Activation of the global gene regulator PrrA (RegA) from Rhodobacter sphaeroides

Biochemistry

Volumn 45, Issue 25, 2006, Pages 7872-7881

  Laguri, Cédric ^a,d   Stenzel, Rachelle A ^b   Donohue, Timothy J ^b   Phillips Jones, Mary K ^c   Williamson, Michael P ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF LEEDS   (United Kingdom)

^d INSTITUT DE BIOLOGIE STRUCTURALE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; DIMERIZATION; DNA; GELS; GENES; NUCLEAR MAGNETIC RESONANCE;

DNA BINDING SEQUENCES; INTERACTION SURFACE; PHOSPHORYLATION; RHODOBACTER SPHAEROIDES;

ENZYMES;

BERYLLIUM; DIMER; DNA; OXYGEN; PHOSPHATE; PHOSPHOTRANSFERASE; PROTEIN PRRA; PROTEIN PRRB; PROTEIN REGA; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BINDING SITE; CONTROLLED STUDY; DIFFUSION; DIMERIZATION; ESCHERICHIA COLI; GEL FILTRATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; REGULATOR GENE; RHODOBACTER SPHAEROIDES; TRANSCRIPTION REGULATION; ULTRACENTRIFUGATION;

AMINO ACID SEQUENCE; BERYLLIUM; CHROMATOGRAPHY, GEL; DIMERIZATION; DNA-BINDING PROTEINS; FLUORIDES; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN KINASES; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; RHODOBACTER SPHAEROIDES; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); ULTRACENTRIFUGATION;

RHODOBACTER SPHAEROIDES;

EID: 33746923497     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060683g     Document Type: Article

References (47)

