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Transmission of Avian Influenza Viruses to Humans: Viral Receptor Specificity and Distribution in Human Airways

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Emerging Infections in Asia
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Direct transmission of highly pathogenic avian influenza (HPAI) viruses to humans was not considered a major risk prior to 1997. In 1997, however, H5N1 HPAI viruses were transmitted to humans in Hong Kong. Six of 18 infected individuals died, marking the first fatal infection of humans with wholly avian influenza viruses (Claas et al., 1998a,b; Subbarao & Shaw, 2000). Since then, H5N1 HPAI viruses have spread throughout southeast Asia and recently into Europe and Africa. To date, more than 200 individuals have been infected and about half have succumbed to the infection (World Health Organization, 2006). Despite the continued transmission of H5N1 HPAI viruses to humans, these viruses have not yet acquired the ability to spread efficiently among humans. Here, we discuss the factors that lead to human infections with H5N1 HPAI viruses as they relate to the binding of the virus to its cellular receptor.

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References

  • Amonsin, A., Payungporn, S., Theamboonlers, A., Thanawongnuwech, R., Suradhat, S., Pariyothorn, N., Tantilertcharoen, R., Damrongwantanapokin, S., Buranathai, C., Chaisingh, A., Songserm, T., & Poovorawan, Y. (2006). Genetic characterization of H5N1 influenza A viruses isolated from zoo tigers in Thailand. Virology, 344, 480–491.

    Article  PubMed  CAS  Google Scholar 

  • Baum, L.G., & Paulson, J.C. (1990). Sialyloligosaccharides of the respiratory epithelium in the selection of human influenza virus receptor specificity. Acta Histochem., 40, 35–38.

    CAS  Google Scholar 

  • Butler, D. (2006a). Alarms ring over bird flu mutations. Nature, 439, 248–249.

    Article  PubMed  CAS  Google Scholar 

  • Butler, D. (2006b). Family tragedy spotlights flu mutations. Nature, 442, 114–115.

    Article  PubMed  CAS  Google Scholar 

  • Claas, E.C., de Jong, D.C., van Reek, B.R., Rimmelzwaan, G.F., & Osterhaus, A.D. (1998a). Human influenza virus A/HongKong/156/97 (H5N1) infection. Vaccine, 16, 977–978.

    Article  PubMed  CAS  Google Scholar 

  • Claas, E.C., Osterhaus, A.D., van Reek, B.R., De Jong, J.C., Rimmelzwaan, G.F., Senne, D.A., Krauss, S., Shortridge, K.F., & Webster, R.G. (1998b). Human influenza A H5N1 virus related to a highly pathogenic avian influenza virus. Lancet, 351, 472–477.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Duksin, D., & Bornstein, P. (1977). Changes in surface properties of normal and transformed cells caused by tunicamycin, an inhibitor of protein glycosylation. Proc. Natl Acad. Sci. U. S. A., 74, 3433–3437.

    Article  PubMed  CAS  Google Scholar 

  • Fouchier, R.A., Schneeberger, P.M., Rozendaal, F.W., Broekman, J.M., Kemink, S.A., Munster, V., Kuiken, T., Rimmelzwaan, G.F., Schutten, M., Van Doornum, G.J., Koch, G., Bosman, A., Koopmans, M., & Osterhaus, A.D. (2004). Avian influenza A virus (H7N7) associated with human conjunctivitis and a fatal case of acute respiratory distress syndrome. Proc. Natl Acad. Sci. U. S. A., 101, 1356–1361.

    Article  PubMed  CAS  Google Scholar 

  • Gambaryan, A., Tuzikov, A., Pazynina, G., Bovin, N., Balish, A., & Klimov, A. (2006). Evolution of the receptor binding phenotype of influenza A (H5) viruses. Virology, 344, 432–438.

    Article  PubMed  CAS  Google Scholar 

  • Gu, J., & Taniguchi, N. (2004). Regulation of integrin functions by N-glycans. Glycoconj. J., 21, 9–15.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Hinshaw, V.S., Webster, R.G., Naeve, C.W., & Murphy, B.R. (1983). Altered tissue tropism of human-avian reassortant influenza viruses. Virology, 128, 260–263.

    Article  PubMed  CAS  Google Scholar 

  • Irie, A., Koyama, S., Kozutsumi, Y., Kawasaki, T., & Suzuki, A. (1998). The molecular basis for the absence of N-glycolylneuraminic acid in humans. J. Biol. Chem., 273, 15866–15871.

    Article  PubMed  CAS  Google Scholar 

  • Ito, T., Suzuki, Y., Suzuki, T., Takada, A., Horimoto, T., Wells, K., Kida, H., Otsuki, K., Kiso, M., Ishida, H., & Kawaoka, Y. (2000). 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., 74, 9300–9305.

