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.

  • Insight
  • Published:

Chitinases, chitosanases, and lysozymes can be divided into procaryotic and eucaryotic families sharing a conserved core

Nature Structural Biology volume 3, pages 133–140 (1996)Cite this article

Abstract

Barley chitinase, bacterial chitosanase, and lysozymes from goose (GEWL), phage (T4L) and hen (HEWL) all hydrolyse related polysaccharides. The proteins share no significant ammo-acid similarities, but have a structurally invariant core consisting of two helices and a three-stranded (β-sheet which form the substrate-binding and catalytic cleft. These enzymes represent a superfamily of hydrolases which are likely to have arisen by divergent evolution. Based on structural criteria, we divide the hydrolase superfamily into a bacterial family (chitosanase and T4L) and a eucaryotic family represented by chitinase and GEWL Both families contain the core but have differing N- and C-terminal domains. Inclusion of chitinase and chitosanase in the superfamily suggests the archetypal catalytic mechanism of the group is an inverting mechanism. The retaining mechanism of HEWL is unusual.

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

References

  1. Hart, P.J., Monzingo, A.F., Ready, M.P., Ernst, S.R. & Robertas, J.D. Crystal structure of an endochitinase from Hordeum vulgare L seeds. J. Mol. Biol. 229, 189–193 (1993).

    Article  CAS  Google Scholar 

  2. Hart, P.J., Pfluger, H.D., Monzingo, A.F., Hollis, T. & Robertus, J.D. The refined crystal structure of an endochitinase from Hordeum vulgare L seeds at 1.8 Å resolution. J. Mol. Biol. 248, 402–413 (1995).

    Article  CAS  Google Scholar 

  3. Marcotte, E., Monzingo, A.F., Ernst, S.R., Brzezinski, R. & Robertus, J.D. X-ray structure of an anti-fungal chitosanase from Streptomyces N174. Nature Struct Biol. 3, 155–162 (1996).

    Article  CAS  Google Scholar 

  4. Blake, C.C.F. et al. Structure of hen egg-white lysozyme. Nature 206, 757–761 (1965).

    Article  CAS  Google Scholar 

  5. Matthews, B.W. & Remington, S.J. The three dimensional structure of the lysozyme from bacteriophage T4. Proc. Natl. Acad. Sci. USA 71, 4178–4182 (1974).

    Article  CAS  Google Scholar 

  6. Rossmann, M.G. & Argos, P. Exploring structural homology of proteins. J. Mol. Biol. 105, 75–96 (1976).

    Article  CAS  Google Scholar 

  7. Matthews, B.W., Grütter, M.G. Anderson, W.F. & Remington, S.J. Common precursor of lysozymes of hen egg-white and bacteriophage T4. Nature 290, 334–335 (1981).

    Article  CAS  Google Scholar 

  8. Grütter, M.G., Weaver, L.H. & Matthews, B.W. Goose lysozyme structure: an evolutionary link between hen and bacteriophage lysozymes? Nature 303, 828–831 (1983).

    Article  Google Scholar 

  9. Thunnissen, A.W.H., Dijkstra, A.J., Kalk, K.H., Rozeboom, H.J., Engel, H., Keck, W., & Dijkstra, B.W. Doughnut-shaped structure of a bacterial muramidase revealed by X-ray crystallography. Nature 367, 750–753 (1994).

    Article  CAS  Google Scholar 

  10. Holm, L. & Sander, C. Structural similarity of plant chitinase and lysozyme from animals and phage. FEBS Lett. 340, 129–132 (1994).

    Article  CAS  Google Scholar 

  11. Jones, T.A. . in Computational Crystallography (ed. Sayre, D.) 303–317 (Oxford University Press, 1982).

    Google Scholar 

  12. Holm, L. & Sander, C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123–138 (1993).

    Article  CAS  Google Scholar 

  13. Kelly, J.A., Sielecki, A.R., Sykes, B.D., James, M.N.G. & Phillips, D.C. X-ray crystallography of the binding of the bacterial cell wall trisaccharide NAM-NAG-NAM to lysozyme. Nature 282, 875–878 (1979).

