Skip to main content
SpringerLink
Log in

Serial passage in ducks of a low-pathogenic avian influenza virus isolated from a chicken reveals a high mutation rate in the hemagglutinin that is likely due to selection in the host

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

An Erratum to this article was published on 02 April 2016

Abstract

A comparative study of the ability of three low-pathogenic avian influenza virus (LPAIV) isolates to be transmitted from duck to duck was performed. Pekin ducks were inoculated with two LPAIV isolates from chickens (A/Ck/PA/13609/93 [H5N2], H5N2-Ck; A/Ck/TX/167280-4/02 [H5N3], H5N3-Ck) and one isolate from a wild bird (A/Mute Swan/ MI/451072/06 [H5N1], H5N1-WB). During the establishment of the passage model, only two viruses (H5N1, H5N2) were able to be transmitted from duck to duck. Transmission of these isolates was dependent on the inoculation dose and route of infection. Analysis of swab samples taken from ducks revealed that the wild-bird isolate, H5N1-WB, was primarily shed via the cloacal route. The chicken isolate, H5N2-Ck, was isolated from cloacal as well as oro-pharyngeal swabs. Analysis of the amino acid sequences of the viral surface glycoproteins showed that the hemagglutinin (HA) of the H5N2-Ck isolate was under a stronger evolutionary pressure than the HA of the H5N1-WB isolate, as indicated by the presence of a larger number of amino acid changes observed during passage. The neuraminidase (NA) of both viruses showed either no (in the case of H5N1-WB) or very few amino acid changes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  1. Achenbach JE, Bowen RA (2011) Transmission of avian influenza A viruses among species in an artificial barnyard. PLoS One 6(3):e17643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Banks J, Speidel ES, Moore E, Plowright L, Piccirillo A, Capua I, Cordioli P, Fioretti A, Alexander DJ (2001) Changes in the haemagglutinin and the neuraminidase genes prior to the emergence of highly pathogenic H7N1 avian influenza viruses in Italy. Arch Virol 146:963–973

    Article  CAS  PubMed  Google Scholar 

  3. Bosch FX, Orlich M, Klenk H-D, Rott R (1979) The structure of the hemagglutinin, a determinant for the pathogenicity of influenza viruses. Virology 95:197–207

    Article  CAS  PubMed  Google Scholar 

  4. Campitelli L, Mogavero E, De Marco MA, Delogu M, Puzelli S, Frezza F, Facchini M, Chiapponi C, Foni E, Cordioli P, Webby R, Barigazzi G, Webster RG, Donatelli I (2004) Interspecies transmission of an H7N3 influenza virus from wild birds to intensively reared domestic poultry in Italy. Virology 323:24–36

    Article  CAS  PubMed  Google Scholar 

  5. Dlugolenski D, Jones L, Saavedra G, Tompkins SM, Tripp RA, Mundt E (2011) Passage of low-pathogenic avian influenza (LPAI) viruses mediates rapid genetic adaptation of a wild-bird isolate in poultry. Arch Virol 156:565–576

    Article  CAS  PubMed  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  CAS  PubMed  PubMed Central  Google Scholar 

  7. Gay L, Mundt E (2010) Testing of a new disinfectant process for poultry viruses. Avian Dis 54(1 Suppl):763–767

    Article  PubMed  Google Scholar 

  8. Gohrbandt S, Veits J, Breithaupt A, Hundt J, Teifke JP, Stech O, Mettenleiter TC, Stech J (2011) H9 avian influenza reassortant with engineered polybasic cleavage site displays a highly pathogenic phenotype in chicken. J Gen Virol 92:1843–1853

    Article  CAS  PubMed  Google Scholar 

  9. Ha Y, Stevens DJ, Skehel JJ, Wiley DC (2002) H5 avian and H9 swine influenza virus haemagglutinin structures: possible origin of influenza subtypes. EMBO J 21:865–875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Hoffmann TW, Munier S, Larcher T, Soubieux D, Ledevin M, Esnault E, Tourdes A, Croville G, Guérin JL, Quéré P, Volmer R, Naffakh N, Marc D (2012) Length variations in the NA stalk of an H7N1 influenza virus have opposite effects on viral excretion in chickens and ducks. J Virol 86:584–588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. 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  CAS  PubMed  Google Scholar 

