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.

  • Letter
  • Published:

Structural basis for the binding of a globular antifreeze protein to ice

A Correction to this article was published on 06 February 1997

Abstract

ANTIFREEZE proteins (AFPs) have the unique ability to adsorb to ice and inhibit its growth1. Many organisms ranging from fish to bacteria use AFPs to retard freezing or lessen the damage incurred upon freezing and thawing2–6. The ice-binding mechanism of the long linear α-helical type I AFPs has been attributed to their regularly spaced polar residues matching the ice lattice along a pyramidal plane7,8. In contrast, it is not known how globular antifreeze proteins such as type III AFP that lack repeating ice-binding residues bind to ice. Here we report the 1.25 Å crystal structure of recombinant type III AFP (QAE iso-form9) from eel pout (Macrozoarces americanus), which reveals a remarkably flat amphipathic ice-binding site where five hydrogen-bonding atoms match two ranks of oxygens on the {10¯0} ice prism plane in the (0001) direction, giving high ice-binding affinity and specificity. This binding site, substantiated by the structures and properties of several ice-binding site mutants, suggests that the AFP occupies a niche in the ice surface in which it covers the basal plane while binding to the prism face.

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

Access options

Buy this article

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

Similar content being viewed by others

References

  1. Raymond, J. A. & DeVries, A. L. Proc. Natl Acad. Sci. USA 74, 2589–2593 (1977).

    Article  ADS  CAS  Google Scholar 

  2. Davies, P. L. & Hew, C. L. FASEB J. 4, 2460–2468 (1990).

    Article  CAS  Google Scholar 

  3. Duman, J. G., Xu, L., Neven, L. G., Tursmon, D. & Wu, D. W. in Insects at Low Temperatures (eds Lee, R. E. & Denlinger, D. L.) 94–127 (Chapman & Hall, New York, 1991).

    Book  Google Scholar 

  4. Griffith, M., Ala, P., Yang, D. S. C., Hon, W. C. & Moffat, B. A. Plant Physiol. 100, 593–596 (1992).

    Article  CAS  Google Scholar 

  5. Urrutia, M. E., Duman, J. G. & Knight, C. A. Biochim Biophys. Acta 1121, 199–206 (1992).

    Article  CAS  Google Scholar 

  6. Sun, X., Griffith, M., Pastemak, J. J. & Glick, B. R. Can. J. Microbiol. 41, 776–784 (1995).

    Article  CAS  Google Scholar 

  7. Knight, C. A., Cheng, C. C. & DeVries, A. L. Biophys. J. 59, 409–418 (1991).

    Article  CAS  Google Scholar 

  8. Sicheri, F. & Yang, D. S. C. Nature 375, 427–431 (1995).

    Article  ADS  CAS  Google Scholar 

  9. Chao, H., Davies, P. L., Sykes, B. D. & Sönnichsen, F. D. Prot Sci. 2, 1411–1428 (1993).

    Article  CAS  Google Scholar 

  10. Chao, H. thesis, Queen's Univ. (1994).

  11. Chao, H., Sönnichsen, F. D., DeLuca, C. I., Sykes, B. D. & Davies, P. L. Prot. Sci. 3, 1760–1769 (1994).

    Article  CAS  Google Scholar 

  12. Cheng, C. C. & DeVries, A. L. in Life Under Extreme Conditions (ed. di Prisco, G.) 1–14 (Springer, Berlin, 1991).

    Book  Google Scholar 

  13. Wen, D. & Laursen, R. A. Biophys. J. 63, 1659–1662 (1992).

    Article  ADS  CAS  Google Scholar 

  14. Jia, Z., DeLuca, C. I. & Davies, P. L. Prot. Sci. 4, 1236–1238 (1995).

    Article  CAS  Google Scholar 

  15. Hendrickson, W. A., Horton, J. R. & LeMaster, D. M. EMBO J. 9, 1665–1672 (1990).

    Article  CAS  Google Scholar 

  16. Otwinowski, Z. in Data Collection and Processing (eds Sawyer, L., Issacs, N. & Bailey, S.) 56–62 (SERC Daresbury Laboratory, Warrington, UK, 1993).

    Google Scholar 

  17. CCP4 Acta Crystallogr. D 50, 760–763 (1994).

  18. Sheldrick, G. M. SHELXS86. Program for the Solution of Crystal Structures (Univ. of Göttingen, Germany, 1986).

    Google Scholar 

  19. Otwinowski, Z. in Isomorphous Replacement and Anomalous Scattering (eds Sawyer, L., Issacs, N. & Bailey, S.) 80–86 (SERC Daresbury Laboratory, Warrington, UK, 1991).

    Google Scholar 

  20. Brünger, A. T. X-PLOR, Version 3.1. A System for X-ray Crystallography and NMR (Yale Univ. Press, New Haven, 1992).

    Google Scholar 

  21. Frishman, D. & Argos, P. Prot. Struct. Funct. Genet. 23, 566–579 (1995).

    Article  CAS  Google Scholar 

  22. Sönnichsen, F. D., Sykes, B. D., Chao, H. & Davies, P. L. Science 259, 1154–1157 (1993).

    Article  ADS  Google Scholar 

  23. Kraulis, P. J. J. Appl. Crystallogr. 24, 946–950 (1991).

    Article  Google Scholar 

  24. Merrit, E. A. & Murphy, M. E. P. Acta Crystallogr. D 50, 869–873 (1994).

    Article  Google Scholar 

  25. Evans, S. V. J. Mol. Graph. 11, 134–138 (1993).

    Article  CAS  Google Scholar 

  26. Kallungal, J. P. thesis, Syracuse Univ. (1975).

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jia, Z., DeLuca, C., Chao, H. et al. Structural basis for the binding of a globular antifreeze protein to ice. Nature 384, 285–288 (1996). https://doi.org/10.1038/384285a0

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/384285a0

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

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