1887

Abstract

We analysed the role of neuraminidase (NA) on haemadsorption by the haemagglutinin (HA) protein of influenza B virus. The influenza B virus mutant ts-7 has a temperature-sensitive mutation in the NA protein. At high temperature, cells infected with this virus did not exhibit haemadsorption activity, but the addition of bacterial neuraminidase (bNA) restored haemadsorption activity. COS cells transfected with HA cDNAs of B/Kanagawa/73 or B/Lee/40 virus showed no evidence of haemadsorption. However, with the addition of bNA or co- transfection with NA cDNA of the B/Lee/40 virus, haemadsorption was observed. Experiments with point-mutated HA cDNAs of B/Lee/40 virus showed that two -acetyl glycosylation sites at amino acid residues 160 and 217 were responsible for the inability of the HA protein to adsorb to erythrocytes. These results indicated that haemadsorption by the HA protein of influenza B virus required the involvement of NA. Because the NA inhibitor Zanamivir was reported not to penetrate cells, we investigated the action of this inhibitor and found that Zanamivir inhibited haemadsorption on MDCK cells infected with B/Kanagawa/73 or B/Lee/40 virus. After removing Zanamivir by washing, the addition of bNA restored the haemadsorption activity on the infected cells. Scanning electron microscopy indicated that at 0·4 μM Zanamivir, HA protein did not adsorb to erythrocytes but retained the ability to aggregate virions. However, at 4 μM Zanamivir, distinct virion formation could not be observed.

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1999-11-01
2019-10-19
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References

