Skip to main content
SpringerLink
Log in

The binding of haem and zinc in the 1.9 Å X-ray structure of Escherichia coli bacterioferritin

  • Original Paper
  • Published:
JBIC Journal of Biological Inorganic Chemistry Aims and scope Submit manuscript

Abstract

The crystal structure of Escherichia coli bacterioferritin has been solved to 1.9 Å, and shows the symmetrical binding of a haem molecule on the local twofold axis between subunits and a pair of metal atoms bound to each subunit at the ferroxidase centre. These metals have been identified as zinc by the analysis of the structure and X-ray data and confirmed by microfocused proton-induced X-ray emission experiments. For the first time the haem has been shown to be linked to both the internal and the external environments via a cluster of waters positioned above the haem molecule.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Frolow F, Kalb A, Yariv J (1994) Nat Struct Biol 1:453–460

    Article  PubMed  CAS  Google Scholar 

  2. Dautant A, Meyer JB, Yariv J, Precigoux G, Sweet R, Kalb J, Frowlow F (1998) Acta Crystallogr D 54:16–24

    Article  PubMed  CAS  Google Scholar 

  3. van Eerde A, Wolterink-van Loo S, van der Oost J, Dijkstra BW (2006) Acta Crystallogr F 62:1061–1066

    Article  Google Scholar 

  4. Stillman TJ, Hempstead PD, Artymiuk PJ, Andrews SC, Hudson AJ, Treffry A, Guest JR, Harrison PM (2001) J Mol Biol 307:587–603

    Article  PubMed  CAS  Google Scholar 

  5. Janowski R, Auerbach-Nevo T, Weiss MS (2008) Protein Sci 17:1138–1150

    Article  PubMed  CAS  Google Scholar 

  6. Guy J (2004) PhD thesis, University of Exeter

  7. Laemmli U (1970) Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  8. Cianci M, Antonyuk S, Bliss N, Bailey MW, Buffey SG, Cheung KC, Clarke JA, Derbyshire GE, Ellis MJ, Enderby MJ, Grant AF, Holbourn MP, Laundy D, Nave C, Ryder R, Stephenson P, Helliwell JR, Hasnain SS (2005) J Synchrotron Radiat 12:455–466

    Article  PubMed  CAS  Google Scholar 

  9. Otwinowski Z, Minor W (1997) Methods Enzymol 267:21839–21843

    Google Scholar 

  10. French GS, Wilson KS (1978) Acta Crystallogr A 34:517

    Article  Google Scholar 

  11. Collaborative Computational Project, Number 4 (1994) Acta Crystallogr D 50:760–763

    Google Scholar 

  12. Cowtan K (1994) Joint CCP4/ESF-EACBM Newsl Protein Crystallogr 31:34–38

    Google Scholar 

  13. Grime GW (2004) In: Budnar M (ed) Tenth international conference on particle induced X-ray emission. Portoroz, Slovenia

  14. Campbell JL, Hopman TL, Maxwell JA, Nejedly Z (2000) Nucl Instrum Methods Phys Res B 170:193–204

    Article  CAS  Google Scholar 

  15. Garman EF, Grime GW (2005) Prog Biophys Mol Biol 89:173–205

    Article  PubMed  CAS  Google Scholar 

  16. Sheldrick GM (2008) Acta Crystallogr A 64:112–122

    Article  PubMed  Google Scholar 

  17. Emsley P, Cowtan K (2004) Acta Crystallogr D 60:2126–2132

    Article  PubMed  Google Scholar 

  18. Murshudov G, Vagin A, Dodson E (1997) Acta Crystallogr D 53:240–255

    Article  PubMed  CAS  Google Scholar 

  19. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  20. Vagin A, Teplyakov A (1997) J Appl Crystallogr 30:1022–1025

    Article  CAS  Google Scholar 

  21. Kabsch W (1976) Acta Crystallogr A 32:922–923

    Article  Google Scholar 

  22. Baaghil S, Thomson AJ, Moore GR, Le Brun NE (2002) J Chem Soc Dalton Trans 811–818

  23. Baaghil S, Lewin A, Moore GR, Le Brun NE (2003) Biochemistry 42:14047–14056

    Article  PubMed  CAS  Google Scholar 

  24. Kadir FHA, Al-Massad FK, Moore GR (1992) Biochem J 282:867–870

    PubMed  CAS  Google Scholar 

  25. Cromer DT (1983) J Appl Crystallogr 16:437–438

    Article  Google Scholar 

  26. Le Brun NE, Andrews SC, Guest JR, Harrison PM, Moore GR, Thomson AJ (1995) Biochem J 312:385–392

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank J.E. Guy for cloning of the AKR enzyme and Inma Gomez-Morilla at the University of Surrey Ion Beam Centre for assistance with the microPIXE experiments. We would also like to thank Chirotech Technology Limited, Cambridge, UK, and the BBSRC for funding of a studentship to S.C.W. The Synchrotron Radiation Source, Daresbury, UK, is acknowledged for provision of data collection facilities on the NWSGC MAD10 beamline funded by BBSRC grants (719/B15474 and 719/REI20571) and an NWDA project award (N0002170). We thank the station scientist Mark Ellis for assistance with data collection.

Author information

Authors and Affiliations

  1. School of Biosciences, Henry Wellcome Building for Biocatalysis, University of Exeter, Stocker Road, Exeter, EX4 4QD, UK

    Simon C. Willies, Michail N. Isupov & Jennifer A. Littlechild

  2. Department of Biochemistry, Rex Richards Building, University of Oxford, South Parks Road, Oxford, OX1 3QU, UK

    Elspeth F. Garman

Authors
  1. Simon C. Willies
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michail N. Isupov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elspeth F. Garman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jennifer A. Littlechild
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jennifer A. Littlechild.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Willies, S.C., Isupov, M.N., Garman, E.F. et al. The binding of haem and zinc in the 1.9 Å X-ray structure of Escherichia coli bacterioferritin. J Biol Inorg Chem 14, 201–207 (2009). https://doi.org/10.1007/s00775-008-0438-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00775-008-0438-8

Keywords

Search

Navigation