    Article  PubMed  CAS  Google Scholar 

  • Iwatsuki-Horimoto, K., Kanazawa, R., Sugii, S., Kawaoka, Y., & Horimoto, T. (2004). The index influenza A virus subtype H5N1 isolated from a human in 1997 differs in its receptor-binding properties from a virulent avian influenza virus. J. Gen. Virol., 85, 1001–1005.

    Article  PubMed  CAS  Google Scholar 

  • Kobasa, D., Takada, A., Shinya, K., Hatta, M., Halfmann, P., Theriault, S., Suzuki, H., Nishimura, H., Mitamura, K., Sugaya, N., Usui, T., Murata, T., Maeda, Y., Watanabe, S., Suresh, M., Suzuki, T., Suzuki, Y., Feldmann, H., & Kawaoka, Y. (2004). Enhanced virulence of influenza A viruses with the haemagglutinin of the 1918 pandemic virus. Nature, 431, 703–707.

    Article  PubMed  CAS  Google Scholar 

  • Le, Q.M., Kiso, M., Someya, K., Sakai, Y.T., Nguyen, T.H., Nguyen, K.H., Pham, N.D., Ngyen, H.H., Yamada, S., Muramoto, Y., Horimoto, T., Takada, A., Goto, H., Suzuki, T., Suzuki, Y., & Kawaoka, Y. (2005). Avian flu: Isolation of drug-resistant H5N1 virus. Nature, 437, 1108.

    Article  PubMed  CAS  Google Scholar 

  • Lin, A.H., & Cannon, P.M. (2002). Use of pseudotyped retroviral vectors to analyze the receptor-binding pocket of hemagglutinin from a pathogenic avian influenza A virus (H7 subtype). Virus Res., 83, 43–56.

    Article  PubMed  CAS  Google Scholar 

  • Matrosovich, M.N., Gambaryan, A.S., Tuzikov, A.B., Byramova, N.E., Mochalova, L.V., Golbraikh, A.A., Shenderovich, M.D., Finne, J., & Bovin, N.V. (1993). Probing of the receptor-binding sites of the H1 and H3 influenza A and influenza B virus hemagglutinins by synthetic and natural sialosides. Virology, 196, 111–121.

    Article  PubMed  CAS  Google Scholar 

  • Matrosovich, M., Zhou, N., Kawaoka, Y., & Webster, R. (1999). The surface glycoproteins of H5 influenza viruses isolated from humans, chickens, and wild aquatic birds have distinguishable properties. J. Virol., 73, 1146–1155.

    PubMed  CAS  Google Scholar 

  • Matrosovich, M., Tuzikov, A., Bovin, N., Gambaryan, A., Klimov, A., Castrucci, M.R., Donatelli, I., & Kawaoka, Y. (2000). Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J. Virol., 74, 8502–8512.

    Article  PubMed  CAS  Google Scholar 

  • Matrosovich, M.N., Matrosovich, T.Y., Gray, T., Roberts, N.A., & Klenk, H.D. (2004). Human and avian influenza viruses target different cell types in cultures of human airway epithelium. Proc. Natl Acad. Sci. U. S. A., 101, 4620–4624.

    Article  PubMed  CAS  Google Scholar 

  • Naffakh, N., Massin, P., Escriou, N., Crescenzo-Chaigne, B., & van der Werf, S. (2000). Genetic analysis of the compatibility between polymerase proteins from human and avian strains of influenza A viruses. J. Gen. Virol., 81, 1283–1291.

    PubMed  CAS  Google Scholar 

  • Reed, B.C., Ronnett, G.V., & Lane, M.D. (1981). Role of glycosylation and protein synthesis in insulin receptor metabolism by 3T3–L1 mouse adipocytes. Proc. Natl Acad. Sci. U. S. A., 78, 2908–2912.

    Article  PubMed  CAS  Google Scholar 

  • Rogers, G.N., & Paulson, J.C. (1983). Receptor determinants of human and animal influenza virus isolates: Differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology, 127, 361–373.

    Article  PubMed  CAS  Google Scholar 

  • Rogers, G.N., Paulson, J.C., Daniels, R.S., Skehel, J.J., Wilson, I.A., & Wiley, D.C. (1983). Single amino acid substitutions in influenza haemagglutinin change receptor binding specificity. Nature, 304, 76–78.

    Article  PubMed  CAS  Google Scholar 

  • Rougon, G., Deagostini-Bazin, H., Hirn, M., & Goridis, C. (1982). Tissue- and developmental stage-specific forms of a neural cell surface antigen linked to differences in glycosylation of a common polypeptide. EMBO J., 1, 1239–1244.

    PubMed  CAS  Google Scholar 

  • Ryan-Poirier, K., Suzuki, Y., Bean, W.J., Kobasa, D., Takada, A., Ito, T., & Kawaoka, Y. (1998). Changes in H3 influenza A virus receptor specificity during replication in humans. Virus Res., 56, 169–176.

