Structural characterization of Escherichia coli sensor histidine kinase EnvZ: The periplasmic C-terminal core domain is critical for homodimerization

Biochemical Journal

Volumn 385, Issue 1, 2005, Pages 255-264

  Khorchid, Ahmad ^a   Inouye, Masayori ^b   Ikura, Mitsuhiko ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Bacterial signal transduction; Membrane receptor; NMR; Osmolarity; Stress response

Indexed keywords

BIOCHEMISTRY; BIOSENSORS; CELLS; CENTRIFUGATION; CHARACTERIZATION; DIMERIZATION; ESCHERICHIA COLI; HYDROPHOBICITY; MOLECULAR STRUCTURE; SODIUM CHLORIDE;

BIOPHYSICAL CHARACTERIZATION; CELL ADAPTATION; EXTRACELLULAR OSMOLARITY; HOMODIMERIC SUBUNITS; HOMODIMERIZATION;

ENZYMES;

ALANINE; ARGININE; GLUTAMINE; PROTEIN HISTIDINE KINASE; PROTEIN HISTIDINE KINASE ENVZ; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; BIOCHEMISTRY; CARBOXY TERMINAL SEQUENCE; CONCENTRATION RESPONSE; CYTOPLASM; DIMERIZATION; ENZYME STRUCTURE; ESCHERICHIA COLI; HYDROPHOBICITY; NONHUMAN; OSMOLARITY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN SECONDARY STRUCTURE; SENSITIVITY ANALYSIS; ULTRACENTRIFUGATION;

AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; CONSERVED SEQUENCE; DIMERIZATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; LEUCINE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIENZYME COMPLEXES; PERIPLASM; PROTEIN KINASES; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 12744271881     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20041125     Document Type: Article

References (36)

