NMR structure of the histidine kinase domain of the E. coli osmosensor EnvZ

Nature volume 396, pages88–92(1998)Cite this article

Abstract

Bacteria live in capricious environments, in which they must continuously sense external conditions in order to adjust their shape, motility and physiology1. The histidine–aspartate phosphorelay signal-transduction system (also known as the two-component system) is important in cellular adaptation to environmental changes in both prokaryotes and lower eukaryotes2,3. In this system, protein histidine kinases function as sensors and signal transducers. The Escherichia coli osmosensor, EnvZ, is a transmembrane protein with histidine kinase activity in its cytoplasmic region2. The cytoplasmic region contains two functional domains4: domain A (residues 223–289) contains the conserved histidine residue (H243), a site of autophosphorylation as well as transphosphorylation to the conserved D55 residue of response regulator OmpR, whereas domain B (residues 290–450) encloses several highly conserved regions (G1, G2, F and N boxes) and is able to phosphorylate H243. Here we present the solution structure of domain B, the catalytic core of EnvZ. This core has a novel protein kinase structure, distinct from the serine/threonine/tyrosine kinase fold, with unanticipated similarities to both heat-shock protein 90 and DNA gyrase B.

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Figure 1: Sequence and structure of the EnvZ catalytic domain.
Figure 2: Identification of the ATP-binding domain in EnvZ and the involvement of N347 in ATP binding.
Figure 3: EnvZ and Hsp90 have a similar fold in their ATP-binding regions.
Figure 4: The EnvZ catalytic domain and DNA gyrase B.

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Acknowledgements

We thank L. Kay for providing NMR pulse sequences, L. Pearl for the Hsp90-ATP coordinates before PDB release and discussions, and S. Bagby for comments on the manuscript. This work was supported by grants from JSPS (to T.T.) from CREST (to M.K.) from the NIH (to M. Inouye), and from HHMI (to M. Ikura). R.I. and D.L. acknowledge HFSP postdoctoral fellowships. M. Ikura is an HHMI International Research Scholar and MRCC Scientist.

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Author notes

  1. Mark B. Swindells

    Present address: Inpharmatica Ltd, 60 Charlotte Street, London, W1P 2AX, UK

Affiliations

  1. Center for Tsukuba Advanced Research Alliance and Institute of Applied Biochemistry, University of Tsukuba, Tsukuba, 305-8577, Japan

    Toshiyuki Tanaka & Chieri Tomomori

  2. Department of Biochemistry, Robert Wood Johnson Medical School, University of Medicine and Dentistry of New Jersey, New Jersey, 08854, USA

    Soumitra K. Saha, Heiyoung Park, Rinku Dutta, Ling Qin & Masayori Inouye

  3. Division of Molecular and Structural Biology, Ontario Cancer Institute and Department of Medical Biophysics, University of Toronto, 610 University Avenue, Toronto, M5G 2M9, Ontario, Canada

    Rieko Ishima, Dingjiang Liu, Kit I. Tong & Mitsuhiko Ikura

  4. Helix Research Institute Inc., Kisarazu, 292-0812, Japan

    Mark B. Swindells

  5. National Institute of Agrobiological Resources, Tsukuba, 305-0856, Japan

    Toshimasa Yamazaki

  6. Department of Chemistry, Tokyo Metropolitan University, Hachioji, 192-0397, Japan

    Akira M. Ono & Masatsune Kainosho

Authors
  1. Toshiyuki Tanaka
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  2. Soumitra K. Saha
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  10. Mark B. Swindells
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  15. Mitsuhiko Ikura
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Correspondence to Mitsuhiko Ikura.

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Tanaka, T., Saha, S., Tomomori, C. et al. NMR structure of the histidine kinase domain of the E. coli osmosensor EnvZ. Nature 396, 88–92 (1998). https://doi.org/10.1038/23968

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