  13. Lee CW, Swayne DE, Linares JA, Senne DA, Suarez DL (2005) H5N2 avian influenza outbreak in Texas in 2004: the first highly pathogenic strain in the United States in 20 years? J Virol 79:11412–11421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Li SQ, Orlich M, Rott R (1990) Generation of seal influenza virus variants pathogenic for chickens, because of hemagglutinin cleavage site changes. J Virol 64:3297–3303

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Monteith HD, Shannon EE, Derbyshire JB (1986) The inactivation of a bovine enterovirus and a bovine parvovirus in cattle manure by anaerobic digestion, heat treatment, gamma irradiation, ensilage and composting. J Hyg 97:175–184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Mundt E, Gay L, Jones L, Saavedra G, Tompkins SM, Tripp RA (2009) Replication and pathogenesis associated with H5N1, H5N2, and H5N3 low-pathogenic avian influenza virus infection in chickens and ducks. Arch Virol 154:1241–1248

    Article  CAS  PubMed  Google Scholar 

  17. OIE, 2006 (http://www.oie.int/eng/normes/mmanual/A_00037.htm)

  18. Pantin-Jackwood MJ, Miller PJ, Spackman E, Swayne D, Susta L, Costa-Hurtado M, Suarez D (2014) Role of poultry in the spread of novel H7N9 influenza virus in China. J Virol 88:5381–5390

    Article  PubMed  PubMed Central  Google Scholar 

  19. Pillai SP, Pantin-Jackwood M, Suarez DL, Saif YM, Lee CW (2010) Pathobiological characterization of low-pathogenicity H5 avian influenza viruses of diverse origins in chickens, ducks and turkeys. Arch Virol 155:1439–1451

    Article  CAS  PubMed  Google Scholar 

  20. Reed LJ, Muench H (1938) A simple method of estimating fifty per cent endpoints. Am J Epidem 27:493–497

    Google Scholar 

  21. 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  CAS  PubMed  Google Scholar 

  22. Shinya K, Makino A, Hatta M, Watanabe S, Kim JH, Kawaoka Y (2010) A mutation in H5 haemagglutinin that conferred human receptor recognition is not maintained stably during duck passage. J Gen Virol 91:1461–1463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Slemons RD, Easterday BC (1977) Type-A influenza viruses in the feces of migratory waterfowl. J Am Vet Med Assoc 171:947–948

    CAS  PubMed  Google Scholar 

  24. Slemons RD, Johnson DC, Osborn JS, Hayes F (1974) Type-A influenza viruses isolated from wild free-flying ducks in California. Avian Dis 18:119–124

    Article  CAS  PubMed  Google Scholar 

  25. Sorrell EM, Perez DR (2007) Adaptation of influenza A/Mallard/Potsdam/178-4/83 H2N2 virus in Japanese quail leads to infection and transmission in chickens. Avian Dis 51(1 Suppl):264–268

    Article  CAS  PubMed  Google Scholar 

  26. Sorrell EM, Song H, Pena L, Perez DR (2010) A 27-amino-acid deletion in the neuraminidase stalk supports replication of an avian H2N2 influenza A virus in the respiratory tract of chickens. J Virol 84:11831–11840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Spackman E, Gelb J Jr, Preskenis LA, Ladman BS, Pope CR, Pantin-Jackwood MJ, McKinley ET (2010) The pathogenesis of low pathogenicity H7 avian influenza viruses in chickens, ducks and turkeys. Virol J 19(7):331

    Article  Google Scholar 

  28. Spackman E, Senne DA, Myers TJ, Bulaga LL, Garber LP, Perdue ML, Lohman K, Daum LT, Suarez DL (2002) Development of a Real-Time Reverse Transcriptase PCR Assay for Type A Influenza Virus and the Avian H5 and H7 Hemagglutinin Subtypes. J Clin Microbiol 40:3256–3260

