Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 Å resolution

Nature volume 303, pages 35–40 (1983)Cite this article

Abstract

The influenza virus neuraminidase glycoprotein is a tetramer with a box-shaped head, 100×100×60 Å, attached to a slender stalk. The three-dimensional structure of neuraminidase heads shows that each monomer is composed of six topologically identical β-sheets arranged in a propeller formation. The tetrameric enzyme has circular 4-fold symmetry stabilized in part by metal ions bound on the symmetry axis. Sugar residues are attached to four of the five potential glycosylation sequences, and in one case contribute to the interaction between subunits in the tetramer.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Laver, W. G. & Valentine, R. C. Virology 38, 105–119 (1969).

    Article  CAS  Google Scholar 

  2. Hirst, G. K. Science 94, 22–23 (1941).

    Article  ADS  CAS  Google Scholar 

  3. Klenk, H.-D., Rott, R., Orlich, M. & Blodorn, J. Virology 68, 426–439 (1975).

    Article  CAS  Google Scholar 

  4. Lazarowitz, S. G. & Choppin, P. W. Virology 68, 440–454 (1975).

    Article  CAS  Google Scholar 

  5. Gottschalk, A. Biochim. biophys. Acta 23, 645–646 (1957).

    Article  CAS  Google Scholar 

  6. Drzeniek, R. Curr. Topics Microbiol. Immun. 59, 35–74 (1972).

    Article  CAS  Google Scholar 

  7. Burnet, F. M. & Stone, J. D. Aust. J. exp. Biol. med. Sci. 25, 227–233 (1947).

    Article  CAS  Google Scholar 

  8. Gottschalk, A. The Glycoproteins. Their Composition, Structure and Function (Elsevier, Amsterdam, 1966).

    Google Scholar 

  9. Palese, P., Tobita, K., Ueda, M. & Compans, R. W. Virology 61, 397–410 (1974).

    Article  CAS  Google Scholar 

  10. Webster, R. G. & Laver, W. G. in The Influenza Viruses and Influenza (ed. Kilbourne, E. D.) 269–314 (Academic, New York, 1975).

    Google Scholar 

  11. Webster, R. G., Laver, W. G., Air, G. M. & Schild, G. C. Nature 296, 115–121 (1982).

    Article  ADS  CAS  Google Scholar 

  12. Ward, C. W. Curr. Topics Microbiol. Immun. 94, 1–74 (1981).

    Google Scholar 

  13. Elleman, T. C., Azad, A. A. & Ward, C. W. Nucleic Acids Res. 10, 7005–7015 (1982).

    Article  CAS  Google Scholar 

  14. Ward, C. W., Elleman, T. C. & Azad, A. A. Biochem. J. 207, 91–95 (1982).

    Article  CAS  Google Scholar 

  15. Schild, G. C. in Structure and Variation in Influenza Virus (eds Laver, W. G. & Air, G. M.) 373–383 (Elsevier, New York, 1981).

    Google Scholar 

  16. Blok, J. et al. Virology 119, 109–121 (1982).

    Article  CAS  Google Scholar 

  17. Fields, S., Winter, G. & Brownlee, G. G. Nature 290, 213–217 (1981).

    Article  ADS  CAS  Google Scholar 

  18. Hiti, A. L. & Nyak, D. P. J. Virol. 41, 730–734 (1982).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Markoff, L. & Lai, C.-J. Virology 119, 288–297 (1982).

    Article  CAS  Google Scholar 

  20. Bentley, D. R. & Brownlee, G. G. Nucleic Acids Res. 10, 5033–5042 (1982).

    Article  CAS  Google Scholar 

  21. Van Rompuy, L., Min-Jou, W., Huylebroeck, D. & Fiers, W. J. molec. Biol. 161, 1–11 (1982).

    Article  CAS  Google Scholar 

  22. Shaw, M. W., Lamb, R. A., Erikson, B. W., Breidis, D. J. & Choppin, P. W. Proc. natn. Acad. Sci. U.S.A. 79, 6817–6821 (1982).

    Article  ADS  CAS  Google Scholar 

  23. Laver, W. G. Virology 86, 78–87 (1978).

    Article  CAS  Google Scholar 

  24. Colman, P. M., Varghese, J. N. & Laver, W. G. Nature 303, 41–44 (1983).

    Article  ADS  CAS  Google Scholar 

  25. Wright, C. E. & Laver, W. G. J. molec. Biol. 120, 133–136 (1978).

    Article  CAS  Google Scholar 

  26. Colman, P. M. & Laver, W. G. in Structural Aspects of Recognition and Assembly in Biological Macromolecules (ed. Balaban, M.) 869–872 (I.S.S., Rehovot, 1981).

