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:

Structure and catalytic mechanism of the E. coli chemotaxis phosphatase CheZ

Nature Structural Biology volume 9, pages 570–575 (2002)Cite this article

A Corrigendum to this article was published on 01 September 2002

Abstract

The protein CheZ, which has the last unknown structure in the Escherichia coli chemotaxis pathway, stimulates the dephosphorylation of the response regulator CheY by an unknown mechanism. Here we report the co-crystal structure of CheZ with CheY, Mg2+ and the phosphoryl analog, BeF3−. The predominant structural feature of the CheZ dimer is a long four-helix bundle composed of two helices from each monomer. The side chain of Gln 147 of CheZ inserts into the CheY active site and is essential to the dephosphorylation activity of CheZ. Gln 147 may orient a water molecule for nucleophilic attack, similar to the role of the conserved Gln residue in the RAS family of GTPases. Similarities between the CheY–CheZ and Spo0F–Spo0B structures suggest a general mode of interaction for modulation of response regulator phosphorylation chemistry.

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

Figure 1: Overall structure of (CheY–BeF3−–Mg2+)2CheZ2.
Figure 2: Interactions between CheY and CheZcore and potential catalytic mechanism.

Similar content being viewed by others

Accession codes

Accessions

Protein Data Bank

References

  1. Bren, A. & Eisenbach, M. J. Bacteriol. 182, 6865–6873 (2000).

    Article  CAS  Google Scholar 

  2. Bourret, R.B. & Stock, A.M. J. Biol. Chem. 277, 9625–9628 (2002).

    Article  CAS  Google Scholar 

  3. Yi, T.M., Huang, Y., Simon, M.I. & Doyle, J. Proc. Natl. Acad. Sci. USA 97, 4649–4653 (2000).

    Article  CAS  Google Scholar 

  4. Duke, T.A., Novere, N.L. & Bray, D. J. Mol. Biol. 308, 541–553 (2001).

    Article  CAS  Google Scholar 

  5. Stock, A.M., Robinson, V.L. & Goudreau, P.N. Annu. Rev. Biochem. 69, 183–215 (2000).

    Article  CAS  Google Scholar 

  6. Segall, J.E., Manson, M.D. & Berg, H.C. Nature 296, 855–857 (1982).

    Article  CAS  Google Scholar 

  7. Stock, A.M. & Stock, J.B. J. Bacteriol. 169, 3301–3311 (1987).

    Article  CAS  Google Scholar 

  8. Boesch, K.C., Silversmith, R.E. & Bourret, R.B. J. Bacteriol. 182, 3544–3552 (2000).

    Article  CAS  Google Scholar 

  9. Sanna, M.G. & Simon, M.I. J. Bacteriol. 178, 6275–6280 (1996).

    Article  CAS  Google Scholar 

  10. McEvoy, M.M., Bren, A., Eisenbach, M. & Dahlquist, F.W. J. Mol. Biol. 289, 1423–1433 (1999).

    Article  CAS  Google Scholar 

  11. Blat, Y. & Eisenbach, M. Biochemistry 35, 5679–5683 (1996).

    Article  CAS  Google Scholar 

  12. Sanna, M.G., Swanson, R.V., Bourret, R.B. & Simon, M.I. Mol. Microbiol. 15, 1069–1079 (1995).

    Article  CAS  Google Scholar 

  13. Zhu, X., Volz, K. & Matsumura, P. J. Biol. Chem. 272, 23758–23764 (1997).

    Article  CAS  Google Scholar 

  14. Lukat, G.S., Stock, A.M. & Stock, J.B. Biochemistry 29, 5436–5442 (1990).

    Article  CAS  Google Scholar 

  15. Stock, A.M. et al. Biochemistry 32, 13375–13380 (1993).

    Article  CAS  Google Scholar 

  16. Blat, Y., Gillespie, B., Bren, A., Dahlquist, F.W. & Eisenbach, M. J. Mol. Biol. 284, 1191–1199 (1998).

    Article  CAS  Google Scholar 

  17. Wang, H. & Matsumura, P. Mol. Microbiol. 19, 695–703 (1996).

    Article  CAS  Google Scholar 

  18. Yan, D. et al. Proc. Natl. Acad. Sci. USA 96, 14789–14794 (1999).

    Article  CAS  Google Scholar 

  19. Lee, S.Y. et al. J. Biol. Chem. 276, 16425–16431 (2001).

    Article  CAS  Google Scholar 

  20. Blat, Y. & Eisenbach, M. J. Biol. Chem. 271, 1226–1231 (1996).

    Article  CAS  Google Scholar 

  21. Saul, F.A. & Alzari, P.M. Methods Mol. Biol. 66, 11–23 (1996).

    CAS  PubMed  Google Scholar 

  22. Silversmith, R.E., Smith, J.G., Guanga, G.P., Les, J.T. & Bourret, R.B. J. Biol. Chem. 276, 18478–18484 (2001).

