Characterization of OxyR as a negative transcriptional regulator that represses catalase production in corynebacterium diphtheriae

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Kim, Ju Sim ^a   Holmes, Randall K ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; HYDROGEN PEROXIDE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR OXYR; UNCLASSIFIED DRUG; BACTERIAL DNA; BACTERIAL PROTEIN; ESCHERICHIA COLI PROTEIN; OXYR PROTEIN, E COLI; RECOMBINANT PROTEIN; REPRESSOR PROTEIN;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERICIDAL ACTIVITY; BACTERIUM MUTANT; CAT GENE; CONTROLLED STUDY; CORYNEBACTERIUM DIPHTHERIAE; CORYNEBACTERIUM GLUTAMICUM; ENZYME ACTIVITY; ENZYME REPRESSION; ENZYME SYNTHESIS; ESCHERICHIA COLI; GENE DELETION; GENE FUNCTION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; GROWTH INHIBITION; NONHUMAN; NUCLEIC ACID STRUCTURE; OPEN READING FRAME; OXIDATIVE STRESS; PROMOTER REGION; PROTEIN BINDING; PROTEIN PURIFICATION; QUORUM SENSING; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; WILD TYPE; BIOSYNTHESIS; DRUG EFFECT; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; SPECIES DIFFERENCE;

CORYNEBACTERIUM DIPHTHERIAE; CORYNEBACTERIUM GLUTAMICUM; ESCHERICHIA COLI;

BACTERIAL PROTEINS; BASE SEQUENCE; CATALASE; CORYNEBACTERIUM DIPHTHERIAE; CORYNEBACTERIUM GLUTAMICUM; DNA, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENES, BACTERIAL; GENETIC COMPLEMENTATION TEST; HYDROGEN PEROXIDE; MUTATION; OXIDATIVE STRESS; PROMOTER REGIONS, GENETIC; RECOMBINANT PROTEINS; REPRESSOR PROTEINS; SPECIES SPECIFICITY;

EID: 84863338633     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031709     Document Type: Article

References (50)

1. Cannio R, Fiorentino G, Morana A, Rossi M, Bartolucci S, (2000) Oxygen: friend or foe? Archaeal superoxide dismutases in the protection of intra- and extracellular oxidative stress. Front Biosci 5: D768-779.
2. Storz G, Tartaglia LA, Farr SB, Ames BN, (1990) Bacterial defenses against oxidative stress. Trends Genet 6: 363-368.
3. González-Flecha B, Demple B, (1997) Homeostatic regulation of intracellular hydrogen peroxide concentration in aerobically growing Escherichia coli. J Bacteriol 179: 382-388.
4. Schellhorn HE, (1995) Regulation of hydroperoxidase (catalase) expression in Escherichia coli. FEMS Microbiol Lett 131: 113-119.
5. Hidalgo E, Demple B, (1994) An iron-sulfur center essential for transcriptional activation by the redox-sensing SoxR protein. EMBO J 13: 138-146.
6. Hidalgo E, Bollinger JM, Bradley TM, Walsh CT, Demple B, (1995) Binuclear [2Fe-2S] clusters in the Escherichia coli SoxR protein and role of the metal centers in transcription. J Biol Chem 270: 20908-20914.
7. Storz G, Imlay JA, (1999) Oxidative stress. Curr Opin Microbiol 2: 188-194.
8. Greenberg JT, Monach P, Chou JH, Josephy PD, Demple B, (1990) Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli. Proc Natl Acad Sci U S A 87: 6181-6185.
9. Schell MA, (1993) Molecular biology of the LysR family of transcriptional regulators. Annu Rev Microbiol 47: 597-626.
10. Zheng M, Aslund F, Storz G, (1998) Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279: 1718-1721.
11. Zheng M, Wang X, Templeton LJ, Smulski DR, LaRossa RA, et al. (2001) DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183: 4562-4570.
12. Christman MF, Morgan RW, Jacobson FS, Ames BN, (1985) Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell 41: 753-762.
13. González-Flecha B, Demple B, (1999) Role for the oxyS gene in regulation of intracellular hydrogen peroxide in Escherichia coli. J Bacteriol 181: 3833-3836.
14. Tseng HJ, McEwan AG, Apicella MA, Jennings MP, (2003) OxyR acts as a repressor of catalase expression in Neisseria gonorrhoeae. Infect Immun 71: 550-556.
15. Seib KL, Wu HJ, Srikhanta YN, Edwards JL, Falsetta ML, et al. (2007) Characterization of the OxyR regulon of Neisseria gonorrhoeae. Mol Microbiol 63: 54-68.
16. Ieva R, Roncarati D, Metruccio MME, Seib KL, Scarlato V, et al. (2008) OxyR tightly regulates catalase expression in Neisseria meningitidis through both repression and activation mechanisms. Mol Microbiol 70: 1152-1165.
17. Holmes RK, (2000) Biology and molecular epidemiology of diphtheria toxin and the tox gene. J Infect Dis 181 (Suppl 1): S156-167.
18. Kunkle CA, Schmitt MP, (2003) Analysis of the Corynebacterium diphtheriae DtxR regulon: Identification of a putative siderophore synthesis and transport system that is similar to the Yersinia high-pathogenicity island-encoded yersiniabactin synthesis and uptake system. J Bacteriol 185: 6826-6840.
19. Lee JH, Wang T, Ault K, Liu J, Schmitt MP, et al. (1997) Identification and characterization of three new promoter/operators from Corynebacterium diphtheriae that are regulated by the diphtheria toxin repressor (DtxR) and iron. Infect Immun 65: 4273-4280.
20. Schmitt MP, Holmes RK, (1991) Iron-dependent regulation of diphtheria toxin and siderophore expression by the cloned Corynebacterium diphtheriae repressor gene DtxR in C. diphtheriae C7 Strains. Infect Immun 59: 1899-1904.
21. Oram DM, Jacobson AD, Holmes RK, (2006) Transcription of the contiguous sigB, dtxR, and galE genes in Corynebacterium diphtheriae: Evidence for multiple transcripts and regulation by environmental factors. J Bacteriol 188: 2959-2973.
22. Merkamm M, Guyonvarch A, (2001) Cloning of the sodA gene from Corynebacterium melassecola and role of superoxide dismutase in cellular viability. J Bacteriol 183: 1284-1295.
23. EI Shafey HM, Ghanem S, Merkamm M, Guyonvarch A, (2008) Corynebacterium glutamicum superoxide dismutase is a manganese-strict non-cambialistic enzyme in vitro. Microbiol Res 163: 80-86.
24. Barksdale WL, Pappenheimer AM, (1954) Phage-host relationships in nontoxigenic and toxigenic diphtheria bacilli. J Bacteriol 67: 220-232.
25. Tai SP, Krafft AE, Nootheti P, Holmes RK, (1990) Coordinate regulation of siderophore and diphtheria toxin production by iron in Corynebacterium diphtheriae. Microb Pathog 9: 267-273.
26. Sambrook J, Russell DW, (2001) Molecular Cloning: A Laboratory Manual, 3rd Ed Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
27. Schafer A, Kalinowski J, Puhler A, (1994) Increased fertility of Corynebacterium glutamicum recipients in intergeneric matings with Escherichia coli after stress exposure. Appl Environ Microbiol 60: 756-759.
28. Simon R, Priefer U, Puhler A, (1983) A broad host mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Bio/Technology 1: 37-45.
29. Ton-That H, Schneewind O, (2003) Assembly of pili on the surface of Corynebacterium diphtheriae. Mol Microbiol 50: 1429-1438.
30. Oram DM, Oram M, Woolston JE, Jacobson AD, Holmes RK, (2007) Bacteriophage-based vectors for site-specific insertion of DNA in the chromosome of Corynebacteria. Gene 391: 53-62.
31. Oram DM, Avdalovic A, Holmes RK, (2002) Construction and characterization of transposon insertion mutations in Corynebactetium diphtheriae that affect expression of the diphtheria toxin repressor (DtxR). J Bacteriol 184: 5723-5732.
32. Prentki P, Krisch HM, (1984) In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29: 303-313.
33. Tai TN, Havelka WA, Kaplan S, (1988) A broad-host-range vector system for cloning and translational lacZ fusion analysis. Plasmid 19: 175-188.
34. Nelson DP, Kiesow LA, (1972) Enthalpy of decomposition of hydrogen-peroxide by catalase at 25 degrees C (with molar extinction coefficients of H2O2 solutions in UV). Anal Biochem 49: 474-478.
35. Wayne LG, Diaz GA, (1986) A double staining method for differentiating between two classes of mycobacterial catalase in polyacrylamide electrophoresis gels. Anal Biochem 157: 89-92.
36. Kim JS, Jang JH, Lee JW, Kang SO, Kim KS, et al. (2000) Identification of cis site involved in nickel-responsive transcriptional repression of sodF gene coding for Fe- and Zn-containing superoxide dismutase of Streptomyces griseus. Biochim Biophys Acta 1493: 200-207.
37. Zeller T, Mraheil MA, Moskvin OV, Li KY, Gomelsky M, et al. (2007) Regulation of hydrogen peroxide-dependent gene expression in Rhodobacter sphaeroides: regulatory functions of OxyR. J Bacteriol 189: 3784-3792.
38. Pomposiello PJ, Demple B, (2001) Redox-operated genetic switches: the SoxR and OxyR transcription factors. Trends Biotechnol 19: 109-114.
39. Cerdeňo-Tarraga AM, Efstratiou A, Dover LG, Holden MT, Pallen M, et al. (2003) The complete genome sequence and analysis of Corynebacterium diphtheriae NCTC13129. Nucleic Acids Res 31: 6516-6523.
40. Tartaglia LA, Storz G, Ames BN, (1989) Identification and molecular analysis of oxyR regulated promoters important for the bacterial adaptation to oxidative stress. J Mol Biol 210: 709-719.
41. Lee JH, Yeo WS, Roe JH, (2004) Induction of the sufA operon encoding Fe-S assembly proteins by superoxide generators and hydrogen peroxide: involvement of OxyR, IHF and an unidentified oxidant-responsive factor. Mol Microbiol 51: 1745-1755.
42. Keen NT, Tamaki S, Kobayashi D, Trollinger D, (1988) Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria. Gene 70: 191-197.
43. Kalinowski J, Bathe B, Bartels D, Bischoff N, Bott M, et al. (2007) The complete Corynebacterium glutamicum ATCC 13032 genome sequence and its impact on the production of L-aspartate-derived amino acids and vitamins. J Biotechnol 104: 5-25.
44. Sak BD, Eisenstark A, Touati D, (1989) Exonuclease III and the catalase hydroperoxidase II in Escherichia coli are both regulated by the katF gene product. Proc Natl Acad Sci U S A 86: 3271-3275.
45. Pátek M, Nešvera J, (2011) Sigma factors and promoters in Corynebacterium glutamicum. J Biotechnol 154: 101-113.
46. Parsek MR, Ye RW, Pun P, Chakrabarty AM, (1994) Critical nucleotides in the interaction of a LysR-type regulator with its target promoter region. J Biol Chem 269: 11279-11284.
47. Goethals K, Van Montagu M, Holsters M, (1992) Conserved motifs in a divergent nod box of Azorhizobium caulinodans ORS571 reveal a common structure in promoters regulated by LysR-type proteins. Proc Natl Acad Sci U S A 89: 1646-1650.
48. Zaim J, Kierzek AM, (2003) The structure of full-length LysR-type transcriptional regulators. Modeling of the full-length OxyR transcription factor dimer. Nucleic Acids Res 31: 1444-1454.
49. Sainsbury S, Lane LA, Ren J, Gilbert RJ, Saunders NJ, et al. (2009) The structure of CrgA from Neisseria meningitidis reveals a new octameric assembly state for LysR transcriptional regulators. Nucleic Acids Res 37: 4545-4558.
50. Hanahan D, (1983) Studies on tansformation of Escherichia coli with plasmids. J Mol Biol 166: 557-580.