    Article  CAS  Google Scholar 

  14. Blake, C.C.F. et al. Crystallographic studies of the activity of hen egg-white lysozyme. Proc. Roy. Soc. B167, 378–388 (1967).

    Google Scholar 

  15. Withers, S.G. et al. Unequivocal demonstration of the involvement of a glutamate residue as a nucleophile in the mechanism of a “retaining” glycosidase. J. Am. Chem. Soc. 112, 5887–5889 (1990).

    Article  CAS  Google Scholar 

  16. Sinnot, M.L. Catalytic mechanisms of enzymic glycosyl transfer. Chem. Rev. 90, 1171–1202 (1990).

    Article  Google Scholar 

  17. Fukamizo, T., Koga, D. & Goto, S. Comparative biochemistry of chitinases-anomeric form of the reaction product. Biosci. Biotech. Biochem. 59, 311–313 (1995).

    Article  CAS  Google Scholar 

  18. Fukamizo, T., Honda, Y., Goto, S., Boucher, I. & Brzezinski, R. Reaction mechanism of chitosanase from Streptomyces sp. N174. Biochem. J. 311, 377–383 (1995).

    Article  CAS  Google Scholar 

  19. Kuroki, R., Weaver, L.H. & Matthews, B.W. A covalent enzyme-substrate intermediate with saccharide distortion in a mutant T4 lysozyme. Science 262, 2030–2033 (1993).

    Article  CAS  Google Scholar 

  20. Wang, Q., Graham, R.W., Trimbur, D., Warren, R.A.J. & Withers, S.G. Changing enzymatic reaction mechanisms by mutagenesis: conversion of a retaining glucosidase to an inverting enzyme. J. Am. Chem. Soc. 116, 11594–11595 (1994).

    Article  CAS  Google Scholar 

  21. Weaver, L.H., Grütter, M.G. & Matthews, B.W. The refined structures of goose lysozyme and its complex with a bound trisaccharide show that the “goose-type” lysozymes lack a catalytic aspartate residue. J. Mol. Biol. 245, 54–68 (1995).

    Article  CAS  Google Scholar 

  22. Robertus, J.D. et al. An X-ray crystallographic study of the binding of peptide chloromethyl ketone inhibitors to subtilisin BPN'. Biochemistry 11, 2439–2449 (1972).

    Article  CAS  Google Scholar 

  23. Thunnissen, A.W.H., Isaacs, N.W. & Dijkstra, B.W. The catalytic domain of a bacterial lytic transglycosylase defines a novel class of lysozymes. Proteins 22, 245–258 (1995).

    Article  CAS  Google Scholar 

  24. Henrissat, B. & Bairoch, A. New families in the classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J. 293, 781–788 (1993).

    Article  CAS  Google Scholar 

  25. Kraulis, J. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946–950 (1991).

    Article  Google Scholar 

  26. Sayle, R. RASMOL V2.5 Molecular visualization program (Glaxo Research and Development, 1994).

  27. Kuroki, R., Weaver, L.H. & Matthews, B.W. Structure-based design of a lysozyme with altered catalytic activity. Nature Struct. Biology 2, 1007–1011 (1995).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Chemistry and Biochemistry, University of Texas, Austin, Texas, 78712, USA

    Arthur F. Monzingo, Edward M. Marcotte, P. John Hart & Jon D. Robertas

Authors
  1. Arthur F. Monzingo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Edward M. Marcotte
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. John Hart
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jon D. Robertas
    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

Monzingo, A., Marcotte, E., Hart, P. et al. Chitinases, chitosanases, and lysozymes can be divided into procaryotic and eucaryotic families sharing a conserved core. Nat Struct Mol Biol 3, 133–140 (1996). https://doi.org/10.1038/nsb0296-133

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nsb0296-133

This article is cited by

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