Signal transduction by the global regulator RegB is mediated by a redox-active cysteine

EMBO Journal

Volumn 22, Issue 18, 2003, Pages 4699-4708

  Swem, Lee R ^a   Kraft, Brian J ^a   Swem, Danielle L ^a   Setterdahl, Aaron T ^b   Masuda, Shinji ^a   Knaff, David B ^b   Zaleski, Jeffrey M ^a   Bauer, Carl E ^a  

^a INDIANA UNIVERSITY   (United States)

^b TEXAS TECH UNIVERSITY   (United States)

Author keywords

Histidine kinase; Photosystem gene expression; Redox regulation; Rhodobacter capsulatus

Indexed keywords

AMINO ACID; CARBON; CYSTEINE; NITROGEN; PROTEIN REGB; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL METABOLISM; CARBON FIXATION; CONTROLLED STUDY; DISULFIDE BOND; ENZYME ACTIVITY; ENZYME STRUCTURE; GENE ACTIVITY; GENE FUNCTION; IN VITRO STUDY; NITROGEN FIXATION; NONHUMAN; OXIDATION; OXYGEN TENSION; PHOTOSYNTHESIS; PHOTOTROPHIC BACTERIUM; PRIORITY JOURNAL; REDUCTION; REGULATOR GENE; SENSOR; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CYSTEINE; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; PROTEIN KINASES; RHODOBACTER CAPSULATUS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); PHOTOBACTERIA; RHODOBACTER; RHODOBACTER CAPSULATUS;

EID: 0141848318     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg461     Document Type: Article

References (51)

