Stability of infectious influenza A viruses to treatment at low pH and heating

Summary

We have measured the infectivity of influenza A virus strains grown either in embryonated eggs or in chick embryo cells in culture after treatment at low pH. At pH values at which hemolysis occurs there was an irreversible loss of infectivity. The threshold pH, at which the infectivity was lost, depended on the hemagglutinin subtype of the virus strain. All H5 and H7 strains tested were extremely labile at low pH. In contrast, all H3 strains were relatively stable, independent of the species from which the viruses were isolated. With several H1 viruses the hemagglutination (HA) activity was irreversibly lost at intermediate pH values causing inactivation of infectivity. Strains with noncleaved hemagglutinins were much more stable. These observations might explain why duck influenza viruses can easily survive in lake water and wet faeces, and multiply in the intestinal tract, where trypsin is present. There are also significant differences in heat stability exhibited by influenza A strains. In contrast to pH stability this is not a specific trait of the hemagglutinin, since it can be influenced by reassortment. There is no correlation between the stability of infectivity at low pH and heat.

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References

  1. 1.

    Appleyard, G., Maber, H. B.: Plaque formation by influenza viruses in the presence of trypsin. J. gen. Virology25, 351–357 (1974).

    Google Scholar 

  2. 2.

    Bosch, F. X., Orlich, M., Klenk, H.-D., Rott, R.: The structure of the hemagglutinin, a determinant for the pathogenicity of influenza viruses. Virology95, 197–207 (1979).

    Google Scholar 

  3. 3.

    Hinshaw, V. S., Webster, R. G., Turner, B.: Waterborne transmission of influenza A viruses? Intervirology11, 66–68 (1979).

    Google Scholar 

  4. 4.

    Hinshaw, V. S., Webster, R. G., Naeve, C. W., Murphy, B. R.: Altered tissue tropism of human-avian reassortant influenza viruses. Virology128, 260–263 (1983).

    Google Scholar 

  5. 5.

    Hosaka, Y., Seriburi, O., Moran, M. G., Yasuda, Y., Fukai, K., Nerome, K.: Haemolysis and fusion by influenza viruses with heat inactivated neuraminidase activity. Biken J.25, 51–62 (1982).

    Google Scholar 

  6. 6.

    Huang, R. T., Rott, R., Klenk, H.-D.: Influenza virus causes haemolysis and fusion of cells. Virology110, 243–247 (1981).

    Google Scholar 

  7. 7.

    Klenk, H.-D., Rott, R., Becht, H.: On the structure of the influenza virus envelope. Virology47, 579–591 (1972).

    Google Scholar 

  8. 8.

    Lenard, J., Baily, C. A., Miller, D. K.: pH dependence of influenza A virus-induced hemolysis is determined by the haemagglutinine gene. J. gen. Virol.62, 353–355 (1982).

    Google Scholar 

  9. 9.

    McCahon, D., Schild, G. C.: An investigation of some factors affecting cross-reactivation between influenza A viruses. J. gen. Virol.12, 207–219 (1971).

    Google Scholar 

  10. 10.

    Meda, T., Ohnishi, S.-I.: Activation of influenza virus by acidic media causes hemolysis and fusion of erythrocytes. FEBS-Lett.122, 283–287 (1980).

    Google Scholar 

  11. 11.

    Maeda, T., Kawasaki, K., Ohnishi, S.-I.: Interaction of influenza virus hemagglutinin with target membrane lipids is a key step in virus induced hemolysis and fusion at pH=5.2. Proc. Natl. Acad. Sci. U.S.A.78, 4133–4137 (1981).

    Google Scholar 

  12. 12.

    Matlin, K. S., Reggio, H., Helenius, A., Simons, K.: Infection entry pathway of influenza virus in a canine kidney cell line. J. Cell Biol.91, 601–603 (1981).

    Google Scholar 

  13. 13.

    Rott, R., Reinacher, M., Orlich, M., Klenk, H.-D.: Cleavability of hemagglutinin determines spread of avian influenza viruses in the chorioallantoic membrane of chicken embryo. Arch. Virol.65, 123–133 (1980).

    Google Scholar 

  14. 14.

    Sato, S. B., Kawasaki, K., Ohnishi, S.-I.: Hemolytic activity of influenza virus hemagglutinin glycoproteins activated in mildly acidic environments. Proc. Natl. Acad. Sci. U.S.A.80, 3153–3157 (1983).

    Google Scholar 

  15. 15.

    Skehel, J. J., Bayley, P. M., Brown, E. B., Martin, S. R., Waterfield, M. D., White, J. M., Wilson, I. A., Wiley, D. C.: Changes in the conformation of the influenza virus hemagglutinin at the pH optimum of virus mediated fusion. Proc. Natl. Acad. Sci. U.S.A.79, 968–972 (1982).

    Google Scholar 

  16. 16.

    Webster, R. G., Yakhno, M., Hinshaw, V. S., Bean, W. J., Murti, G.: Intestinal influenza: Replication and characterization of influenza viruses in ducks. Virology84, 268–276 (1978).

    Google Scholar 

  17. 17.

    White, J., Helenius, A., Gething, M. J.: Haemagglutinin of influenza virus expressed from a cloned gene promotes membrane fusion. Nature300, 658–659 (1982).

    Google Scholar 

  18. 18.

    Yoshimura, A., Kuroda, K., Kawasaki, K., Yamashima, S., Maeda, T., Ohnishi, S.: Infectious cell entry mechanism of influenza virus. J. Virol.43, 284–293 (1982).

    Google Scholar 

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Scholtissek, C. Stability of infectious influenza A viruses to treatment at low pH and heating. Archives of Virology 85, 1–11 (1985). https://doi.org/10.1007/BF01317001

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Keywords

  • Influenza
  • Influenza Virus
  • Virus Strain
  • Chick Embryo
  • Embryo Cell