1887

Abstract

Two genetically distinct lineages of H1N1 influenza A viruses, circulated worldwide before 1994, were antigenically indistinguishable. In 1994, viruses emerged in China, including A/Beijing/262/95, with profound antigenic differences from the contemporary circulating H1N1 strains. Haemagglutinin sequence comparisons of either a predecessor virus, A/Hebei/52/94, or one representative of the cocirculating A/Bayern/7/95-like clade, A/Shenzhen/227/95, revealed a deletion of K at position 134 (H3 numbering) in the antigenic variants. The K134 deletion conferred a selective advantage to the Chinese deletion lineage, such that it eventually gave rise to currently circulating H1 viruses. Using reverse genetics to generate viruses with either an insertion or deletion of aa 134, we have confirmed that the K134 deletion, rather than a constellation of sublineage specific amino acid changes, was sufficient for the antigenic difference observed in the Chinese deletion lineage, and reinsertion of K134 revealed the requirement of a compatible neuraminidase surface glycoprotein for viral growth.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.83184-0
2007-12-01
2019-11-17
Loading full text...

Full text loading...

/deliver/fulltext/jgv/88/12/3209.html?itemId=/content/journal/jgv/10.1099/vir.0.83184-0&mimeType=html&fmt=ahah

References

  1. Aytay, S. & Schulze, I. T. ( 1991; ). Single amino acid substitutions in the hemagglutinin can alter the host range and receptor binding properties of H1 strains of influenza A virus. J Virol 65, 3022–3028.
    [Google Scholar]
  2. Baigent, S. J. & McCauley, J. W. ( 2001; ). Glycosylation of haemagglutinin and stalk-length of neuraminidase combine to regulate the growth of avian influenza viruses in tissue culture. Virus Res 79, 177–185.[CrossRef]
    [Google Scholar]
  3. Baum, L. G. & Paulson, J. C. ( 1991; ). The N2 neuraminidase of human influenza virus has acquired a substrate specificity complementary to the hemagglutinin receptor specificity. Virology 180, 10–15.[CrossRef]
    [Google Scholar]
  4. Bause, E. ( 1983; ). Structural requirements of N-glycosylation of proteins. Studies with proline peptides as conformational probes. Biochem J 209, 331–336.
    [Google Scholar]
  5. Bause, E., Hettkamp, H. & Legler, G. ( 1982; ). Conformational aspects of N-glycosylation of proteins. Studies with linear and cyclic peptides as probes. Biochem J 203, 761–768.
    [Google Scholar]
  6. Caton, A. J., Brownlee, G. G., Yewdell, J. W. & Gerhard, W. ( 1982; ). The antigenic structure of the influenza virus A/PR/8/34 hemagglutinin (H1 subtype). Cell 31, 417–427.[CrossRef]
    [Google Scholar]
  7. Cox, R. J. & Brokstad, K. A. ( 1999; ). The postvaccination antibody response to influenza virus proteins. APMIS 107, 289–296.[CrossRef]
    [Google Scholar]
  8. Daniels, R. S., Douglas, A. R., Skehel, J. J., Wiley, D. C., Naeve, C. W., Webster, R. G., Rogers, G. N. & Paulson, J. C. ( 1984; ). Antigenic analyses of influenza virus haemagglutinins with different receptor-binding specificities. Virology 138, 174–177.[CrossRef]
    [Google Scholar]
  9. Gamblin, S. J., Haire, L. F., Russell, R. J., Stevens, D. J., Xiao, B., Ha, Y., Vasisht, N., Steinhauer, D. A., Daniels, R. S. & other authors ( 2004; ). The structure and receptor binding properties of the 1918 influenza hemagglutinin. Science 303, 1838–1842.[CrossRef]
    [Google Scholar]
  10. Hoffmann, E., Neumann, G., Kawaoka, Y., Hobom, G. & Webster, R. G. ( 2000; ). A DNA transfection system for generation of influenza A virus from eight plasmids. Proc Natl Acad Sci U S A 97, 6108–6113.[CrossRef]
    [Google Scholar]
  11. Huang, C. C., Couch, G. S., Pettersen, E. F. & Ferrin, T. E. ( 1996; ). Chimera: an extensible molecular modeling application constructed using standard components. In Pacific Symposium on Biocomputing ‘96, p. 724. Edited by L. Hunter & T. E. Klein. Singapore: World Scientific Publishing.
  12. Kaverin, N. V., Matrosovich, M. N., Gambaryan, A. S., Rudneva, I. A., Shilov, A. A., Varich, N. L., Makarova, N. V., Kropotkina, E. A. & Sinitsin, B. V. ( 2000; ). Intergenic HA-NA interactions in influenza A virus: postreassortment substitutions of charged amino acid in the hemagglutinin of different subtypes. Virus Res 66, 123–129.[CrossRef]
    [Google Scholar]
  13. Kendal, A. P., Pereira, M. S. & Skehel, J. J. ( 1982; ). Hemagglutination inhibition. In Concepts and Procedures for Laboratory-Based Influenza Surveillance, pp. B17–B35. Edited by A. P. Kendal, M. S. Pereira & J. J. Skehel. Atlanta, GA: Centers for Disease Control and Prevention.
  14. Kumar, S., Tamura, K. & Nei, M. ( 2004; ). mega3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5, 150–163.[CrossRef]
    [Google Scholar]
  15. Lu, B., Zhou, H., Ye, D., Kemble, G. & Jin, H. ( 2005; ). Improvement of influenza A/Fujian/411/02 (H3N2) virus growth in embryonated chicken eggs by balancing the hemagglutinin and neuraminidase activities, using reverse genetics. J Virol 79, 6763–6771.[CrossRef]