    Article  PubMed  CAS  Google Scholar 

  • Schauer, R. (2000). Achievements and challenges of sialic acid research. Glycoconj. J., 17, 485–499.

    Article  PubMed  CAS  Google Scholar 

  • Shinya, K., Hatta, M., Yamada, S., Takada, A., Watanabe, S., Halfmann, P., Horimoto, T., Neumann, G., Kim, J.H., Lim, W., Guan, Y., Peiris, M., Kiso, M., Suzuki, T., Suzuki, Y., & Kawaoka, Y. (2005). Characterization of a human H5N1 influenza A virus isolated in 2003. J. Virol., 79, 9926–9932.

    Article  PubMed  CAS  Google Scholar 

  • Shinya, K., Ebina, M., Yamada, S., Ono, M., Kasai, N., & Kawaoka, Y. (2006). Avian flu: Influenza virus receptors in the human airway. Nature, 440, 435–436.

    Article  PubMed  CAS  Google Scholar 

  • Stevens, J., Corper, A.L., Basler, C.F., Taubenberger, J.K., Palese, P., & Wilson, I.A. (2004). Structure of the uncleaved human H1 hemagglutinin from the extinct 1918 influenza virus. Science, 303, 1866–1870.

    Article  PubMed  CAS  Google Scholar 

  • Stevens, J., Blixt, O., Tumpey, T.M., Taubenberger, J.K., Paulson, J.C., & Wilson, I.A. (2006). Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science, 312, 404–410.

    Article  PubMed  CAS  Google Scholar 

  • Subbarao, K., & Shaw, M.W. (2000). Molecular aspects of avian influenza (H5N1) viruses isolated from humans. Rev. Med. Virol., 10, 337–348.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Suzuki, Y. (2005). Sialobiology of influenza: Molecular mechanism of host range variation of influenza viruses. Biol. Pharm. Bull., 28, 399–408.

    Article  PubMed  CAS  Google Scholar 

  • Suzuki, Y., Ito, T., Suzuki, T., Holland Jr., R.E., Chambers, T.M., Kiso, M., Ishida, H., & Kawaoka, Y. (2000). Sialic acid species as a determinant of the host range of influenza A viruses. J. Virol., 74, 11825–11831.

    Article  PubMed  CAS  Google Scholar 

  • Uiprasertkul, M., Puthavathana, P., Sangsiriwut, K., Pooruk, P., Srisook, K., Peiris, M., Nicholls, J.M., Chokephaibulkit, K., Vanprapar, N., & Auewarakul, P. (2005). Influenza A H5N1 replication sites in humans. Emerg. Infect. Dis., 11, 1036–1041.

    PubMed  CAS  Google Scholar 

  • Ungchusak, K., Auewarakul, P., Dowell, S.F., Kitphati, R., Auwanit, W., Puthavathana, P., Uiprasertkul, M., Boonnak, K., Pittayawonganon, C., Cox, N.J., Zaki, S.R., Thawatsupha, P., Chittaganpitch, M., Khontong, R., Simmerman, J.M., & Chunsutthiwat, S. (2005). Probable person-to-person transmission of avian influenza A (H5N1). N. Engl. J. Med., 352, 333–340.

    Article  PubMed  CAS  Google Scholar 

  • van Riel, D., Munster, V.J., de Wit, E., Rimmelzwaan, G.F., Fouchier, R.A., Osterhaus, A.D., & Kuiken, T. (2006). H5N1 virus attachment to lower respiratory tract. Science, 312, 399.

    Article  PubMed  Google Scholar 

  • World Health Organization. (2006). Epidemiology of WHO-confirmed human cases of avian influenza A(H5N1) infection. Wkly. Epidemiol. Rec., 81, 249–257.

    Google Scholar 

  • Yamada, S., Suzuki, Y., Suzuki, T., Le, M.Q., Nidom, C.A., Sakai-Tagawa, Y., Muramoto, Y., Ito, M., Kiso, M., Horimoto, T., Shinya, K., Sawada, T., Kiso, M., Usui, T., Murata, T., Lin, Y., Hay, A., Haire, L.F., Stevens, D.J., Russell, R.J., Gamblin, S.J., Skehel, J.J., & Kawaoka, Y. (2006). Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature, 444, 378–382.

    Article  PubMed  CAS  Google Scholar 

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Kawaoka, Y., Shinya, K. (2008). Transmission of Avian Influenza Viruses to Humans: Viral Receptor Specificity and Distribution in Human Airways. In: Lu, Y., Essex, M., Roberts, B. (eds) Emerging Infections in Asia. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-75722-3_3

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  • DOI: https://doi.org/10.1007/978-0-387-75722-3_3

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