Skip to main content

Advertisement

SpringerLink
Log in

Human trachea primary epithelial cells express both sialyl(α2-3)Gal receptor for human parainfluenza virus type 1 and avian influenza viruses, and sialyl(α2-6)Gal receptor for human influenza viruses

  • Published:
Glycoconjugate Journal Aims and scope Submit manuscript

Abstract

We reported previously that the dominant receptors of influenza A and B viruses, and human and murine respiroviruses, were sialylglycoproteins and gangliosides containing monosialo-lactosamine type I-and II-residues, such as sialic acid-α2-3(6)-Galβ1-3(4)-GlcNAcβ1-. In addition, the Siaα2-3Gal linkage was predominantly recognized by avian and horse influenza viruses, and human parainfluenza virus type 1 (hPIV-1), whereas the Siaα2-6Gal linkage was mainly recognized by human influenza viruses (Paulson JC in “The Receptors'' [Conn M Ed] 2, 131–219 (1985); Suzuki Y, Prog Lipid Res 33, 429–57 (1994); Ito T, J Virol 73, 6743–51 (2000); Suzuki Y, J Virol 74, 11825–31 (2000); Suzuki T, J. Virol 75, 4604–4613 (2001); Suzuki Y, Biol. Pharm. Bull. 28, 399–408 (2005)). To clarify the distribution of influenza virus receptors on the human bronchial epithelium cell surface, we investigated a primary culture of normal human bronchial epithelial (NHBE) cells using two types of lectin (MAA and SNA), which recognize sialyl linkages (α2-3 and α2-6), using fluorescence-activated cell-sorting analysis. The results showed that both α2-3- and α2-6-linked Sias were expressed on the surface of primary human bronchial epithelial cells. The cells infected by hPIV-1 bound to MAA, confirming that cells targeted by hPIV-1 have α2-3-linked oligosaccharides. We also compared the ability of hPIV-1 and human influenza A virus to infect primary human bronchial epithelial cells pre-treated with Siaα2-3Gal-specific sialidase from Salmonella typhimurium. No difference was observed in the number of sialidase pre-treated and non-treated cells infected with human influenza A virus, which binds to Siaα2-6Gal-linked oligosaccharides. By contrast, the number of cells infected with hPIV-1 decreased significantly upon sialidase treatment. Thus, cultured NHBE cells showed both α2-3-linked Sias recognized by hPIV-1 and avian influenza virus receptors, and α2-6-linked Sias recognized by human influenza virus receptors.

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

Similar content being viewed by others

References

  1. Suzuki, Y., Ito, T., Suzuki, T., Holland, R.E., Chambers, T.M., Kiso, M., Ishida, H., Kawaoka, Y.: Sialic acid species as a determinant of the host range of influenza A viruses. J. Virol. 74, 11825–31 (2000)

    CAS  PubMed  Google Scholar 

  2. Ito, T., Nelson, J., Couceiro, S.S., Kelm, S., Baum, G., Krauss, S., Castrucci, M.R., Donatelli, I., Kida, H., Paulson, J.C., Webster, R.G., Kawaoka, Y.: Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J. Virol. 72, 7367–73 (1998)

    CAS  PubMed  Google Scholar 

  3. Rogers, G.N., Paulson, J.C.: Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology 127, 361–73 (1983)

    Article  CAS  PubMed  Google Scholar 

  4. Rogers, G.N., Pritchett, T.J., Lane, J.L., Paulson, J.C.: 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 (1983)

    Article  CAS  PubMed  Google Scholar 

  5. Connor, R.J., Kawaoka, Y., Webster, R.G., Paulson, J.C.: Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology 205, 17–23 (1994)

    Article  CAS  PubMed  Google Scholar 

  6. Baum, L.G., Paulson, J.C.: Sialyloligosaccharides of the respiratory epithelium in the selection of human influenza virus receptor specificity. Acta histochemica S(suppl. xl(s)) 35–8 (1990)

  7. Couceiro, J.N., Paulson, J.C., Baum, L.G.: Influenza virus strains selectively recognize sialyloligosaccharides on human respiratory epithelium; the role of the host cell in selection of hemagglutinin receptor specificity. Virus Research 29, 155–65 (1993)