    [Google Scholar]
  16. Maines, T. R., Chen, L. M., Matsuoka, Y., Chen, H., Rowe, T., Ortin, J., Falcon, A., Nguyen, T. H., Mai, L. Q. & other authors ( 2006; ). Lack of transmission of H5N1 avian-human reassortant influenza viruses in a ferret model. Proc Natl Acad Sci U S A 103, 12121–12126.[CrossRef]
    [Google Scholar]
  17. Matrosovich, M. N., Gambaryan, A. S., Teneberg, S., Piskarev, V. E., Yamnikova, S. S., Lvov, D. K., Robertson, J. S. & Karlsson, K. A. ( 1997; ). Avian influenza A viruses differ from human viruses by recognition of sialyloligosaccharides and gangliosides and by a higher conservation of the HA receptor-binding site. Virology 233, 224–234.[CrossRef]
    [Google Scholar]
  18. 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.[CrossRef]
    [Google Scholar]
  19. Nakajima, S., Nishikawa, F. & Nakajima, K. ( 2000; ). Comparison of the evolution of recent and late phase of old influenza A (H1N1) viruses. Microbiol Immunol 44, 841–847.[CrossRef]
    [Google Scholar]
  20. National Research Council ( 2002; ). Guide for the Care and Use of Laboratory Animals. Washington, DC: National Academy Press.
  21. Nobusawa, E., Aoyama, T., Kato, H., Suzuki, Y., Tateno, Y. & Nakajima, K. ( 1991; ). Comparison of complete amino acid sequences and receptor-binding properties among 13 serotypes of hemagglutinins of influenza A viruses. Virology 182, 475–485.[CrossRef]
    [Google Scholar]
  22. Raymond, F. L., Caton, A. J., Cox, N. J., Kendal, A. P. & Brownlee, G. G. ( 1986; ). The antigenicity and evolution of influenza H1 haemagglutinin, from 1950–1957 and 1977–1983: two pathways from one gene. Virology 148, 275–287.[CrossRef]
    [Google Scholar]
  23. Rocha, E., Cox, N. J., Black, R. A., Harmon, M. W., Harrison, C. J. & Kendal, A. P. ( 1991; ). Antigenic and genetic variation in influenza A (H1N1) virus isolates recovered from a persistently infected immunodeficient child. J Virol 65, 2340–2350.
    [Google Scholar]
  24. Sanner, M. F., Olson, A. J. & Spehner, J. C. ( 1996; ). Reduced surface: an efficient way to compute molecular surfaces. Biopolymers 38, 305–320.[CrossRef]
    [Google Scholar]
  25. Sato, K., Morishita, T., Nobusawa, E., Tonegawa, K., Sakae, K., Nakajima, S. & Nakajima, K. ( 2004; ). Amino-acid change on the antigenic region B1 of H3 haemagglutinin may be a trigger for the emergence of drift strain of influenza A virus. Epidemiol Infect 132, 399–406.[CrossRef]
    [Google Scholar]
  26. Shaw, M. W., Xu, X., Li, Y., Normand, S., Ueki, R. T., Kunimoto, G. Y., Hall, H., Klimov, A., Cox, N. J. & Subbarao, K. ( 2002; ). Reappearance and global spread of variants of influenza B/Victoria/2/87 lineage viruses in the 2000–2001 and 2001–2002 seasons. Virology 303, 1–8.[CrossRef]
    [Google Scholar]
  27. Stohr, K. ( 2002; ). Influenza–WHO cares. Lancet Infect Dis 2, 517 [CrossRef]
    [Google Scholar]
  28. Subbarao, K., Chen, H., Swayne, D., Mingay, L., Fodor, E., Brownlee, G., Xu, X., Lu, X., Katz, J. & other authors ( 2003; ). Evaluation of a genetically modified reassortant H5N1 influenza A virus vaccine candidate generated by plasmid-based reverse genetics. Virology 305, 192–200.[CrossRef]
    [Google Scholar]
  29. Wagner, R., Wolff, T., Herwig, A., Pleschka, S. & Klenk, H. D. ( 2000; ). Interdependence of hemagglutinin glycosylation and neuraminidase as regulators of influenza virus growth: a study by reverse genetics. J Virol 74, 6316–6323.[CrossRef]
    [Google Scholar]
  30. Weis, W., Brown, J. H., Cusack, S., Paulson, J. C., Skehel, J. J. & Wiley, D. C. ( 1988; ). Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature 333, 426–431.[CrossRef]
    [Google Scholar]
  31. Wilson, I. A. & Cox, N. J. ( 1990; ). Structural basis of immune recognition of influenza virus hemagglutinin. Annu Rev Immunol 8, 737–771.[CrossRef]
    [Google Scholar]
  32. Wilson, I. A., Skehel, J. J. & Wiley, D. C. ( 1981; ). Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 A resolution. Nature 289, 366–373.[CrossRef]
    [Google Scholar]
  33. Xu, X., Lindstrom, S. E., Shaw, M. W., Smith, C. B., Hall, H. E., Mungall, B. A., Subbarao, K., Cox, N. J. & Klimov, A. ( 2004; ). Reassortment and evolution of current human influenza A and B viruses. Virus Res 103, 55–60.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.83184-0
Loading
/content/journal/jgv/10.1099/vir.0.83184-0
Loading

Data & Media loading...

Supplements

vol. , part 12, pp. 3209 - 3213

Amino acid alignments of (a) HA and (b) NA gene segments of the three H1N1 influenza A strains used in this study

Predicted surface charge distribution of A/Puerto Rico/8/1934 HA1 domain monomer with insertion of K134

Accession numbers of isolates used in this study

. Microneutralization titres of H1N1 recombinant viruses bearing K134 insertion or deletion in the HA glycoprotein [Single PDF file](195 KB)



PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error