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Genetic and phenotypic characterization of a low-pathogenicity avian influenza H11N9 virus

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Abstract

An H11N9 low-pathogenicity avian influenza virus, A/duck/WA/663/97, was isolated from a sick Mandarin duck kept in an outdoor bird exhibit. Genetic and phenotypic characterization of the virus suggested that it originated from free-flying birds, a concept supported by genetic similarity with waterfowl isolates from the same geographic area and time period. This duck-origin virus had genetic features typical of H11 and N9 viruses, including no neuraminidase stalk deletion, no differences in putative glycosylation sites in either surface protein, and no addition of basic amino acid residues at the hemagglutinin cleavage site compared to published sequences. It replicated in both avian and mammalian cells in vitro, and experimentally challenged chickens developed mild acute upper respiratory lesions but no clinical signs of disease. It elicited immune responses in chickens, resulting in seroconversion in all infected birds, although antibody titers remained low over the experimental period.

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References

  1. Abolnik C, Bisschop SP, Gerdes GH, Olivier AJ, Horner RF (2007) Phylogenetic analysis of low-pathogenicity avian influenza H6N2 viruses from chicken outbreaks (2001–2005) suggest that they are reassortants of historic ostrich low-pathogenicity avian influenza H9N2 and H6N8 viruses. Avian Dis 51:279–284

    Article  PubMed  CAS  Google Scholar 

  2. Alexander DJ (2000) A review of avian influenza in different bird species. Vet Microbiol 74:3–13

    Article  PubMed  CAS  Google Scholar 

  3. Chen H, Li Y, Li Z, Shi J, Shinya K, Deng G, Qi Q, Tian G, Fan S, Zhao H, Sun Y, Kawaoka Y (2006) Properties and dissemination of H5N1 viruses isolated during an influenza outbreak in migratory waterfowl in western China. J Virol 80:5976–5983

    Article  PubMed  CAS  Google Scholar 

  4. Cowen BS, Braune MO (1988) The propagation of avian viruses in a continuous cell line (QT35) of Japanese quail origin. Avian Dis 32:282–297

    Article  PubMed  CAS  Google Scholar 

  5. Di Trani L, Bedini B, Cordioli P, Muscillo M, Vignolo E, Moreno A, Tollis M (2004) Molecular characterization of low pathogenicity H7N3 avian influenza viruses isolated in Italy. Avian Dis 48:376–383

    Article  PubMed  CAS  Google Scholar 

  6. Fouchier RA, Munster V, Wallensten A, Bestebroer TM, Herfst S, Smith D, Rimmelzwaan GF, Olsen B, Osterhaus AD (2005) Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol 79:2814–2822

    Article  PubMed  CAS  Google Scholar 

  7. Gambaryan AS, Tuzikov AB, Piskarev VE, Yamnikova SS, Lvov DK, Robertson JS, Bovin NV, Matrosovich MN (1997) Specification of receptor-binding phenotypes of influenza virus isolates from different hosts using synthetic sialylglycopolymers: non-egg-adapted human H1 and H3 influenza A and influenza B viruses share a common high binding affinity for 6′-sialyl(N-acetyllactosamine). Virology 232:345–350

    Article  PubMed  CAS  Google Scholar 

  8. Gambaryan AS, Karasin AI, Tuzikov AB, Chinarev AA, Pazynina GV, Bovin NV, Matrosovich MN, Olsen CW, Klimov AI (2005) Receptor-binding properties of swine influenza viruses isolated and propagated in MDCK cells. Virus Res 114:15–22

    Article  PubMed  CAS  Google Scholar 

  9. Gill JS, Webby R, Gilchrist MJ, Gray GC (2006) Avian influenza among waterfowl hunters and wildlife professionals. Emerg Infect Dis 12:1284–1286

    PubMed  Google Scholar 

  10. Hatta M, Gao P, Halfmann P, Kawaoka Y (2001) Molecular basis for high virulence of Hong Kong H5N1 influenza A viruses. Science 293:1840–1842

    Article  PubMed  CAS  Google Scholar 

  11. Hinshaw VS, Air GM, Gibbs AJ, Graves L, Prescott B, Karunakaran D (1982) Antigenic and genetic characterization of a novel hemagglutinin subtype of influenza A viruses from gulls. J Virol 42:865–872

    PubMed  CAS  Google Scholar 

  12. Hoffmann E, Stech J, Guan Y, Webster RG, Perez DR (2001) Universal primer set for the full-length amplification of all influenza A viruses. Arch Virol 146:2275–2289

    Article  PubMed  CAS  Google Scholar 

  13. Jones YL, Swayne DE (2004) Comparative pathobiology of low and high pathogenicity H7N3 Chilean avian influenza viruses in chickens. Avian Dis 48:119–128

    Article  PubMed  Google Scholar 

  14. Kawaoka Y, Yamnikova S, Chambers TM, Lvov DK, Webster RG (1990) Molecular characterization of a new hemagglutinin, subtype H14, of influenza A virus. Virology 179:759–767

