Species and age related differences in the type and distribution of influenza virus receptors in different tissues of chickens, ducks and turkeys

We undertook one of the most detailed studies on the distribution of α2,3 sialic acid (SA)-galactose (gal) (avian type) and α2,6SA-gal (human type) receptors on different tissues of chickens, ducks and turkeys of varying age groups. On the tracheal epithelium, all 3 bird species expressed strong positive staining (80-90%) for α2,3SA-gal receptors in the 3 different age groups. In addition, a lesser amount of α2,6SA-gal receptors (30-90%) were observed with slight differences in distribution with age and species. The epithelium of the small and large intestine of turkeys and ducks showed negligible staining for α2,6SA-gal receptors whereas the large intestine consistently showed 40-70% positive staining for α2,3SA-gal receptors. In contrast, a greater amount of staining for α2,3SA-gal (50-80%) and α2,6SA-gal (20-50%) receptors were observed along the epithelium of small and large intestine of chickens. Kidney and esophagus sections from the 3 bird species also expressed both avian and human type receptors. In other tissues examined, brain, breast muscles, bursa, spleen, cecal tonsils and oviduct, human type receptors were absent. Though different viral and receptor components may play roles in successful viral replication and transmission, understanding the receptor types and distribution in different tissues of domestic birds might be good initial tool to understand host factors that promote successful influenza viral infection.

[1]  Y. Matsuoka,et al.  Duck influenza lacking evidence of disease signs and immune response , 1980, Infection and immunity.

[2]  M. Aymard,et al.  Disease in turkeys associated with H1N1 influenza virus following an outbreak of the disease in pigs , 1985, Veterinary Record.

[3]  Y. Guan,et al.  The Quest of Influenza A Viruses for New Hosts , 2003, Avian diseases.

[4]  Yoshihiro Kawaoka,et al.  Early Alterations of the Receptor-Binding Properties of H1, H2, and H3 Avian Influenza Virus Hemagglutinins after Their Introduction into Mammals , 2000, Journal of Virology.

[5]  H. Faillard,et al.  [Enzymatic effect of the influenza virus]. , 1955, Hoppe-Seyler's Zeitschrift fur physiologische Chemie.

[6]  R. Webster,et al.  Avian influenza viruses in Korean live poultry markets and their pathogenic potential. , 2005, Virology.

[7]  Yoshihiro Kawaoka,et al.  Molecular Basis for the Generation in Pigs of Influenza A Viruses with Pandemic Potential , 1998, Journal of Virology.

[8]  O. Fletcher,et al.  Comparative pathology of chickens experimentally inoculated with avian influenza viruses of low and high pathogenicity. , 1997, Avian diseases.

[9]  R. Webster,et al.  The Surface Glycoproteins of H5 Influenza Viruses Isolated from Humans, Chickens, and Wild Aquatic Birds Have Distinguishable Properties , 1999, Journal of Virology.

[10]  J. Paulson,et al.  Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. , 1983, Virology.

[11]  J. Mcclure,et al.  Lectin Histochemistry of Normal Human Lung , 2003, Journal of Molecular Histology.

[12]  S. Dunham,et al.  Differences in influenza virus receptors in chickens and ducks: Implications for interspecies transmission , 2009, Journal of molecular and genetic medicine : an international journal of biomedical research.

[13]  J. Paulson,et al.  Different cell-surface receptor determinants of antigenically similar influenza virus hemagglutinins. , 1981, The Journal of biological chemistry.

[14]  T. Tumpey,et al.  Characterization of a Highly Pathogenic H5N1 Avian Influenza A Virus Isolated from Duck Meat , 2002, Journal of Virology.

[15]  D. Stallknecht,et al.  Susceptibility of North American Ducks and Gulls to H5N1 Highly Pathogenic Avian Influenza Viruses , 2006, Emerging infectious diseases.

[16]  D. Suarez,et al.  Evaluation of chicken-origin (DF-1) and quail-origin (QT-6) fibroblast cell lines for replication of avian influenza viruses. , 2008, Journal of virological methods.

[17]  R. Manvell,et al.  Experimental assessment of the pathogenicity of eight avian influenza A viruses of H5 subtype for chickens, turkeys, ducks and quail. , 1986, Avian pathology : journal of the W.V.P.A.

[18]  G. Air,et al.  Evolving complexities of influenza virus and its receptors. , 2008, Trends in microbiology.

[19]  R. Webster,et al.  [Differences in receptor specificity between the influenza A viruses isolated from the duck, chicken, and human]. , 2002, Molekuliarnaia biologiia.

[20]  C. J. Randall,et al.  An outbreak of highly pathogenic avian influenza in turkeys in Great Britain in 1991 , 1993, Veterinary Record.

[21]  H. Yassine,et al.  Pathobiology of triple reassortant H3N2 influenza viruses in breeder turkeys and its potential implication for vaccine studies in turkeys. , 2009, Vaccine.

[22]  D. Pérez,et al.  Quail carry sialic acid receptors compatible with binding of avian and human influenza viruses. , 2006, Virology.

[23]  W. H. Allan,et al.  The pathogenicity of four avian influenza viruses for fowls, turkeys and ducks. , 1978, Research in veterinary science.

[24]  Y. Kawaoka,et al.  The quail and chicken intestine have sialyl-galactose sugar chains responsible for the binding of influenza A viruses to human type receptors. , 2007, Glycobiology.

[25]  R. Webster,et al.  Differences between influenza virus receptors on target cells of duck and chicken , 2002, Archives of Virology.

[26]  R. Webster,et al.  Water-bone transmission of influenza A viruses? , 1979, Intervirology.

[27]  R. Webster,et al.  Influenza: an emerging disease. , 1998, Emerging infectious diseases.

[28]  D. Swayne,et al.  Tissue tropism and replicative properties of waterfowl-origin influenza viruses in chickens. , 1995, Avian diseases.

[29]  N V Bovin,et al.  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). , 1997, Virology.

[30]  D. Swayne,et al.  Susceptibility of Laughing Gulls (Larus atricilla) to H5N1 and H5N3 Highly Pathogenic Avian Influenza Viruses , 2002, Avian diseases.

[31]  T. Tumpey,et al.  Characterization of Highly Pathogenic H5N1 Avian Influenza A Viruses Isolated from South Korea , 2005, Journal of Virology.

[32]  D. Swayne,et al.  Assessing pathogenicity potential of waterfowl-origin type A influenza viruses in chickens. , 1991, Avian diseases.

[33]  D J Alexander,et al.  A review of avian influenza in different bird species. , 2000, Veterinary microbiology.

[34]  F. Mutinelli,et al.  Pathologic Findings of Highly Pathogenic Avian Influenza Virus A/Duck/Vietnam/12/05 (H5N1) in Experimentally Infected Pekin Ducks, Based on Immunohistochemistry and In Situ Hybridization , 2007, Veterinary pathology.

[35]  D. Swayne,et al.  Varied Pathogenicity of a Hong Kong-origin H5N1 Avian Influenza Virus in Four Passerine Species and Budgerigars , 2003, Veterinary pathology.

[36]  J. Gelb,et al.  Virulence of Low Pathogenicity H7N2 Avian Influenza Viruses from the Delmarva Peninsula for Broiler and Leghorn Chickens and Turkeys , 2008, Avian diseases.

[37]  D. Swayne,et al.  Using Mean Infectious Dose of High- and Low-Pathogenicity Avian Influenza Viruses Originating from Wild Duck and Poultry as One Measure of Infectivity and Adaptation to Poultry , 2008, Avian diseases.