    Google Scholar 

  27. Kilbourne, E. D., Laver, W. G., Schulman, J. L. & Webster, R. G. J. Virol. 2, 281–288 (1968).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Schwager, P., Bartels, K. & Jones, A. J. appl. Crystallogr. 8, 275–280 (1975).

    Article  Google Scholar 

  29. Dickerson, R. E., Kendrew, J. C. & Strandberg, B. Acta crystallogr. 14, 1188–1195 (1961).

    Article  CAS  Google Scholar 

  30. Rossmann, M. G. J. appl. Crystallogr. 12, 225–238 (1979).

    Article  CAS  Google Scholar 

  31. Rossmann, M. G., Leslie, A. G. W., Abdel-Meguid, S. S. & Tsukihara, T. J. appl. Crystallogr. 12, 570–581 (1979).

    Article  CAS  Google Scholar 

  32. Rossmann, M. G. & Blow, D. M. Acta crystallogr. 15, 24–31 (1962).

    Article  CAS  Google Scholar 

  33. Colman, P. M. Z. Kristallogr. Krystallgeom. 140, 344–349 (1974).

    ADS  Google Scholar 

  34. Bricogne, G. Acta crystallogr. A32, 832–847 (1976).

    Article  Google Scholar 

  35. Richardson, J. S. Nature 268, 495–500 (1977).

    Article  ADS  CAS  Google Scholar 

  36. Chothia, C. J. molec. Biol. 75, 295–302 (1973).

    Article  CAS  Google Scholar 

  37. Banner, D. W. et al. Nature 255, 609–614 (1975).

    Article  ADS  CAS  Google Scholar 

  38. Stuart, D. I., Levine, M., Muirhead, H. & Stammers, D. K. J. molec. Biol. 134, 109–142 (1979).

    Article  CAS  Google Scholar 

  39. Davies, D. R., Padlan, E. A. & Segal, D. M. A. Rev. Biochem. 44, 639–667 (1975).

    Article  CAS  Google Scholar 

  40. Ward, C. W., Colman, P. M. & Laver, W. G. Febs Lett. (in the press).

  41. Richardson, J. S. Adv. Protein Chem. 34, 167–339 (1981).

    Article  CAS  Google Scholar 

  42. Ward, C. W., Murray, J. M., Roxburgh, C. M. & Jackson, D. C. Virology (in the press).

  43. Deisenhofer, J., Colman, P. M., Epp, O. & Huber, R. Hoppe-Seyler's Z. physiol. Chem. 357, 1421–1434 (1976).

    Article  CAS  Google Scholar 

  44. Ward, C. W. & Dopheide, T. A. Biochem. J. 193, 953–962 (1981).

    Article  CAS  Google Scholar 

  45. Wilson, I. A., Skehel, J. J. & Wiley, D. C. Nature 289, 366–373 (1981).

    Article  ADS  CAS  Google Scholar 

  46. Allen, A. K., Skehel, J. J. & Yuferov, V. J. gen. Virol, 37, 625–628 (1977).

    Article  CAS  Google Scholar 

  47. Rothman, J. E. & Lodish, H. F. Nature 269, 775–780 (1977).

    Article  ADS  CAS  Google Scholar 

  48. Baker, N. J. & Gandhi, S. S. Archs Virol. 52, 7–18 (1976).

    Article  CAS  Google Scholar 

  49. Colman, P. M., Jansonius, J. N. & Matthews, B. W. J. molec. Biol. 70, 701–724 (1972).

    Article  CAS  Google Scholar 

  50. Blok, J. & Air, G. M. Biochemistry 21, 4001–4007 (1982).

    Article  CAS  Google Scholar 

  51. Wrigley, N. G., Skehel, J. J., Charlwood, P. A. & Brand, C. M. Virology 51, 525–529 (1973).

    Article  CAS  Google Scholar 

  52. Lazdins, I., Haslam, E. A. & White, D. O. Virology 49, 758–765 (1972).

    Article  CAS  Google Scholar 

  53. McNamara, D. et al. Biochem. J. 205, 345–351 (1982).

    Article  CAS  Google Scholar 

Download references

Author information

Author notes

  1. W. G. Laver: Department of Microbiology, John Curtin School of Medical Research, Australian National University, Canberra, Australia

Authors and Affiliations

  1. Division of Protein Chemistry, CSIRO, Parkville, 3052, Victoria, Australia

    J. N. Varghese, W. G. Laver & P. M. Colman

Authors
  1. J. N. Varghese
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. W. G. Laver
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. M. Colman
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Varghese, J., Laver, W. & Colman, P. Structure of the influenza virus glycoprotein antigen neuraminidase at 2.9 Å resolution. Nature 303, 35–40 (1983). https://doi.org/10.1038/303035a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/303035a0

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing