochem 69:531–569 [View Article][PubMed]
    [Google Scholar]
  42. 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]
  43. Song D., Kang B., Lee C., Jung K., Ha G., Kang D., Park S., Park B., Oh J. 2008; Transmission of avian influenza virus (H3N2) to dogs. Emerg Infect Dis 14:741–746 [View Article][PubMed]
    [Google Scholar]
  44. Song D., Lee C., Kang B., Jung K., Oh T., Kim H., Park B., Oh J. 2009; Experimental infection of dogs with avian-origin canine influenza A virus (H3N2). Emerg Infect Dis 15:56–58 [View Article][PubMed]
    [Google Scholar]
  45. Stephenson I., Wood J. M., Nicholson K. G., Zambon M. C. 2003; Sialic acid receptor specificity on erythrocytes affects detection of antibody to avian influenza haemagglutinin. J Med Virol 70:391–398 [View Article][PubMed]
    [Google Scholar]
  46. Stevens J., Blixt O., Tumpey T. M., Taubenberger J. K., Paulson J. C., Wilson I. A. 2006; Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 312:404–410 [View Article][PubMed]
    [Google Scholar]
  47. Stevens J., Blixt O., Chen L. M., Donis R. O., Paulson J. C., Wilson I. A. 2008; Recent avian H5N1 viruses exhibit increased propensity for acquiring human receptor specificity. J Mol Biol 381:1382–1394 [View Article][PubMed]
    [Google Scholar]
  48. van Riel D., Munster V. J., de Wit E., Rimmelzwaan G. F., Fouchier R. A. M., Osterhaus A. D. M. E., Kuiken T. 2006; H5N1 virus attachment to lower respiratory tract. Science 312:399 [View Article][PubMed]
    [Google Scholar]
  49. Varki A. 2001; N-glycolylneuraminic acid deficiency in humans. Biochimie 83:615–622 [View Article][PubMed]
    [Google Scholar]
  50. Vines A., Wells K., Matrosovich M., Castrucci M. R., Ito T., Kawaoka Y. 1998; The role of influenza A virus hemagglutinin residues 226 and 228 in receptor specificity and host range restriction. J Virol 72:7626–7631[PubMed]
    [Google Scholar]
  51. Viswanathan K., Chandrasekaran A., Srinivasan A., Raman R., Sasisekharan V., Sasisekharan R. 2010; Glycans as receptors for influenza pathogenesis. Glycoconj J 27:561–570 [View Article][PubMed]
    [Google Scholar]
  52. von Grotthuss M., Rychlewski L. 2006; Influenza mutation from equine to canine. Science 311:1241–1242 [View Article][PubMed]
    [Google Scholar]
  53. Wan H., Perez D. R. 2007; Amino acid 226 in the hemagglutinin of H9N2 influenza viruses determines cell tropism and replication in human airway epithelial cells. J Virol 81:5181–5191 [View Article][PubMed]
    [Google Scholar]
  54. 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[PubMed]
    [Google Scholar]
  55. Wu R., Yankaskas J., Cheng E., Knowles M. R., Boucher R. 1985; Growth and differentiation of human nasal epithelial cells in culture. Serum-free, hormone-supplemented medium and proteoglycan synthesis. Am Rev Respir Dis 132:311–320[PubMed]
    [Google Scholar]
  56. Xu Q., Wang W., Cheng X., Zengel J., Jin H. 2010; Influenza H1N1 A/Solomon Island/3/06 virus receptor binding specificity correlates with virus pathogenicity, antigenicity, and immunogenicity in ferrets. J Virol 84:4936–4945 [View Article][PubMed]
    [Google Scholar]
  57. Yoon K. J., Cooper V. L., Schwartz K. J., Harmon K. M., Kim W. I., Janke B. H., Strohbehn J., Butts D., Troutman J. 2005; Influenza virus infection in racing greyhounds. Emerg Infect Dis 11:1974–1976[PubMed] [CrossRef]
    [Google Scholar]
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