1. Swem, L. R., Elsen, S., Bird, T. H., Swem, D. L., Koch, H. G., Myllykallio, H., Daldal, F., and Bauer, C. E. (2001) The RegB/RegA two-component regulatory system controls synthesis of photosynthesis and respiratory electron-transfer components in Rhodobacter capsulatus, J. Mol. Biol. 309, 121-138.
2. Oh, J. I., and Kaplan, S. (2000) Redox signaling: Globalization of gene expression, EMBO J. 19, 4237-4247.
3. Elsen, S., Swem, L. R., Swem, D. L., and Bauer, C. E. (2004) RegB/RegA, a highly conserved redox-responding global two-component regulatory system, Microbiol. Mol. Biol. Rev. 68, 263-279.
4. Elsen, S., Dischert, W., Colbeau, A., and Bauer, C. E. (2000) Expression of uptake hydrogenase and molybdenum nitrogenase in Rhodobacter capsulatus is coregulated by the RegB-RegA two-component regulatory system, J. Bacteriol. 182, 2831-2837.
5. Laratta, W. P., Choi, P. S., Tosques, I. E., and Shapleigh, J. P. (2002) Involvement of the PrrB/PrrA two-component system in nitrite respiration in Rhodobacter sphaeroides 2.4.3: Evidence for transcriptional regulation, J. Bacteriol. 184, 3521-3529.
6. Romagnoli, S., Packer, H. L., and Armitage, J. P. (2002) Tactic responses to oxygen in the phototrophic bacterium Rhodobacter sphaeroides WS8N, J. Bacteriol. 184, 5590-5598.
7. Robinson, V. L., Buckler, D. R., and Stock, A. M. (2000) A tale of two components: A novel kinase and a regulatory switch, Nat. Struct. Biol. 7, 626-633.
8. Masuda, S., Matsumoto, Y., Nagashima, K. V. P., Shimada, K., Inoue, K., Bauer, C. E., and Matsuura, K. (1999) Structural and functional analyses of photosynthetic regulatory genes regA and regB from Rhodovulum sulfidophilum, Roseobacter denitrificans, and Rhodobacter capsulatus, J. Bacteriol. 181, 4205-4215.
9. Emmerich, R., Hennecke, H., and Fischer, H. M. (2000) Evidence for a functional similarity between the two-component regulatory systems RegSR, ActSR, and RegBA (PrrBA) in α-proteobacteria, Arch. Microbiol. 174, 307-313.
10. Swem, L. R., Kraft, B. J., Swem, D. L., Setterdahl, A. T., Masuda, S., Knaff, D. B., Zaleski, J. M., and Bauer, C. E. (2003) Signal transduction by the global regulator RegB is mediated by a redox-active cysteine, EMBO J, 22, 4699-4708.
11. McEwan, A. G., Lewin, A., Davy, S. L., Boetzel, R., Leech, A., Walker, D., Wood, T., and Moore, G. R. (2002) PrrC from Rhodobacter sphaeroides, a homologue of eukaryotic Sco proteins, is a copper-binding protein and may have a thiol-disulfide oxidoreductase activity, FEBS Lett. 518, 10-16.
12. Lee, S. Y., Cho, H. S., Pelton, J. G., Yan, D., Berry, E. A., and Wemmer, D. E. (2001) Crystal structure of activated CheY, J. Biol. Chem. 276, 16425-16431.
13. Birck, C., Mourey, L., Gouet, P., Fabry, B., Schumacher, J., Rousseau, P., Kahn, D., and Samama, J. P. (1999) Conformational changes induced by phosphorylation of the FixJ receiver domain, Structure 7, 1505-1515.
14. Volkman, B. F., Nohaile, M. J., Amy, N. K., Kustu, S., and Wemmer, D. E. (1995) Three-dimensional solution structure of the N-terminal receiver domain of NtrC, Biochemistry 34, 1413-1424.
15. Laguri, C., Phillips-Jones, M. K., and 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.
16. 3 oxidase expression by multiple regulators in Rhodobacter capsulatus, J. Bacteriol. 184, 2815-2820.
17. Du, S. Y., Bird, T. H., and Bauer, C. E. (1998) DNA binding characteristics of RegA: A constitutively active anaerobic activator of photosynthesis gene expression in Rhodobacter capsulatus, J. Biol. Chem. 273, 18509-18513.
18. 1 promoter-operator region, J. Biol. Chem. 275, 19224-19230.
19. 2 gene by the photosynthesis response regulator, Mol. Microbiol. 34, 822-835.
20. II promoter-operator region with CbbR and RegA (PrrA) regulators indicate distinct mechanisms to control expression of the two cbb operons of Rhodobacter sphaeroides, J. Biol. Chem. 278, 16443-16450.
21. Hemschemeier, S. K., Kirndorfer, M., Hebermehl, M., and Klug, G. (2000) DNA binding of wild-type RegA protein and its differential effect on the expresion of pigment binding proteins in Rhodobacter capsulatus, J. Mol. Microbiol. Biotechnol. 2, 235-243.
22. Emmerich, R., Strehler, P., Hennecke, H., and Fischer, H. M. (2000) An imperfect inverted repeat is critical for DNA binding of the response regulator RegR of Bradyrhizobium japonicum, Nucleic Acids Res. 28, 4166-4171.
23. Baikalov, I., Schroder, I., Kaczor-Grzeskowiak, M., Grzeskowiak, K., Gunsalus, R. P., and Dickerson, R. E. (1996) Structure of the Escherichia coli response regulator NarL, Biochemistry 35, 11053-11061.
24. Djordjevic, S., Goudreau, P. N., Xu, Q. P., Stock, A. M., and West, A. H. (1998) Structural basis for methylesterase CheB regulation by a phosphorylation-activated domain, Proc. Natl. Acad. Sci. U.S.A. 95, 1381-1386.
25. Buckler, D. R., Zhou, Y. C., and Stock, A. M. (2002) Evidence of intradomain and interdomain flexibility in an OmpR/PhoB homolog from Thermotoga maritima, Structure 10, 153-164.
26. Robinson, V. L., Wu, T., and Stock, A. M. (2003) Structural analysis of the domain interface in DrrB, a response regulator of the OmpR/PhoB subfamily, J. Bacteriol. 185, 4186-4194.
27. Maris, A. E., Sawaya, M. R., Kaczor-Grzeskowiak, M., Jarvis, M. R., Bearson, S. M. D., Kopka, M. L., Schroder, I., Gunsalus, R. P., and Dickerson, R. E. (2002) Dimerization allows DNA target site recognition by the NarL response regulator, Nat. Struct. Biol. 9, 771-778.
28. Pelton, J. G., Kustu, S., and Wemmer, D. E. (1999) Solution structure of the DNA-binding domain of NtrC with three alanine substitutions, J. Mol. Biol. 292, 1095-1110.
29. Blanco, A. G., Sola, M., Gomis-Ruth, F. X., and Coll, M. (2002) Tandem DNA recognition by PhoB, a two-component signal transduction transcriptional activator, Structure 10, 701-713.
30. Zhao, H., Msadek, T., Zapf, J., Madhusudan, Hoch, J. A., and Varughese, K. I. (2002) DNA complexed structure of the key transcription factor initiating development in sporulating bacteria, Structure 10, 1041-1050.
31. Toro-Roman, A., Mack, T. R., and Stock, A. M. (2005) Structural analysis and solution studies of the activated regulatory domain of the response regulator ArcA: A symmetric dimer mediated by the α4-β5-α5 face, J. Mol. Biol. 349, 11-26.
32. 2 gene P2 promoter by the response regulator PrrA, J. Bacteriol. 184, 390-399.
33. Bird, T. H., Du, S. Y., and 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.
34. Yan, D., Cho, H. S., Hastings, C. A., Igo, M. M., Lee, S. Y., Pelton, J. G., Stewart, V., Wemmer, D. E., and Kustu, S. (1999) Beryllofluoride mimics phosphorylation of NtrC and other bacterial response regulators, Proc. Natl. Acad. Sci. U.S.A. 96, 14789-14794.
35. Philo, J. S. (2000) A method for directly fitting the time derivative of sedimentation velocity data and an alternative algorithm for calculating sedimentation coefficient distribution functions, Anal. Biochem. 279, 151-163.
36. Altieri, A. S., Hinton, D. P., and Byrd, R. A. (1995) Association of biomolecular systems via pulsed field gradient NMR self-diffusion measurements, J. Am. Chem. Soc. 117, 7566-7567.
37. Wilkins, D. K., Grimshaw, S. B., Receveur, V., Dobson, C. M., Jones, J. A., and Smith, L. J. (1999) Hydrodynamic radii of native and denatured proteins measured by pulse field gradient NMR techniques, Biochemistry 38, 16424-16431.
38. Jones, J. A., Wilkins, D. K., Smith, L. J., and Dobson, C. M. (1997) Characterisation of protein unfolding by NMR diffusion measurements, J. Biomol. NMR 10, 199-203.
39. Potter, C. A., Ward, A., Laguri, C., Williamson, M. P., Henderson, P. J. F., and Phillips-Jones, M. K. (2002) Expression, purification and characterisation of full-length histidine protein kinase RegB from Rhodobacter sphaeroides, J. Mol. Biol. 320, 201-213.
40. Comolli, J. C., and Donohue, T. J. (2002) Pseudomonas aeruginosa RoxR, a response regulator related to Rhodobacter sphaeroides PrrA, activates expression of the cyanide-insensitive terminal oxidase, Mol. Microbiol. 45, 755-768.
41. Yuan, H. S., Finkel, S. E., Feng, J. A., Kaczor-Grzeskowiak, M., Johnson, R. C., and Dickerson, R. E. (1991) The molecular structure of wild-type and a mutant FIS protein: Relationship between mutational changes and recombinational enhancer function or DNA binding, Proc. Natl. Acad. Sci. U.S.A. 88, 9558-9562.
42. Hemschemeier, S. K., Ebel, U., Jager, A., Balzer, A., Kirndorfer, M., and Klug, G. (2000) In vivo and in vitro analysis of RegA response regulator mutants of Rhodobacter capsulatus, J. Mol. Microbiol. Biotechnol. 2, 291-300.
43. - complex with phosphoserine phosphatase, Proc. Natl. Acad. Sci. U.S.A. 98, 8525-8530.
44. Gomelsky, M., and Kaplan, S. (1995) Isolation of regulatory mutants in photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1 and partial complementation of a PrrB mutant by the HupT histidine kinase, Microbiology 141, 1805-1819.
45. Jones, D. F., Stenzel, R. A., and Donohue, T. J. (2005) Mutational analysis of the C-terminal domain of the Rhodobacter sphaeroides response regulator PrrA, Microbiology 151, 4103-4110.
46. Laguri, C. (2003) Structural characterisation of PrrA from Rhodobacter sphaeroides, Ph.D. Thesis, University of Sheffield, Sheffield, U.K.
47. Roh, J. H., Smith, W. E., and Kaplan, S. (2004) Effects of oxygen and light intensity on transcriptome expression in Rhodobacter sphaeroides 2.4.1: Redox active gene expression profile, J. Biol. Chem. 279, 9146-9155.