1. Aslund, F., Zheng, M., Beckwith, J. and Storz, G. (1999) Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thioldisulfide status. Proc. Natl Acad. Sci. USA, 96, 6161-6165.
2. Astley, T., Ellis, P.J., Freeman, H.C., Hitchman, M.A., Keene, F.R. and Tiekink, E.R.T. (1995) Extended x-ray absorption fine structure, crystal structures at 295 and 173 K and electron paramagnetic resonance and electronic spectra of bis[tris(2-pyridyl)methane]copper(II) dinitrate. J. Chem. Soc. Dalton Trans., 595-601.
3. Bauer, C.E., Young, D.A. and Marrs, B.L. (1988) Analysis of the Rhodobacter capsulatus puf operon. Location of the oxygen-regulated promoter region and the identification of an additional puf-encoded gene. J. Biol. Chem., 263, 4820-4827.
4. Beers, J., Glerum, D.M. and Tzagoloff, A. (2002) Purification and characterization of yeast Scolp, a mitochondrial copper protein. J. Biol. Chem., 277, 22185-22190.
5. Bemarducci, E., Schwindinger, W.F., Hughey, J.L. IV, Krogh-Jespersen, K. and Schugar, H.J. (1981) Electronic spectra of copper(II)-imidazole and copper(II)-pyrazole chromophores. J. Am. Chem. Soc., 103, 1686-1691.
6. Bird, T.H., Du, S. 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.
7. Brenner, A.J. and Harris, E.D. (1995) A quantitative test for copper using bicinchoninic acid. Anal. Biochem., 226, 80-84.
8. Buggy, J. and Bauer, C.E. (1995) Cloning and characterization of senC, a gene involved in both aerobic respiration and photosynthesis gene expression in Rhodobacter capsulatus. J. Bacteriol., 177, 6958-6965.
9. Cervantes, C. and Gutierrez-Corona, F. (1994) Copper resistance mechanisms in bacteria and fungi. FEMS Microbiol. Rev., 14, 121-137.
10. Chen, W., Jager, A. and Klug, G. (2000) Correction of the DNA sequence of the regB gene of Rhodobacter capsulatus with implications for the membrane topology of the sensor kinase regB. J. Bacteriol., 182, 818-820.
11. Dong, C., Elsen, S., Swem, L.R. and Bauer, C.E. (2002) AerR, a second aerobic repressor of photosynthesis gene expression in Rhodobacter capsulatus. J. Bacteriol., 184, 2805-2814.
12. Du, S., Kouadio, J.L. and Bauer, C.E. (1999) Regulated expression of a highly conserved regulatory gene cluster is necessary for controlling photosynthesis gene expression in response to anaerobiosis in Rhodobacter capsulatus. J. Bacteriol., 181, 4334-4341.
13. 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.
14. Eraso, J.M. and Kaplan, S. (2000) From redox flow to gene regulation: role of the PrrC protein of Rhodobacter sphaeroides 2.4.1. Biochemistry, 39, 2052-2062.
15. Fawcett, T.G., Bernarducci, E.E., Krogh-Jespersen, K. and Schugar, H.J. (1980) Charge-transfer absorptions of copper(II)-imidazole and copper(II)-imidazolate chromophores. J. Am. Chem. Soc., 102, 2598-2604.
16. Gaffney, B.J. and Silverstone, H.J. (1993) Biological magnetic resonance. In Reuben, J. and Berliner, J. (eds), NMR of Paramagnetic Molecules, Vol. 13. Plenum Press, New York, NY, p. 1.
17. Georgellis, D., Kwon, O. and Lin, E.C. (2001) Quinones as the redox signal for the arc two-component system of bacteria. Science, 292, 2314-2316.
18. Grebe, T.W. and Stock, J.B. (1999) The histidine protein kinase superfamily. Adv. Microb. Physiol., 41, 139-227.
19. Hathaway, B.J. (1987) Copper. In Wilkinson, G. (ed.), Comprehensive Coordination Chemistry. Pergamon Press, Oxford, UK, pp. 662-674.
20. Hemmert, C., Renz, M., Gornitzka, H. and Meunier, B. (1999) Synthesis, characterization and crystal structures of copper(II) complexes containing multidentate polypyridine ligands. J. Chem. Soc. Dalton Trans., 3989-3994.
21. Hirasawa, M., Hurley, J.K., Salamon, Z., Tollin, G., Markley, J.L., Cheng, H., Xia, B. and Knaff, D.B. (1998) The role of aromatic and acidic amino acids in the electron transfer reaction catalyzed by spinach ferredoxin-dependent glutamate synthase. Biochim. Biophys Acta, 1363, 134-146.
22. Huang, G.-S., Lai, J.-K., Ueng, C.-H. and Su, C.-C. (2000) Molecular and electronic structures of bis(dipicolylamine)copper(II) perchlorate and bis[2-(2-pyridylethyl)picolylamine]copper(II) perchlorate. Transit. Met. Chem., 25, 84-92.
23. Innes, K.K., Ross, I.G. and Moomaw, W.R. (1988) Electronic states of azabenzenes and azanaphthalenes: a revised and extended critical review. J. Mol. Spectrosc., 132, 492-544.
24. Inoue, K., Mosley, C., Kouadio, J.-L. and Bauer, C.E. (1995) Isolation and in vitro phosphorylation of sensory transduction components controlling anaerobic induction of light harvesting and reaction center gene expression in R.capsulatus. Biochemistry, 34, 391-396.