    Article  CAS  Google Scholar 

  23. Lee, S.Y. et al. Nature Struct. Biol. 8, 52–56 (2001).

    Article  CAS  Google Scholar 

  24. Robinson, V.L., Buckler, D. & Stock, A.M. Nature Struct. Biol. 7, 626–633 (2000).

    Article  CAS  Google Scholar 

  25. Lukat, G.S., Lee, B.H., Mottonen, J.M., Stock, A.M. & Stock, J.B. J. Biol. Chem. 266, 8348–8354 (1991).

    CAS  PubMed  Google Scholar 

  26. Maegley, K.A., Admiraal, S.J. & Herschlag, D. Proc. Natl. Acad. Sci. USA 93, 8160–8166 (1996).

    Article  CAS  Google Scholar 

  27. Lowy, D.R. & Willumsen, B.M. Annu. Rev. Biochem. 62, 851–891 (1993).

    Article  CAS  Google Scholar 

  28. Scheffzek, K. et al. Science 277, 333–338 (1997).

    Article  CAS  Google Scholar 

  29. Zapf, J., Sen, U., Madhusudan, Hoch, J.A. & Varughese, K.I. Structure 8, 851–862 (2000).

    Article  CAS  Google Scholar 

  30. Mourey, L. et al. J. Biol. Chem. 276, 31074–31082 (2001).

    Article  CAS  Google Scholar 

  31. Reizer, J., Reizer, A., Perego, M. & Saier, M.H.J. Microb. Comp. Genomics 2, 103–111 (1997).

    Article  CAS  Google Scholar 

  32. Hess, J.F., Bourret, R.B. & Simon, M.I. Methods Enzymol. 200, 188–204 (1991).

    Article  CAS  Google Scholar 

  33. Bourret, R.B., Hess, J.F. & Simon, M.I. Proc. Natl. Acad. Sci. USA 87, 41–45 (1990).

    Article  CAS  Google Scholar 

  34. Otwinowski, Z. & Minor, W. Methods Enzymol. 276, 307–326 (1996).

    Article  Google Scholar 

  35. Terwilliger, T.C. & Berendzen, J. Acta Crystallogr. D 55, 849–861 (1999).

    Article  CAS  Google Scholar 

  36. Brünger, A.T. et al. Acta Crystallogr. D 54, 905–911 (1998).

    Article  Google Scholar 

  37. Jones, T.A., Zou, J.-Y., Cowan, S.W. & Kjeldgaard, M. Acta Crystallogr. A 47, 110–119 (1991).

    Article  Google Scholar 

  38. Esnouf, R.M. Acta Crystallogr. D 55, 938–940 (1999).

    Article  CAS  Google Scholar 

  39. Nicholls, A., Sharp, K. & Honig, B. Proteins 11, 281–296 (1991).

    Article  CAS  Google Scholar 

  40. Carson, M. J. Appl. Crystallogr. 24, 958–961 (1991).

    Article  Google Scholar 

Download references

Acknowledgements

We thank J. Snyder and M. Kimple (UNC Chapel Hill) for help collecting the native data set; D. Wemmer and S.-Y. Lee (UC Berkeley) for sharing the BeF3− parameter and topology files and the coordinates for the CheY–BeF3−-FliM structure before they were publicly accessible; G. Zhang (National Jewish Medical and Research Center) and H. Ke, D. Worthylake and M. Redinbo (UNC Chapel Hill) for helpful discussion; L. Betts (UNC X-ray facility) for technical support; X. Chen, M. Churchill and the X-ray Core Facility at the University of Colorado Health Science Center (UCHSC) for their support for the completion of R.Z.'s project at UCHSC; and the Brookhaven beamline staff for help with data collection.

Author information

Author notes

  1. Rui Zhao

    Present address: Department of Biochemistry and Molecular Genetics, University of Colorado Health Science Center, Denver, Colorado, 80262, USA

Authors and Affiliations

  1. Department of Microbiology and Immunology University of North Carolina, University of North Carolina, Chapel Hill, 27599-7290, North Carolina, USA

    Rui Zhao, Edward J. Collins, Robert B. Bourret & Ruth E. Silversmith

Authors
  1. Rui Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Edward J. Collins
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert B. Bourret
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ruth E. Silversmith
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ruth E. Silversmith.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhao, R., Collins, E., Bourret, R. et al. Structure and catalytic mechanism of the E. coli chemotaxis phosphatase CheZ. Nat Struct Mol Biol 9, 570–575 (2002). https://doi.org/10.1038/nsb816

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nsb816

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