1887

Abstract

Using a yeast two-hybrid assay system, it was demonstrated that the four-helix bundle of the PrrB histidine kinase both serves as the interaction site for the regulatory domain of its cognate response regulator PrrA and is the primary determinant of the interaction specificity. The -helix 1 and its flanking turn region within the dimerization domain (DD) of the PrrB histidine kinase appear to play an important role in conferring the recognition specificity for the PrrA response regulator on the DD. The catalytic ATP-binding domain of the histidine kinase, which functions as the catalytic unit for the phosphotransfer reaction from ATP to the conserved histidine residue in the DD, also appears to contribute to the enhancement of the recognition specificity conferred by the DD. It was also revealed that replacement of Asp-63 and Lys-113 of the PrrA response regulator by alanine abolished protein–protein interactions between PrrA and its cognate histidine kinase PrrB, whereas mutations of Asp-19, Asp-20 and Thr-87 to alanine did not affect protein–protein interactions, indicating that among the active site residues of PrrA, Asp-63 and Lys-113 are important not only in the function of PrrA but also for protein–protein interactions between PrrA and PrrB.

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2006-08-01
2024-03-28
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References

  1. Appleby J. L, Bourret R. B. 1998; Proposed signal transduction role for conserved CheY residue Thr87, a member of the response regulator active-site quintet. J Bacteriol 180:3563–3569
    [Google Scholar]
  2. Bird T. H, Du S, Bauer C. E. 1999; Autophosphorylation, phosphotransfer, and DNA-binding properties of the RegB/RegA two-component regulatory system in Rhodobacter capsulatus . J Biol Chem 274:16343–16348 [CrossRef]
    [Google Scholar]
  3. Brissette R. E, Tsung K. L, Inouye M. 1991; Suppression of a mutation in OmpR at the putative phosphorylation center by a mutant EnvZ protein in Escherichia coli . J Bacteriol 173:601–608
    [Google Scholar]
  4. Chien C. T, Bartel P. L, Sternglanz R, Fields S. 1991; The two-hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest. Proc Natl Acad Sci U S A 88:9578–9582 [CrossRef]
    [Google Scholar]
  5. Comolli J. C, Carl A. J, Hall C, Donohue T. 2002; Transcriptional activation of the Rhodobacter sphaeroides cytochrome c [sub]2[/sub] gene P2 promoter by the response regulator PrrA. J Bacteriol 184:390–399 [CrossRef]
    [Google Scholar]
  6. Dutta R, Qin L, Inouye M. 1999; Histidine kinases: diversity of domain organization. Mol Microbiol 34:633–640 [CrossRef]
    [Google Scholar]
  7. Eraso J. M, Kaplan S. 1994; prrA , a putative response regulator involved in oxygen regulation of photosynthesis gene expression in Rhodobacter sphaeroides . J Bacteriol 176:32–43
    [Google Scholar]
  8. Eraso J. M, Kaplan S. 1995; Oxygen-insensitive synthesis of the photosynthetic membranes of Rhodobacter sphaeroides : a mutant histidine kinase. J Bacteriol 177:2695–2706
    [Google Scholar]
  9. Grebe T. W, Stock J. B. 1999; The histidine protein kinase superfamily. Adv Microb Physiol 41:139–227
    [Google Scholar]
  10. Guthrie C, Fink G. R. 1991; Guide to yeast genetics and molecular biology. Methods Enzymol 194:1–932
    [Google Scholar]
  11. James P, Halladay J, Craig E. A. 1996; Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144:1425–1436
    [Google Scholar]
  12. Jessee J. 1986; New subcloning efficiency competent cells: >1×10[sup]6[/sup] transformants/μg. Focus 8:9
    [Google Scholar]
  13. Kiley P. J, Kaplan S. 1988; Molecular genetics of photosynthetic membrane biosynthesis in Rhodobacter sphaeroides . Microbiol Rev 52:50–69
    [Google Scholar]
  14. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685 [CrossRef]
    [Google Scholar]
  15. Laguri C, Phillips-Jones M. K, Williamson M. P. 2003; Solution structure and DNA binding of the effector domain from the global regulator PrrA (RegA) from Rhodobacter sphaeroides : insights into DNA binding specificity. Nucleic Acids Res 31:6778–6787 [CrossRef]
    [Google Scholar]
  16. Louret O. F, Doignon F, Crouzet M. 1997; Stable DNA binding yeast vector allowing high bait expression for use in the two-hybrid system. Bio Techniques 23:816–819
    [Google Scholar]
  17. Lukat G. S, Stock A. M, Stock J. B. 1990; Divalent metal ion binding to the CheY protein and its significance to phosphotransfer in bacterial chemotaxis. Biochemistry 29:5436–5442 [CrossRef]
    [Google Scholar]
  18. Lukat G. S, Lee B. H, Mottonen J. M, Stock A. M, Stock J. B. 1991; Roles of the highly conserved aspartate and lysine residues in the response regulator of bacterial chemotaxis. J Biol Chem 266:8348–8354
