Differences in influenza virus receptors in chickens and ducks: Implications for interspecies transmission

Avian influenza viruses are considered to be key contributors to the emergence of human influenza pandemics. A major determinant of infection is the presence of virus receptors on susceptible cells to which the viral haemagglutinin is able to bind. Avian viruses preferentially bind to sialic acid α2,3-galactose (SAα2,3-Gal) linked receptors, whereas human strains bind to sialic acid α2,6-galactose (SAα2,6-Gal) linked receptors. While ducks are the major reservoir for influenza viruses, they are typically resistant to the effects of viral infection, in contrast to the frequently severe disease observed in chickens. In order to understand whether differences in receptors might contribute to this observation, we studied the distribution of influenza receptors in organs of ducks and chickens using lectin histochemistry with linkage specific lectins and receptor binding assays with swine and avian influenza viruses. Although the intestinal epithelial cells of both species expressed only SAα2,3-Gal receptors, we found widespread presence of both SAα2,6-Gal and SAα2,3-Gal receptors in many organs of both chickens and ducks. Co-expression of both receptors may allow infection of cells with both avian and human viruses and so present a route to genetic reassortment. There was a marked difference in the primary receptor type in the trachea of chickens and ducks. In chicken trachea, SAα2,6-Gal was the dominant receptor type whereas in ducks SAα2,3-Gal receptors were most abundant. This suggests that chickens could be more important as an intermediate host for the generation of influenza viruses with increased ability to bind to SAα2,6-Gal receptors and thus greater potential for infection of humans. Chicken tracheal and intestinal epithelial cells also expressed a broader range of SAα2,3-Gal receptors (both β(1-4)GlcNAc and β(1-3)GalNAc subtypes) in contrast to ducks, which suggests that they may be able to support infection with a broader range of avian influenza viruses.

[1]  S. More,et al.  Avian Influenza , 2008, Respirology.

[2]  J. Banks,et al.  Pathogenesis of highly pathogenic avian influenza A/turkey/Turkey/1/2005 H5N1 in Pekin ducks (Anas platyrhynchos) infected experimentally , 2008, Avian pathology : journal of the W.V.P.A.

[3]  Jiang Gu,et al.  Avian influenza receptor expression in H5N1‐infected and noninfected human tissues , 2008, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[4]  A. J. Bourne,et al.  Sialic acid receptor detection in the human respiratory tract: evidence for widespread distribution of potential binding sites for human and avian influenza viruses , 2007, Respiratory research.

[5]  Yoshihiro Kawaoka,et al.  [Influenza virus receptors in the human airway]. , 2006, Uirusu.

[6]  Yoshihiro Kawaoka,et al.  Avian flu: Influenza virus receptors in the human airway , 2006, Nature.

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

[8]  David E. Swayne,et al.  Characterization of the Reconstructed 1918 Spanish Influenza Pandemic Virus , 2005, Science.

[9]  Jeffery K. Taubenberger,et al.  Characterization of the 1918 influenza virus polymerase genes , 2005, Nature.

[10]  M. Perdue,et al.  Public Health Risk from Avian Influenza Viruses , 2005, Avian diseases.

[11]  Yoshihiro Kawaoka,et al.  Influenza: lessons from past pandemics, warnings from current incidents , 2005, Nature Reviews Microbiology.

[12]  H. Klenk,et al.  Human and avian influenza viruses target different cell types in cultures of human airway epithelium. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[13]  A. Varki,et al.  Human-specific Regulation of α2–6-linked Sialic Acids* , 2003, Journal of Biological Chemistry.

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

[15]  Niall Johnson,et al.  Updating the Accounts: Global Mortality of the 1918-1920 "Spanish" Influenza Pandemic , 2002, Bulletin of the history of medicine.

[16]  Toshihiro Ito Interspecies Transmission and Receptor Recognition of Influenza A Viruses , 2000, Microbiology and immunology.

[17]  Y. Kawaoka,et al.  Host-range barrier of influenza A viruses. , 2000, Veterinary microbiology.

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

[19]  R. Webster,et al.  Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus , 1998, The Lancet.

[20]  N. Cox,et al.  Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. , 1998, Science.

[21]  D. Swayne Pathobiology of H5N2 Mexican Avian Influenza Virus Infections of Chickens , 1997, Veterinary pathology.

[22]  Jeffery K. Taubenberger,et al.  Initial Genetic Characterization of the 1918 “Spanish” Influenza Virus , 1997, Science.

[23]  T. Irimura,et al.  Strong affinity of Maackia amurensis hemagglutinin (MAH) for sialic acid‐containing Ser/Thr‐linked carbohydrate chains of N‐terminal octapeptides from human glycophorin A , 1994, FEBS letters.

[24]  J. Paulson,et al.  Influenza virus strains selectively recognize sialyloligosaccharides on human respiratory epithelium; the role of the host cell in selection of hemagglutinin receptor specificity. , 1993, Virus research.

[25]  I. Goldstein,et al.  The elderberry (Sambucus nigra L.) bark lectin recognizes the Neu5Ac(alpha 2-6)Gal/GalNAc sequence. , 1987, The Journal of biological chemistry.

[26]  R. Webster,et al.  Differences Between Influenza Virus Receptors on Target Cells of Duck and Chicken and Receptor Specificity of the 1997 H5N1 Chicken and Human Influenza Viruses from Hong Kong , 2003, Avian diseases.

[27]  R. Webster,et al.  In £ uenza : interspecies transmission and emergence of new pandemics , 1997 .

[28]  INFLUENZA viruses. , 1952, Lancet.