25. Jones, D.P. (2002) Redox potential of GSH/GSSG couple: assay and biological significance. Methods Enzymol., 348, 93-112.
26. Kim, S.O., Merchant, K., Nudelman, R., Beyer, W.F., Jr, Keng, T., DeAngelo, J., Hausladen, A. and Stamler, J.S. (2002) OxyR: a molecular code for redox-related signaling. Cell, 109, 383-396.
27. Krimm, I., Lemaire, S., Ruelland, E., Miginiac-Maslow, M., Jaquot, J.P., Hirasawa, M., Knaff, D.B. and Lancelin, J.M. (1998) The single mutation Trp35→Ala in the 35-40 redox site of Chlamydomonas reinhardtii thioredoxin h affects its biochemical activity and the pH dependence of C36-C39 1H-13C NMR. Eur. J. Biochem., 255, 185-195.
28. Lamb, A.L., Torres, A.S., O'Halloran, T.V. and Rosenzweig, A.C. (2000) Heterodimer formation between superoxide dismutase and its copper chaperone. Biochemistry, 39, 14720-14727.
29. Lever, A.B.P. (1984) Studies in Physical and Theoretical Chemistry, Vol. 33: Inorganic Electronic Spectroscopy, 2nd edn. Elsevier, Amsterdam, The Netherlands.
30. Masuda, S., Matsumoto, Y., Nagashima, K.V., 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.
31. Masuda, S., Dong, C., Swem, D., Setterdahl, A.T., Knaff, D.B. and Bauer, C.E. (2002) Repression of photosynthesis gene expression by formation of a disulfide bond in CrtJ. Proc. Natl Acad. Sci. USA, 99, 7078-7083.
32. 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.
33. McLachlan, G.A., Fallon, G.D., Martin, R.L. and Spiccia, L. (1995) Synthesis, structure and properties of five-coordinate copper(II) complexes of entadentate ligands with pyridyl pendant arms. Inorg. Chem., 34, 254-261.
34. Miyatake, H. et al. (2000) Sensory mechanism of oxygen sensor FixL from Rhizobium meliloti: crystallographic, mutagenesis and resonance Raman spectroscopic studies. J. Mol. Biol., 301, 415-431.
35. Mosley, C.S., Suzuki, J.Y. and Bauer, C.E. (1995) Identification and molecular genetic characterization of a sensor kinase responsible for coordinately regulating light harvesting and reaction center gene expression in response to anaerobiosis. J. Bacteriol., 177, 3359.
36. Neese, F. (1995) The EPR program. Quantum Chemistry Program Exchange, Bull., 15, 5.
37. Nittis, T., George, G.N. and Winge, D.R. (2001) Yeast Scol, a protein essential for cytochrome c oxidase function is a Cu(I)-binding protein. J. Biol. Chem., 276, 42520-42526.
38. Ouchane, S. and Kaplan, S. (1999) Topological analysis of the membrane-localized redox-responsive sensor kinase PrrB from Rhodobacter sphaeroides 2.4.1. J. Biol. Chem., 274, 17290-17296.
39. Paget, M.S., Bae, J.B., Hahn, M.Y., Li, W., Kleanthous, C., Roe, J.H. and Buttner, M.J. (2001) Mutational analysis of RsrA, a zinc-binding anti-σ factor with a thiol-disulphide redox switch. Mol. Microbiol., 39, 1036-1047.
40. Peisach, J. and Blumberg, W.E. (1974) Structural implications derived from the analysis of EPR spectra of natural and artificial copper proteins. Arch. Biochem. Biophys., 165, 691-708.
41. Potter, C.A., Ward, A., Laguri, C., Williamson, M.P., Henderson, P.J. and Phillips-Jones, M.K. (2002) Expression, purification and characterization of full-length histidine protein kinase RegB from Rhodobacter sphaeroides. J. Mol. Biol., 320, 201-213.
42. Roh, J.H. and Kaplan, S. (2000) Genetic and phenotypic analyses of the rdx locus of Rhodobacter sphaeroides 2.4.1. J. Bacteriol., 182, 3475-3481.
43. 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.
44. Saito, H. (2001) Histidine phosphorylation and two-component signaling in eukaryotic cells. Chem. Rev., 101, 2497-2509.
45. Setterdahl, A. et al. (2000) Oxidation-reduction properties of two engineered redox-sensitive mutant Escherichia coli malate dehydrogenases. Arch. Biochem. Biophys., 382, 15-21.
46. Sganga, M.W. and Bauer, C.E. (1992) Regulatory factors controlling photosynthetic reaction center and light-harvesting gene expression in Rhodobacter capsulatus. Cell, 68, 945-954.
47. Silver, S. (1996) Transport of inorganic cations. In Neidhardt, F.C. (ed.), Escherichia coli and Salmonella Cellular and Molecular Biology. ASM Press, Washington DC, pp. 1091-1102.
48. 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.
49. Vichivanives, P., Bird, T.H., Bauer, C.E. and Robert Tabita, F. (2000) Multiple regulators and their interactions in vivo and in vitro with the cbb regulons of Rhodobacter capsulatus. J. Mol Biol., 300, 1079-1099.
50. Wang, W. and Malcolm, B.A. (1999) Two-stage PCR protocol allowing introduction of multiple mutations, deletions and insertions using QuikChange site-directed mutagenesis. Biotechniques, 26, 680-682.
51. 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.