Oxidation of a single active site suffices for the functional inactivation of the dimeric Bacillus subtilis OhrR repressor in vitro

Nucleic Acids Research

Volumn 37, Issue 4, 2009, Pages 1174-1181

  Eiamphungporn, Warawan ^a   Soonsanga, Sumarin ^a   Lee, Jin Won ^b   Helmann, John D ^a  

^a Cornell University ^*  (United States)

^b Hanyang University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CYSTEINE; MONOMER; PROTEIN OHRR; REPRESSOR PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BACILLUS SUBTILIS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA BINDING; ENZYME ACTIVE SITE; GENE LOCUS; HUMAN; IN VITRO STUDY; MUTATIONAL ANALYSIS; OXIDATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; WILD TYPE;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; BENZENE DERIVATIVES; CYSTEINE; LINOLEIC ACIDS; LIPID PEROXIDES; MUTATION; OXIDANTS; OXIDATION-REDUCTION; PEROXIDES; REPRESSOR PROTEINS; RNA, MESSENGER;

BACILLUS SUBTILIS;

EID: 62549099131     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn1052     Document Type: Article

References (31)

1. Hong,M., Fuangthong,M., Helmann,J.D. and Brennan,R.G. (2005) Structure of an OhrR-ohrA operator complex reveals the DNA binding mechanism of the MarR family. Mol. Cell, 20, 131-141.
2. Mongkolsuk,S. and Helmann,J.D. (2002) Regulation of inducible peroxide stress responses. Mol. Microbiol, 45, 9-15.
3. Fuangthong,M., Atichartpongkul,S., Mongkolsuk,S. and Helmann,J.D. (2001) OhrR is a repressor of ohrA, a key organic hydroperoxide resistance determinant in Bacillus subtilis. J. Bacteriol., 183 4134-4141.
4. Panmanee,W., Vattanaviboon,P., Eiamphungporn,W., Whangsuk,W., Sallabhan,R. and Mongkolsuk,S. (2002) OhrR, a transcription repressor that senses and responds to changes in organic peroxide levels in Xanthomonas campestris pv. phaseoli. Mol. Microbiol., 45, 1647-1654.
5. Panmanee,W., Vattanaviboon,P., Poole,L.B. and Mongkolsuk,S. (2006) Novel organic hydroperoxide-sensing and responding mechanisms for OhrR, a major bacterial sensor and regulator of organic hydroperoxide stress. J. Bacteriol., 188, 1389-1395.
6. Newberry,K.J., Fuangthong,M., Panmanee,W., Mongkolsuk,S. and Brennan,R.G. (2007) Structural mechanism of organic hydroperoxide induction of the transcription regulator OhrR. Mol. Cell, 28 652-664.
7. Chen,H., Hu,J., Chen,P.R., Lan,L., Li,Z., Hicks,L.M., Dinner,A.R. and He,C. (2008) The Pseudomonas aeruginosa multidrug e.ux regulator MexR uses an oxidation-sensing mechanism. Proc. Natl Acad. Sci. USA 105, 13586-13591.
8. Chen,P.R., Bae,T., Williams,W.A., Duguid,E.M., Rice,P.A., Schneewind,O. and He,C. (2006) An oxidation-sensing mechanism is used by the global regulator MgrA in Staphylococcus aureus. Nat. Chem. Biol., 2 591-595.
9. Wilke,M.S., Heller,M., Creagh,A.L., Haynes,C.A., McIntosh,L.P., Poole,K. and Strynadka,N.C. (2008) The crystal structure of MexR from Pseudomonas aeruginosa in complex with its antirepressor ArmR. Proc. Natl Acad. Sci. USA, 105, 14832-14837.
10. Alekshun,M.N., Levy,S.B., Mealy,T.R., Seaton,B.A. and Head,J.F. (2001) The crystal structure of MarR, a regulator of multiple antibiotic resistance, at 2.3Å resolution. Nat. Struct. Biol., 8, 710-714.
11. Saridakis,V., Shahinas,D., Xu,X. and Christendat,D. (2008) Structural insight on the mechanism of regulation of the MarR family of proteins: high-resolution crystal structure of a transcriptional repressor from Methanobacterium thermoautotrophicum. J. Mol. Biol., 377, 655-667.
12. Wilkinson,S.P. and Grove,A. (2006) Ligand-responsive transcriptional regulation by members of the MarR family of winged helix proteins. Curr. Issues Mol. Biol., 8, 51-62.
13. Lee,J.W., Soonsanga,S. and Helmann,J.D. (2007) A complex thiolate switch regulates the Bacillus subtilis organic peroxide sensor OhrR. Proc. Natl Acad. Sci. USA, 104, 8743-8748.
14. Soonsanga,S., Lee,J.W. and Helmann,J.D. (2008) Oxidant-dependent switching between reversible and sacrificial oxidation pathways for Bacillus subtilis OhrR. Mol. Microbiol., 68, 978-986.
15. Soonsanga,S., Lee,J.W. and Helmann,J.D. (2008) Conversion of Bacillus subtilis OhrR from a 1-Cys to a 2-Cys peroxide sensor. J. Bacteriol., 190, 5738-5745.
16. Soonsanga,S., Fuangthong,M. and Helmann,J.D. (2007) Mutational analysis of active site residues essential for sensing of organic hydroperoxides by Bacillus subtilis OhrR. J. Bacteriol., 189, 7069-7076.
17. Guerout-Fleury,A.M., Frandsen,N. and Stragier,P. (1996) Plasmids for ectopic integration in Bacillus subtilis. Gene, 180, 57-61.
18. Lee,S., Arunkumar,A.I., Chen,X. and Giedroc,D.P. (2006) Structural insights into homo- and heterotropic allosteric coupling in the zinc sensor S. aureus CzrA from covalently fused dimers. J. Am. Chem. Soc., 128, 1937-1947.
19. Fuangthong,M. and Helmann,J.D. (2002) The OhrR repressor senses organic hydroperoxides by reversible formation of a cysteine-sulfenic acid derivative. Proc. Natl Acad. Sci. USA, 99, 6690-6695.
20. Miller,J.H. (1972) Experiments in Molecular Genetics, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, pp. 352-355.
21. Aravind,L., Anantharaman,V., Balaji,S., Babu,M.M. and Iyer,L.M. (2005) The many faces of the helix-turn-helix domain: Transcription regulation and beyond. FEMS Microbiol. Rev., 29, 231-262.
22. von Hippel,P.H. and Berg,O.G. (1986) On the specificity of DNA-protein interactions. Proc. Natl Acad. Sci. USA, 83, 1608-1612.
23. Shanblatt,S.H. and Revzin,A. (1983) Two catabolite activator protein molecules bind to the galactose promoter region of Escherichia coli in the presence of RNA polymerase. Proc. Natl Acad. Sci. USA, 80, 1594-1598.
24. Heyduk,T. and Lee,J.C. (1989) Escherichia coli cAMP receptor protein: Evidence for three protein conformational states with di fferent promoter binding affinities. Biochemistry, 28, 6914-6924.
25. Shewchuk,L.M., Verdine,G.L. and Walsh,C.T. (1989) Transcriptional switching by the metalloregulatory MerR protein: Initial characterization of DNA and mercury (II) binding activities. Biochemistry, 28, 2331-2339.
26. Liu,T., Golden,J.W. and Giedroc,D.P. (2005) A zinc(II)/lead(II)/ cadmium(II)-inducible operon from the Cyanobacterium anabaena is regulated by AztR, an alpha3N ArsR/SmtB metalloregulator. Biochemistry, 44, 8673-8683.
27. Cavet,J.S., Graham,A.I., Meng,W. and Robinson,N.J. (2003) A cadmium-lead-sensing ArsR-SmtB repressor with novel sensory sites. Complementary metal discrimination by NmtR AND CmtR in a common cytosol. J. Biol. Chem., 278, 44560-44566.
28. Kamionka,A., Majewski,M., Roth,K., Bertram,R., Kraft,C. and Hillen,W. (2006) Induction of single chain tetracycline repressor requires the binding of two inducers. Nucleic Acids Res., 34, 3834-3841.
29. Sun,Y., Wong,M.D. and Rosen,B.P. (2002) Both metal binding sites in the homodimer are required for metalloregulation by the CadC repressor. Mol. Microbiol., 44, 1323-1329.
30. Eicken,C., Pennella,M.A., Chen,X., Koshlap,K.M., VanZile,M.L., Sacchettini,J.C. and Giedroc,D.P. (2003) A metal-ligand-mediated intersubunit allosteric switch in related SmtB/ArsR zinc sensor proteins. J. Mol. Biol., 333, 683-695.
31. Schumacher,M.A., Miller,M.C., Grkovic,S., Brown,M.H., Skurray,R.A. and Brennan,R.G. (2001) Structural mechanisms of QacR induction and multidrug recognition. Science, 294, 2158-2163.