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Spackman E, Swayne DE, Suarez DL, Senne DA, Pedersen JC, Killian ML, Pasick J, Handel K, Pillai SP, Lee CW, Stallknecht D, Slemons R, Ip HS, Deliberto T (2007) Characterization of Low-Pathogenicity H5N1 Avian Influenza Viruses from North America. J Virol 81:11612–11619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Stallknecht DE, Shane SM (1988) Host range of avian influenza virus in free-living birds. Vet Res Commun 12:125–141

    Article  CAS  PubMed  Google Scholar 

  31. Stech O, Veits J, Weber S, Deckers D, Schröer D, Vahlenkamp TW, Breithaupt A, Teifke J, Mettenleiter TC, Stech J (2009) Acquisition of a polybasic hemagglutinin cleavage site by a low-pathogenic avian influenza virus is not sufficient for immediate transformation into a highly pathogenic strain. J Virol 83:5864–5868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Stevens J, Blixt O, Tumpey TM, Taubenberger JK, Paulson JC, Wilson IA (2006) Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science 312:404–410

    Article  CAS  PubMed  Google Scholar 

  33. Tong S, Li Y, Rivailler P, Conrardy C, Castillo DA, Chen LM, Recuenco S, Ellison JA, Davis CT, York IA, Turmelle AS, Moran D, Rogers S, Shi M, Tao Y, Weil MR, Tang K, Rowe LA, Sammons S, Xu X, Frace M, Lindblade KA, Cox NJ, Anderson LJ, Rupprecht CE, Donis RO (2012) A distinct lineage of influenza A virus from bats. Proc Natl Acad Sci USA 109:4269–4274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Tong S, Zhu X, Li Y, Shi M, Zhang J, Bourgeois M, Yang H, Chen X, Recuenco S, Gomez J, Chen LM, Johnson A, Tao Y, Dreyfus C, Yu W, McBride R, Carney PJ, Gilbert AT, Chang J, Guo Z, Davis CT, Paulson JC, Stevens J, Rupprecht CE, Holmes EC, Wilson IA, Donis RO (2013) New world bats harbor diverse influenza A viruses. PLoS Pathog 9:e1003657

    Article  PubMed  PubMed Central  Google Scholar 

  35. Tsan-Yuk Lam T, Wang J, Shen Y, Zhou B, Duan L, Cheung C-L, Ma C, Leung C, Chen X, Li L, Hong W, Chai Y, Zhou L, Liang H, Ou Z, Liu Y, Faroogui A, Klevin D, Poon LL, Smith DK, Pybus OG, Leung GM, Shu Y, Webster RG, Webby RJ, Peiris JS, Rambaut A, Zhu H, Guan Y (2013) The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature 502:241–244

    Article  Google Scholar 

  36. Veits J, Weber S, Stech O, Breithaupt A, Gräber M, Gohrbandt S, Bogs J, Hundt J, Teifke JP, Mettenleiter TC, Stech J (2012) Avian influenza virus hemagglutinins H2, H4, H8, and H14 support a highly pathogenic phenotype. Proc Natl Acad Sci USA 109:2579–2584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y (1992) Evolution and ecology of influenza A viruses. Microbiol Rev 56:152–179

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Webster RG, Rott R (1987) Influenza virus A pathogenicity: the pivotal role of hemagglutinin. Cell 50:665–666

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Population Health, Poultry Diagnostic and Research Center, University of Georgia, Athens, 30603, GA, USA

    Callie Ridenour, Susan M. Williams & Egbert Mundt

  2. Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, 30603, GA, USA

    Callie Ridenour, Les Jones, S. Mark Tompkins & Ralph A. Tripp

Authors
  1. Callie Ridenour
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Susan M. Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Les Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. Mark Tompkins
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ralph A. Tripp
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Egbert Mundt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Egbert Mundt.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ridenour, C., Williams, S.M., Jones, L. et al. Serial passage in ducks of a low-pathogenic avian influenza virus isolated from a chicken reveals a high mutation rate in the hemagglutinin that is likely due to selection in the host. Arch Virol 160, 2455–2470 (2015). https://doi.org/10.1007/s00705-015-2504-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-015-2504-1

Keywords

Search

Navigation