1. Mizuno, T. (1998) His-Asp phosphotransfer signal transduction. J. Biochem. (Tokyo) 123, 555-563
2. Falke, J. J., Bass, R. B., Butler, S. L., Chervitz, S. A. and Danielson, M. A. (1997) The two-component signaling pathway of bacterial chemotaxis: a molecular view of signal transduction by receptors, kinases, and adaptation enzymes. Annu. Rev. Cell Dev. Biol. 13, 457-512
3. West, A. H. and Stock, A. M. (2001) Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem. Sci. 26, 369-376
4. Mizuno, T., Wurtzel, E. T. and Inouye, M. (1982) Osmoregulation of gene expression. II. DNA sequence of the envZ gene of the ompB operon of Escherichia coli and characterization of its gene product. J. Biol. Chem. 257, 13692-13698
5. Forst, S., Comeau, D., Norioka, S. and Inouye, M. (1987) Localization and membrane topology of EnvZ, a protein involved in Osmoregulation of OmpF and OmpC in Escherichia coli. J. Biol. Chem. 262, 16433-16438
6. Park, H., Saha, S. K. and Inouye, M. (1998) Two-domain reconstitution of a functional protein histidine kinase. Proc. Natl. Acad. Sci. U.S.A. 95, 6728-6732
7. Muller-Dieckmann, H. J. and Kim, S.-H. (2003) Structure-function relationships: chemotaxis and ethylene receptors. In Histidine Kinases in Signal Transduction (Inouye, M. and Dutta, R., eds.), pp. 123-141, Academic Press, San Diego
8. Yang, Y. and Inouye, M. (1993) Requirement of both kinase and phosphatase activities of an Escherichia coli receptor (Taz1) for ligand-dependent signal transduction. J. Mol. Biol. 231, 335-342
9. Jin, T. and Inouye, M. (1993) Ligand binding to the receptor domain regulates the ratio of kinase to phosphatase activities of the signaling domain of the hybrid Escherichia coli transmembrane receptor, Taz1. J. Mol. Biol. 232, 484-492
10. Mizuno, T. and Mizushima, S. (1990) Signal transduction and gene regulation through the phosphorylation of two regulatory components: the molecular basis for the osmotic regulation of the porin genes. Mol. Microbiol. 4, 1077-1082
11. Utsumi, R., Brissette, R. E., Rampersaud, A., Forst, S. A., Oosawa, K. and Inouye, M. (1989) Activation of bacterial porin gene expression by a chimeric signal transducer in response to aspartate. Science 245, 1246-1249
12. Baumgartner, J. W., Kim, C., Brissette, R. E., Inouye, M., Park, C. and Hazelbauer, G. L. (1994) Transmembrane signalling by a hybrid protein: communication from the domain of chemoreceptor Trg that recognizes sugar-binding proteins to the kinase/phosphatase domain of osmosensor EnvZ. J. Bacteriol. 176, 1157-1163
13. Jin, T. and Inouye, M. (1994) Transmembrane signaling: mutational analysis of the cytoplasmic linker region of Taz1-1, a Tar-EnvZ chimeric receptor in Escherichia coli. J. Mol. Biol. 244, 477-481
14. Zhu, Y. and Inouye, M. (2003) Analysis of the role of the EnvZ linker region in signal transduction using a chimeric Tar/EnvZ receptor protein, Tez1. J. Biol. Chem. 278, 22812-22819
15. Tokishita, S., Kojima, A. and Mizuno, T. (1992) Transmembrane signal transduction and osmoregulation in Escherichia coli: functional importance of the transmembrane regions of membrane-located protein kinase, EnvZ. J. Biochem. (Tokyo) 111, 707-713
16. Tokishita, S. and Mizuno, T. (1994) Transmembrane signal transduction by the Escherichia coli osmotic sensor, EnvZ: intermolecular complementation of transmembrane signalling. Mol. Microbiol. 13, 435-444
17. + stimulates specifically the autokinase activity of purified and reconstituted EnvZ of Escherichia coil J. Biol. Chem. 276, 40896-40902
18. Leonardo, M. R. and Forst, S. (1996) Re-examination of the role of the periplasmic domain of EnvZ in sensing of osmolarity signals in Escherichia coli. Mol. Microbiol. 22, 405-413
19. Waukau, J. and Forst, S. (1999) Identification of a conserved N-terminal sequence involved in transmembrane signal transduction in EnvZ. J. Bacteriol. 181, 5534-5538
20. Yaku, H. and Mizuno, T. (1997) The membrane-located osmosensory kinase, EnvZ, that contains a leucine zipper-like motif functions as a dimer in Escherichia coli. FEBS Lett. 417, 409-413
21. Lepre, C. A. and Moore, J. M. (1998) Microdrop screening: a rapid method to optimize solvent conditions for NMR spectroscopy of proteins. J. Biomol. NMR 12, 493-499
22. Egger, L. A. and Inouye, M. (1997) Purification and characterization of the periplasmic domain of EnvZ osmosensor in Escherichia coli. Biochem. Biophys. Res. Commun. 231, 68-72
23. Ouali, M. and King, R. D. (2000) Cascaded multiple classifiers for secondary structure prediction. Protein Sci. 9, 1162-1176
24. Seiden, L. A., Kinosian, H. J., Estes, J. E. and Gershman, L. C. (1994) Influence of the high affinity divalent cation on actin tryptophan fluorescence. Adv. Exp. Med. Biol. 358, 51-57
25. Gross, M., Lustig, A., Wallimann, T. and Furter, R. (1995) Multiple-state equilibrium unfolding of guanidino kinases. Biochemistry 34, 10350-10357
26. Haq, S. K., Rasheedi, S. and Khan, R. H. (2002) Characterization of a partially folded intermediate of stem bromelain at low pH. Eur. J. Biochem. 269, 47-52
27. Pawar, S. A. and Deshpande, V. V. (2000) Characterization of acid-induced unfolding intermediates of glucose/xylose isomerase. Eur. J. Biochem. 267, 6331-6338
28. Bagby, S., Tong, K. I. and Ikura, M. (2001) Optimization of protein solubility and stability for protein nuclear magnetic resonance. Methods Enzymol. 339, 20-41
29. Zappacosta, F, Pessi, A., Bianchi, E., Venturini, S., Sollazzo, M., Tramontano, A., Marino, G. and Pucci, P. (1996) Probing the tertiary structure of proteins by limited proteolysis and mass spectrometry: the case of Minibody. Protein Sci. 5, 802-813
30. Tomomori, C., Tanaka, T., Dutta, R., Park, H., Saha, S. K., Zhu, Y., Ishima, R., Liu, D., Tong, K. I., Kurokawa, H. et al. (1999) Solution structure of the homodimeric core domain of Escherichia coli histidine kinase EnvZ. Nat. Struct. Biol. 6, 729-734
31. Zoetewey, D. L., Tripet, B. P., Kutateladze, T. G., Overduin, M. J., Wood, J. M. and Hodges, R. S. (2003) Solution structure of the C-terminal antiparallel coiled-coil domain from Escherichia coli osmosensor ProP. J. Mol. Biol. 334, 1063-1076
32. Culham, D. E., Tripet, B., Racher, K. I., Voegele, R. T, Hodges, R. S. and Wood, J. M. (2000) The role of the carboxyl terminal α-helical coiled-coil domain in osmosensing by transporter ProP of Escherichia coli. J. Mol. Recognit. 13, 309-322
33. Chervitz, S. A. and Falke, J. J. (1996) Molecular mechanism of transmembrane signaling by the aspartate receptor: a model. Proc. Natl. Acad. Sci. U.S.A. 93, 2545-2550
34. Ottemann, K. M., Xiao, W., Shin, Y. K. and Koshland, Jr, D. E. (1999) A piston model for transmembrane signaling of the aspartate receptor. Science 285, 1751-1754
35. Maruyama, I. N., Mikawa, Y. G. and Maruyama, H. I. (1995) A model for transmembrane signalling by the aspartate receptor based on random-cassette mutagenesis and site-directed disulfide cross-linking. J. Mol. Biol. 253, 530-546
36. Cochran, A. G. and Kim, P. S. (1996) Imitation of Escherichia coli aspartate receptor signaling in engineered dimers of the cytoplasmic domain. Science 271, 1113-1116