  1. Brassard, D. & Lamb, R. A. ( 1997; ). Expression of influenza B virus hemagglutinin containing multibasic residue cleavage sites. Virology 236, 234-248.[CrossRef]
    [Google Scholar]
  2. Enami, M. & Enami, K. ( 1996; ). Influenza virus hemagglutinin and neuraminidase glycoprotein stimulate the membrane association of the matrix protein. Journal of Virology 70, 6653-6657 .
    [Google Scholar]
  3. Gambaryan, A. S. , Robertson, J. S. & Matroosovich, M. N. ( 1999; ). Effects of egg- adaptation on the receptor-binding properties of human influenza A and B viruses. Virology 258, 232-239.[CrossRef]
    [Google Scholar]
  4. Huang, R. T. C. , Rott, R. & Klenk, H.-D. ( 1981; ). Influenza viruses cause hemolysis and fusion of cells. Virology 110, 243-247.[CrossRef]
    [Google Scholar]
  5. Itzstein, M. V. , Wu, W.-Y. , Kok, G. B. , Pegg, M. S. , Dyason, J. C. , Jin, B. , Phan, T. V. , Smythe, M. L. , White, H. F. , Oliver, S. W. , Colman, P. M. , Vargheses, J. N. , Ryan, D. M. , Woods, J. M. , Bethell, R. C. , Hotham, V. J. , Cameron, J. M. & Penn, C. R. ( 1993; ). Rational design of potent sialidase-based inhibitors of influenza virus replication. Nature 363, 418-423.[CrossRef]
    [Google Scholar]
  6. Jie, Z. & Lamb, R. A. ( 1996; ). Characterization of the membrane association of the influenza virus matrix protein in living cells. Virology 225, 255-266.[CrossRef]
    [Google Scholar]
  7. Klenk, H.-D. , Ohuchi, M. , Ohuchi, R. , Fischer, C. , Feldman, A. & Garter, W. ( 1996; ). Receptor binding and fusion activity of the hemagglutinin as depending on glycosylation and cytoplasmic tail modification. In Options for the Control of Influenza, vol. III, pp. 315-327. Edited by L. E. Brown, A. W. Hampson & R. G. Webster. New York: Elsevier Science.
  8. Krystal, M. , Young, J. F. , Palese, P. , Wilson, I. A. , Skehel, J. J. & Wiley, D. C. ( 1983; ). Sequential mutations in hemagglutinin of influenza B virus isolates: definition of antigenic domains. Proceedings of the National Academy of Sciences, USA 800, 4527-4531 .
    [Google Scholar]
  9. Lenard, J. & Miller, D. K. ( 1981; ). pH-dependent hemolysis by influenza, Semliki-Forest virus, Sendai virus. Virology 110, 479-482.[CrossRef]
    [Google Scholar]
  10. Maeda, T. & Ohnishi, S. ( 1980; ). Activation of influenza virus by acidic media causes hemolysis and fusion of erythrocytes. FEBS Letters 122, 283-287.[CrossRef]
    [Google Scholar]
  11. Mitnaul, L. J. , Castrucci, M. R. , Murti, K. G. & Kawaoka, Y. ( 1996; ). The cytoplasmic tail of influenza A virus neuraminidase (NA) affects NA incorporation into virions, virion morphology, and virulence in mice but is not essential for virus replication. Journal of Virology 70, 873-879.
    [Google Scholar]
  12. Morishita, T. , Kobayashi, S. , Miyake, T. , Ishihara, Y. , Nakajima, S. & Nakajima, K. ( 1993; ). Host-specific hemagglutination of influenza A (H1N1) virus. Microbiology and Immunology 37, 661-665.[CrossRef]
    [Google Scholar]
  13. Morishita, T. , Nobusawa, E. , Nakajima, K. & Nakajima, S. ( 1996; ). Studies on the molecular basis for loss of the ability of recent influenza A (H1N1) virus strains to agglutinate chicken erythrocytes. Journal of General Virology 77, 2499-2506 .[CrossRef]
    [Google Scholar]
  14. Morris, S. J. , Price, G. E. , Barnett, J. M. , Hiscox, S. A. , Smith, H. & Sweet, C. ( 1999; ). Role of neuraminidase in influenza virus-induced apoptosis. Journal of General Virology 80, 137-146.
    [Google Scholar]
  15. Nobusawa, E. & Nakajima, K. ( 1988; ). Amino acid substitution at 226 of the hemagglutinin molecule of influenza A (H1N1) affects receptor binding activity but not fusion activity. Virology 167, 8-14.[CrossRef]
    [Google Scholar]
  16. Nobusawa, E. , Morishita, T. & Nakajima, K. ( 1996; ). Novel receptor binding specificity of recent isolates of human influenza A viruses. In Options for the Control of Influenza, vol. III, pp. 437-442. Edited by L. E. Brown, A. W. Hampson & R. G. Webster. New York: Elsevier Science.
  17. Ohuchi, M. , Feldmann, A. , Ohuchi, R. & Klenk, H.-D. ( 1995; ). Neuraminidase is essential for fowl plague virus hemagglutinin to show hemagglutinating activity. Virology 212, 77-83.[CrossRef]
    [Google Scholar]
  18. Oxford, J. S. , Schild, G. C. , Corcoran, T. , Newman, R. , Major, D. , Robertson, J. , Bootman, J. , Higgins, P. , Al-Nakib, W. & Tyrell, D. A. J. ( 1990; ). A host- cell-selected variant of influenza B virus with a single nucleotide substitution in HA affecting a potential glycosylation site was attenuated in virulence for volunteers. Archives of Virology 110, 34-46.
    [Google Scholar]
  19. Palese, P. , Tobita, K. , Ueda, M. & Compans, R. W. ( 1974; ). Characterization of temperature sensitive influenza virus mutants defective in neuraminidase. Virology 61, 397-410.[CrossRef]
    [Google Scholar]
  20. Palmer, D. F., Coleman, M. T., Dowdle, W. R. & Schild, G. C. (1975). Neuraminidase inhibition test. In Advanced Laboratory Techniques for Influenza Diagnosis, pp. 107–126. Atlanta: Center for Disease Control.
  21. Robertson, J. S. , Naeve, C. W. , Webster, R. G. , Bootman, J. S. , Newman, R. & Schild, G. C. ( 1985; ). Alterations in the hemagglutinin associated with adaptation of influenza B virus to growth in eggs. Virology 143, 166-174.[CrossRef]
    [Google Scholar]
  22. Shibata, S. , Yamamoto-Goshima, F. , Maeno, K. , Hanaichi, T. , Fujita, Y. , Nakajima, K. , Imai, M. , Komatsu, T. & Sugiura, S. ( 1993; ). Characterization of a temperature- sensitive influenza B virus mutant defective in neuraminidase. Journal of Virology 67, 3264-3273 .
    [Google Scholar]
  23. Show, M. W. , Lamb, R. A. , Erickson, B. W. , Briedis, D. J. & Choppin, P. W. ( 1982; ). Complete nucleotide sequence of the neuraminidase gene of influenza B virus. Proceedings of the National Academy of Sciences, USA 79, 6817-6821 .[CrossRef]
    [Google Scholar]
  24. Tong, N. , Nobusawa, E. , Morishita, M. , Nakajima, S. & Nakajima, K. ( 1998; ). M protein correlates with the receptor-binding specificity of haemagglutinin protein of reassortant influenza A (H1N1) virus. Journal of General Virology 79, 2425-2434 .
    [Google Scholar]
  25. Wandinger-Ness, A. , Bennett, M. K. , Atonny, C. & Simons, K. ( 1990; ). Distinct transport vesicles mediate the delivery of plasma membrane proteins to the apical and basolateral domains of MDCK cells. Journal of Cell Biology 111, 987-1000 .[CrossRef]
    [Google Scholar]
  26. Yamamoto-Goshima, F. , Maeno, K. , Morishita, T. , Ueda, M. , Fujita, Y. , Nakajima, K. & Yoshii, S. ( 1994; ). Role of neuraminidase in the morphogenesis of influenza B virus. Journal of Virology 68, 1250-1254 .
    [Google Scholar]
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