    Article  CAS  PubMed  Google Scholar 

  8. Suzuki, T., Portner, A., Scroggs, R.A., Uchikawa, M., Koyama, N., Matsuo, K., Suzuki, Y., Takimoto, T.: Receptor specificities of human respiroviruses. J. Virol. 75, 4604–13 (2001)

    Article  CAS  PubMed  Google Scholar 

  9. Mercer, R.R., Russell, M.L., Roggli, V.L., Crapo, J.D.: Cell number and distribution in human and rat airways. Am. J. Respir. Cell. Mol. Biol. 10, 613–24 (1994)

    CAS  PubMed  Google Scholar 

  10. Gorman, W.L., Pridgen, C., Portner, A.: Glycosylation of the hemagglutinin- neuraminidase glycoprotein of human parainfluenza virus type 1 affects its functional but not its antigenic properties. Virology 183, 83–90 (1991)

    Article  CAS  PubMed  Google Scholar 

  11. Portner, A., Scroggs, R.A., Metzger, D.W.: Distinct functions of antigenic sites of the HN glycoprotein of Sendai virus. Virology 158, 61–8 (1987)

    Article  CAS  PubMed  Google Scholar 

  12. Suzuki, Y., Matsunaga, M., Matsumoto, M.: N-Acetylneura- minyllactosylceramide, GM3-NeuAc, a new influenza A virus receptor which mediates the adsorption-fusion process of viral infection. J. Biol. Chem. 260, 1362–5 (1985)

    CAS  PubMed  Google Scholar 

  13. Suzuki, T., Sometani, A., Yamazaki, Y., Horiike, G., Mizutani, Y., Masuda, H., Yamada, M., Tahara, H., Xu, G., Miyamoto, D., Oku, N., Okada, S., Kiso, M., Hasegawa, A., Ito, T., Kawaoka, Y., Suzuki, Y.: Sulphatide binds to human and animal influenza A viruses, and inhibits the viral infection. Biochem. J. 318, 389–93 (1996)

    CAS  PubMed  Google Scholar 

  14. Suzuki, Y., Nakao, T., Ito, T., Watanabe, N., Toda, Y., Xu, G.Y., Suzuki, T., Kobayashi, T., Kimura, Y., Yamada, A., Sugawara, K., Nishimura, H., Kitame, F., Nakamura, K., Deya, E., Kiso, M., Hasegawa, A.: Structural determination of gangliosides that bind to influenza A, B, and C viruses by an improved binding assay: strain-specific receptor epitopes in sialo-sugar chains. Virology 189, 121–31 (1992)

    Article  CAS  PubMed  Google Scholar 

  15. Shibuya, N., Goldstein, I.F., Broekaert, W.F., Nsimba-Lubake, M., Peeters, B., Peumans, W.J.: The elderberry (Sambucus nigra L.) bark lectin recognizes the NeuAc(α2,6)Gal/GalNac sequence. J. Biol. Chem. 262, 1596–601 (1987)

    CAS  PubMed  Google Scholar 

  16. Wang, W.C., Cummings, R.D.: The immobilized leukoagglutinins from the seeds of Maackia amurensis binds with high affinity to complex-type Asn-linked oligosaccharides containing terminal sialic acid linked α-2,3 linked to the penultimate galactose residues. J. Biol. Chem. 263, 4576–85 (1988)

    CAS  PubMed  Google Scholar 

  17. Hoyer, L.L., Roggentin, P., Schauer, R., Vimr, E.R.: Purification and properties of cloned Salmonella typhimurium LT2 sialidase with virus-typical kinetic preference for sialyl α2→3 linkages. J Biochem 110, 462–7 (1991)

    CAS  PubMed  Google Scholar 

  18. Ito, T., Suzuki, Y., Suzuki, T., Tanaka, A., Horimoto, T., Wells, K., Kida, H., Otsuki, K., Kiso, M., Ishida, H., Kawaoka, Y.: Recognition of N-glycolylneuraminic acid linked to galactose by the alpha2,3 linkage is associated with intestinal replication of influenza A virus in ducks. J. Virol. 73, 6743–51 (2000)