    Article  PubMed  CAS  Google Scholar 

  15. Levy AM, Gilad O, Xia L, Izumiya Y, Choi J, Tsalenko A, Yakhini Z, Witter R, Lee L, Cardona CJ, Kung HJ (2005) Marek’s disease virus Meq transforms chicken cells via the v-Jun transcriptional cascade: a converging transforming pathway for avian oncoviruses. Proc Natl Acad Sci USA 102:14831–14836

    Article  PubMed  CAS  Google Scholar 

  16. Liu J, Xiao H, Lei F, Zhu Q, Qin K, Zhang XW, Zhang XL, Zhao D, Wang G, Feng Y, Ma J, Liu W, Wang J, Gao GF (2005) Highly pathogenic H5N1 influenza virus infection in migratory birds. Science 309:1206

    Google Scholar 

  17. Macken C, Lu H, Goodman J, Boykin L (2001) The value of a database in surveillance and vaccine selection. In: A.D.M.E. Osterhaus NCAWH (ed) Options for the control of influenza IV.Elsevier, Amsterdam, pp 103–106

  18. Matrosovich MN, Gambaryan AS, Teneberg S, Piskarev VE, Yamnikova SS, Lvov DK, Robertson JS, Karlsson KA (1997) Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the HA receptor-binding site. Virology 233:224–234

    Article  PubMed  CAS  Google Scholar 

  19. McCracken C (2006) The influenza sequence database. Los Alamos National Laboratory

  20. Mo IP, Brugh M, Fletcher OJ, Rowland GN, Swayne DE (1997) Comparative pathology of chickens experimentally inoculated with avian influenza viruses of low and high pathogenicity. Avian Dis 41:125–136

    Article  PubMed  CAS  Google Scholar 

  21. Myers KP, Setterquist SF, Capuano AW, Gray GC (2007) Infection due to 3 avian influenza subtypes in United States veterinarians. Clin Infect Dis 45:4–9

    Article  PubMed  Google Scholar 

  22. Nobusawa E, Aoyama T, Kato H, Suzuki Y, Tateno Y, Nakajima K (1991) Comparison of complete amino acid sequences and receptor-binding properties among 13 serotypes of hemagglutinins of influenza A viruses. Virology 182:475–485

    Article  PubMed  CAS  Google Scholar 

  23. Palmer D, Coleman M, Dowdle W, Schild G (1975) Advanced laboratory techniques for influenza diagnosis. US Department of Health, Education, and Warefare, Immunology Series No. 6

  24. Peiris JS, de Jong MD, Guan Y (2007) Avian influenza virus (H5N1): a threat to human health. Clin Microbiol Rev 20:243–267

    Article  PubMed  Google Scholar 

  25. Rath NC, Parcells MS, Xie H, Santin E (2003) Characterization of a spontaneously transformed chicken mononuclear cell line. Vet Immunol Immunopathol 96:93–104

    Article  PubMed  CAS  Google Scholar 

  26. Reid AH, Janczewski TA, Lourens RM, Elliot AJ, Daniels RS, Berry CL, Oxford JS, Taubenberger JK (2003) 1918 influenza pandemic caused by highly conserved viruses with two receptor-binding variants. Emerg Infect Dis 9:1249–1253

    PubMed  Google Scholar 

  27. Rohm C, Zhou N, Suss J, Mackenzie J, Webster RG (1996) Characterization of a novel influenza hemagglutinin, H15: criteria for determination of influenza A subtypes. Virology 217:508–516

    Article  PubMed  CAS  Google Scholar 

  28. Subbarao K, Klimov A, Katz J, Regnery H, Lim W, Hall H, Perdue M, Swayne D, Bender C, Huang J, Hemphill M, Rowe T, Shaw M, Xu X, Fukuda K, Cox N (1998) Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279:393–396

    Article  PubMed  CAS  Google Scholar 

  29. Swayne DE, Perdue ML, Garcia M, Rivera-Cruz E, Brugh M (1997) Pathogenicity and diagnosis of H5N2 Mexican avian influenza viruses in chickens. Avian Dis 41:335–346

    Article  PubMed  CAS  Google Scholar 

  30. Swayne DE (2007) Understanding the complex pathobiology of high pathogenicity avian influenza viruses in birds. Avian Dis 51:242–249

    Article  PubMed  Google Scholar 

  31. Tumpey TM, Kapczynski DR, Swayne DE (2004) Comparative susceptibility of chickens and turkeys to avian influenza A H7N2 virus infection and protective efficacy of a commercial avian influenza H7N2 virus vaccine. Avian Dis 48:167–176

    Article  PubMed  Google Scholar 

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Acknowledgments

This project is supported by funds from the Center for Food Animal Health at the University of California, Davis. Drs Li, Xing, Woolcock and Cardona would like to express their heartfelt appreciation to Nichole L. Anchell, Nguyet Dao, and Phuong Dao for their expert technical support.

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Correspondence to Jinling Li.

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Li, J., Cardona, C.J., Xing, Z. et al. Genetic and phenotypic characterization of a low-pathogenicity avian influenza H11N9 virus. Arch Virol 153, 1899–1908 (2008). https://doi.org/10.1007/s00705-008-0217-4

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  • DOI: https://doi.org/10.1007/s00705-008-0217-4

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