    [Google Scholar]
  19. Martinez-Argudo I, Martin-Nieto J, Salinas P, Maldonado R, Drummond M, Contreras A. 2001; Two-hybrid analysis of domain interactions involving NtrB and NtrC two-component regulators. Mol Microbiol 40:169–178 [CrossRef]
    [Google Scholar]
  20. Martinez-Argudo I, Salinas P, Maldonado R, Contreras A. 2002; Domain interactions on the ntr signal transduction pathway: two-hybrid analysis of mutant and truncated derivatives of histidine kinase NtrB. J Bacteriol 184:200–206 [CrossRef]
    [Google Scholar]
  21. Mattison K, Kenney L. J. 2002; Phosphorylation alters the interaction of the response regulator OmpR with its sensor kinase EnvZ. J Biol Chem 277:11143–11148 [CrossRef]
    [Google Scholar]
  22. Mayuri Bagchi G, Das T. K, Tyagi J. S. 2002; Molecular analysis of the dormancy response in Mycobacterium smegmatis : expression analysis of genes encoding the DevR-DevS two-component system, Rv3134c and chaperone α -crystallin homologues. FEMS Microbiol Lett 211:231–237
    [Google Scholar]
  23. Mouncey N. J, Kaplan S. 1998; Redox-dependent gene regulation in Rhodobacter sphaeroides 2.4.1[sup]T[/sup]: effects on dimethyl sulfoxide reductase (dor) gene expression. J Bacteriol 180:5612–5618
    [Google Scholar]
  24. Oh J. I, Kaplan S. 2001; Generalized approach to the regulation and integration of gene expression. Mol Microbiol 39:1116–1123 [CrossRef]
    [Google Scholar]
  25. Oh J. I, Ko I. J, Kaplan S. 2004; Reconstitution of the Rhodobacter sphaeroides cbb [sub]3[/sub]-PrrBA signal transduction pathway in vitro . Biochemistry 43:7915–7923 [CrossRef]
    [Google Scholar]
  26. Ohta N, Newton A. 2003; The core dimerization domains of histidine kinases contain recognition specificity for the cognate response regulator. J Bacteriol 185:4424–4431 [CrossRef]
    [Google Scholar]
  27. Park H, Saha S. K, Inouye M. 1998; Two-domain reconstitution of a functional protein histidine kinase. Proc Natl Acad Sci U S A 95:6728–6732 [CrossRef]
    [Google Scholar]
  28. Sambrook J, Fritsch E. F, Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd edn.. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  29. Schneider S, Buchert M, Hovens C. M. 1996; An in vitro assay of beta-galactosidase from yeast. Biotechniques 20:960–962
    [Google Scholar]
  30. Sola M, Lopez-Hernandez E, Cronet P, Lacroix E, Serrano L, Coll M, Parraga A. 2000; Towards understanding a molecular switch mechanism: thermodynamic and crystallographic studies of the signal transduction protein CheY. J Mol Biol 303:213–225 [CrossRef]
    [Google Scholar]
  31. Stock A. M, Martinez-Hackert E, Rasmussen B. F, West A. H, Stock J. B, Ringe D, Petsko G. A. 1993; Structure of the Mg[sup]2+[/sup]-bound form of CheY and mechanism of phosphoryl transfer in bacterial chemotaxis. Biochemistry 32:13375–13380 [CrossRef]
    [Google Scholar]
  32. Stock A. M, Robinson V. L, Goudreau P. N. 2000; Two-component signal transduction. Annu Rev Biochem 69:183–215 [CrossRef]
    [Google Scholar]
  33. Tanaka T, Saha S. K, Tomomori C. 12 other authors 1998; NMR structure of the histidine kinase domain of the E. coli osmosensor EnvZ. Nature 396:88–92 [CrossRef]
    [Google Scholar]
  34. Tomomori C, Tanaka T, Dutta R. 11 other authors 1999; Solution structure of the homodimeric core domain of Escherichia coli histidine kinase EnvZ. Nat Struct Biol 6:729–734 [CrossRef]
    [Google Scholar]
  35. Volz K, Matsumura P. 1991; Crystal structure of Escherichia coli CheY refined at 1.7-Å resolution. J Biol Chem 266:15511–15519
    [Google Scholar]
  36. West A. H, Stock A. M. 2001; Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 26:369–376 [CrossRef]
    [Google Scholar]
  37. Yanisch-Perron C, Vieira J, Messing J. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103–119 [CrossRef]
    [Google Scholar]
  38. Zapf J, Sen U, Madhusudan Hoch J. A, Varughese K. I. 2000; A transient interaction between two phosphorelay proteins trapped in a crystal lattice reveals the mechanism of molecular recognition and phosphotransfer in signal transduction. Structure 8:851–862 [CrossRef]
    [Google Scholar]
  39. Zeilstra-Ryalls J. H, Gomelsky M, Yeliseev A. A, Eraso J. M, Kaplan S. 1998; Transcriptional regulation of photosynthesis operons in Rhodobacter sphaeroides 2.4.1. Methods Enzymol 297:151–166
    [Google Scholar]
  40. Zundel C. J, Capener D. C, McCleary W. R. 1998; Analysis of the conserved acidic residues in the regulatory domain of PhoB. FEBS Lett 441:242–246 [CrossRef]
    [Google Scholar]
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