    Google Scholar 

  19. Ito, T., Suzuki, Y., Takada, A., Kawamoto, A., Otsuki, K., Masuda, H., Suzuki, T., Kida, H., Kawaoka, Y.: Differences in sialic acid-galactose linkages in the chicken egg amnion and allantois influence human influenza virus receptor specificity and variant selection. J. Virol. 71, 3357–62 (1997)

    CAS  PubMed  Google Scholar 

  20. Pyan-Poirier, K., Suzuki, Y., Bean, W.J., Kobasa, D., Takada, A., Ito, T., Kawaoka, Y.: Changes in H3 influenza A virus receptor specificity during replication in humans. Virus. Res. 56, 169–76 (1998)

    Google Scholar 

  21. Snyder, M.H., Clements, M.L., Borde, D.D., Maassab, H.F., Murphy, B.R.: Attenuation of wild-type human influenza A virus by acquisition of the PA polymerase and matrix protein genes of influenza A/Ann Arbor/6/60 cold-adapted donor virus. J. Clin. Microbiol. 22, 719–25 (1987)

    Google Scholar 

  22. Ito, T., Couceiro, J.N.S.S., Kelm, S., Baum, S., Krauss, S., Castrucci, M.R., Donatelli, I., Kida, H., Paulson, J.C., Webster, R.G., Kawaoka, Y.: Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J. Virol. 72, 7367–73 (1998)

    CAS  PubMed  Google Scholar 

  23. World Health Organization, Influenza activity, Morbid Mortal Wkly Rep. 46, 1204 (1997)

    Google Scholar 

  24. 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.: Characterization of an avian influenza A (H5N1) virus isolated from a child with a fatal respiratory illness. Science 279, 393–6 (1998)

    Article  CAS  PubMed  Google Scholar 

  25. Claas, E.C., Osterhaus, A.D., van Beek, R., De Jong, J.C., Rimmelzwaan, G.F., Senne, D.A., Krauss, S., Shortridge, K.F., Webster, R.G.: Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet 351, 472–77 (1998)

    Article  CAS  PubMed  Google Scholar 

  26. Cauthern, A.N., Swayne, D.E., Schultz-Cherry, S., Pergue, M.L., Suarez, D.L.: Continued circulation in China of highly pathogenic avian influenza viruses encoding the hemagglutinin gene associated with the 1997 H5N1 outbreak in poultry and humans. J. Virol. 74, 6592–99 (2000)

    Google Scholar 

  27. Guan, Y., Poon, L.L.M., Cheung, C.Y., Ellis, T.M., Lim, W., Lipatov, A.S., Chan, K.H., Sturm-Ramirez, K.M., Cheung, C.L., Leung, Y.H.C., Yuen, K.Y., Webster, R.G., Peiris, J.S.M.: H5N1 influenza: A protean pandemic threat. Proc. Natl. Acad. Sci. 101, 8156–61 (2004)

    CAS  PubMed  Google Scholar 

  28. Matrosovich, M., Zhou, N., Kawaoka, Y., Webster, R.G.: The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J. Virol. 73, 1146–55 (1999)

    CAS  PubMed  Google Scholar 

  29. Lipatov, A.S., Govorkova, E.A., Webby, R.J., Ozaki, H., Peiris, M., Guan, Y., Poon, L.: Webster RG (Minireview), Influenza: Emergence and control. J. Virol. 78, 8951–9, (2004)

    Article  CAS  PubMed  Google Scholar 

  30. Matrovich, M.N., Kraus, S., Webster, R.G.: H9N2 influenza A viruses from poultry in Asia have human virus-like receptor specificity. Virology 281, 156–62 (2001)

    Google Scholar 

  31. Saito, T., Lim, W., Suzuki, T., Suzuki, Y., Kida, H., Nishimura, S.-I., Tashiro, M.: Characterization of a human H9N2 influenza virus isolated in Hong Kong. Vaccine 20, 125–33 (2001)

    Article  CAS  PubMed  Google Scholar 

  32. Matrosovich, M.N., Matrosovich, T.Y., Gray, T., Roberts, N.A., Klenk, H.D.: Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc. Natl. Acad. Sci. 101, 4620–24 (2004)

    Article  CAS  PubMed  Google Scholar 

  33. Beare, A.S., Webster, R.G.: Replication of avian influenza viruses in humans. Arch. Virol. 119, 37–42 (1991)

    Article  CAS  PubMed  Google Scholar 

  34. Murphy, B.R., Hinshaw, V.S., Sly, D.L., London, W.T., Hosier, N.T., Wood, F.T., Webster, R.G., Chanock, R.M.: Virulence of avian influenza A viruses for squirrel monkeys. Infect. Immun. 37, 1119–26 (1982)

    CAS  PubMed  Google Scholar 

  35. Snyder, M.H., Buckler-White, A.J., London, W.T., Tierney, E.L., Murphy, B.R.: The avian influenza virus nucleoprotein gene and a specific constellation of avian and human virus polymerase genes each specify attenuation of avian-human influenza A/Pintail/79 reassortant viruses for monkeys. J. Virol. 61, 2857–63 (1987)

    CAS  PubMed  Google Scholar 

  36. Hinshaw, V.S., Webster, R.G., Naeve, C.W., Murphy, B.R.: Altered tissue tropism of human-avian reassortant influenza viruses. Virology 128, 260–3 (1983)

    Article  CAS  PubMed  Google Scholar 

  37. Kida, H., Yanagawa, R., Matsuoka, Y.: Duck influenza lacking evidence of disease signs and immune response. Infect Immun 30, 547–53 (1980)

    CAS  PubMed  Google Scholar 

  38. Webster, R.G., Yakhno, M., Hinshaw, V.S., Bean, W.J., Murti, K.G.: Intestinal influenza: replication and characterization of influenza viruses in ducks. Virology 842, 268–78 (1978)

    Google Scholar 

  39. Suzuki, Y.: (Review), Sialobiology of influenza – molecular mechanism of host range variation of influenza viruses. Biol. Pharm. Bull. submitted (2005)

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry,School of Pharmaceutical Sciences, University of Shizuoka, Shizuoka, 422-8526

    Toshihiro Kogure, Takashi Suzuki, Tadanobu Takahashi, Daisei Miyamoto, Kazuya I. P. J. Hidari, Chao-Tan Guo & Yasuo Suzuki

  2. CREST JST and COE Program in the 21st Century, Shizuoka, 422-8526

    Takashi Suzuki, Tadanobu Takahashi, Daisei Miyamoto, Kazuya I. P. J. Hidari, Chao-Tan Guo & Yasuo Suzuki

  3. Institute of Bioengineering, Zhejiang Academy of Medical Sciences, Hang Zhou, 310013, China

    Chao-Tan Guo

  4. Department of Veterinary Public Health, Faculty of Agriculture, Tottori University, Tottori, 680-8553

    Toshihiro Ito

  5. CREST JST; Division of Virology, Department of Microbiology and Immunology, Institute of Medical Science, University of Tokyo, Tokyo, 108-8639, Japan

    Yoshihiro Kawaoka

  6. Department of Pathobiological Sciences, University of Wisconsin, Madison, Wisconsin, 53706, USA

    Yoshihiro Kawaoka

  7. Department of Biochemistry,School of Pharmaceutical Sciences, University of Shizuoka, Shizuoka, 422-8526, Japan

    Yasuo Suzuki

Authors
  1. Toshihiro Kogure
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takashi Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tadanobu Takahashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daisei Miyamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kazuya I. P. J. Hidari
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chao-Tan Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Toshihiro Ito
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yoshihiro Kawaoka
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Yasuo Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yasuo Suzuki.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kogure, T., Suzuki, T., Takahashi, T. et al. Human trachea primary epithelial cells express both sialyl(α2-3)Gal receptor for human parainfluenza virus type 1 and avian influenza viruses, and sialyl(α2-6)Gal receptor for human influenza viruses. Glycoconj J 23, 101–106 (2006). https://doi.org/10.1007/s10719-006-5442-z

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10719-006-5442-z

Keywords

Search

Navigation