Peroxiredoxins in Bacterial Antioxidant Defense

  • James M. Dubbs
  • Skorn Mongkolsuk
Part of the Subcellular Biochemistry book series (SCBI, volume 44)


Peroxiredoxins constitute an important component of the bacterial defense against toxic peroxides. These enzymes use reactive cysteine thiols to reduce peroxides with electrons ultimately derived from reduced pyridine dinucleotides. Studies examining the regulation and physiological roles of AhpC, Tpx, Ohr and OsmC reveal the multi-layered nature of bacterial peroxide defense. AhpC is localized in the cytoplasm and has a wide substrate range that includesH2O2, organic peroxides and peroxynitrite. This enzyme functions in both the control of endogenous peroxides, as well as in the inducible defense response to exogenous peroxides or general stresses. Ohr, OsmC and Tpx are organic peroxide specific. Tpx is localized to the periplasm and can be involved in either constitutive peroxide defense or participate in oxidative stress inducible responses depending on the organism. Ohr is an organic peroxide specific defense system that is under the control of the organic peroxide sensing repressor OhrR. In some organisms Ohr homologs are regulated in response to general stress. Clear evidence indicates that AhpC, Tpx and Ohr are involved in virulence. The role of OsmC is less clear. Regulation of OsmC expression is not oxidative stress inducible, but is controlled by multiple general stress responsive regulators

Peroxiredoxin Oxidative stress Gene regulation Ohr OsmC AhpC Tpx OhrR OxyR PerR HypR Organic peroxide Hydrogen peroxide Peroxynitrite Bacteria Virulence 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ades, S.E., 2004, Control of the alternative sigma factor sigmaE in Escherichia coli. Curr. Opin. Microbiol. 7: 157–162.PubMedCrossRefGoogle Scholar
  2. Antelmann, H., Engelmann, S., Schmid, R., and Hecker, M., 1996, General and oxidative stress responses in Bacillus subtilis: cloning, expression, and mutation of the alkyl hydroperoxide reductase operon. J. Bacteriol. 178: 6571–6578.PubMedGoogle Scholar
  3. Armstrong-Buisseret, L., Cole, M.B., and Stewart, G.S., 1995, A homologue to the Escherichia coli alkyl hydroperoxide reductase AhpC is induced by osmotic upshock in Staphylococcus aureus. Microbiol. 141: 1655–1661.Google Scholar
  4. Arnold, C.N., McElhanon, J., Lee, A., Leonhart, R., and Siegele, D.A., 2001, Global analysis of Escherichia coli gene expression during the acetate-induced acid tolerance response. J. Bacteriol. 183: 2178–2186.PubMedCrossRefGoogle Scholar
  5. Atichartpongkul, S., Loprasert, S., Vattanaviboon, P., Whangsuk, W., Helmann John, D., and Mongkolsuk, S., 2001, Bacterial Ohr and OsmC paralogues define two protein families with distinct functions and patterns of expression. Microbiol. 147: 1775–1782.Google Scholar
  6. Baillon, M.-L.A., van Vliet, A.H.M., Ketley, J.M., Constantinidou, C., and Penn, C.W., 1999, An iron-regulated alkyl hydroperoxide reductase (AhpC) confers aerotolerance and oxidative stress resistance to the microaerophilic pathogen Campylobacter jejuni. J. Bacteriol. 181: 4798–4804.Google Scholar
  7. Baker, L.M., and Poole, L.B., 2003, Catalytic mechanism of thiol peroxidase from Escherichia coli. Sulfenic acid formation and overoxidation of essential CYS61. J. Biol. Chem. 278: 9203–9211.PubMedCrossRefGoogle Scholar
  8. Baker, L.M., Raudonikiene, A., Hoffman, P.S., and Poole, L.B., 2001, Essential thioredoxin-dependent peroxiredoxin system from Helicobacter pylori: genetic and kinetic characterization. J. Bacteriol. 183: 1961–1973.PubMedCrossRefGoogle Scholar
  9. Banjerdkij, P., Vattanaviboon, P., and Mongkolsuk, S., 2005, Exposure to cadmium elevates expression of genes in the OxyR and OhrR regulons and induces cross-resistance to peroxide killing treatments in Xanthomonas campestris. Appl. Environ. Microbiol. 7: 1843–1849.CrossRefGoogle Scholar
  10. Bernhardt, J., Volker, U., Volker, A., Antelmann, H., Schmid, R., Mach, H., and Hecker, M., 1997, Specific and general stress proteins in Bacillus subtilis - a two-dimensional protein electrophoresis study. Microbiol. 143: 999–1017.CrossRefGoogle Scholar
  11. Blankenhorn, D., Phillips, J., and Slonczewski, J.L., 1999, Acid- and base-induced proteins during aerobic and anaerobic growth of Escherichia coli revealed by two-dimensional gel electrophoresis. J. Bacteriol. 181: 2209–2216.PubMedGoogle Scholar
  12. Bouvier, J., Gordia, S., Kampmann, G., Lange, R., Hengge-Aronis, R., and Gutierrez, C., 1998, Interplay between global regulators of Escherichia coli: effect of RpoS, Lrp and H-NS on transcription of the gene osmC. Mo.l Microbiol. 28: 971–980.CrossRefGoogle Scholar
  13. Brenot, A., King, K.Y., and Caparon, M.G., 2005, The PerR regulon in peroxide resistance and virulence of Streptococcus pyogenes. Mol. Microbiol. 55: 221–234.PubMedCrossRefGoogle Scholar
  14. Brune, I., Brinkrolf, K., Kalinowski, J., Puhler, A., and Tauch, A., 2005, The individual and common repertoire of DNA-binding transcriptional regulators of Corynebacterium glutamicum, Corynebacterium efficiens, Corynebacterium diphtheriae and Corynebacterium jeikeium deduced from the complete genome sequences. BMC Genomics 6: 86.PubMedCrossRefGoogle Scholar
  15. Bryk, R., Griffin, P., and Nathan, C., 2000, Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407: 211–215.PubMedCrossRefGoogle Scholar
  16. Bryk, R., Lima, C.D., Erdjument-Bromage, H., Tempst, P., and Nathan, C., 2002, Metabolic enzymes of mycobacteria linked to antioxidant defense by a thioredoxin-like protein. Science 295: 1073–1077.PubMedCrossRefGoogle Scholar
  17. Bsat, N., Chen, L., and Helmann, J.D., 1996, Mutation of the Bacillus subtilis alkyl hydroperoxide reductase (ahpCF) operon reveals compensatory interactions among hydrogen peroxide stress genes. J. Bacteriol. 178: 6579–6586.PubMedGoogle Scholar
  18. Bsat, N., Herbig, A.F., Cassillas-Martinez, L., Setlow, P., and Helmann, J.D., 1998, Bacillus subtilis contains multiple Fur homologues: identification of the iron uptake (Fur) and peroxide regulon (PerR) repressors. Mol. Microbiol. 29: 189–198.PubMedCrossRefGoogle Scholar
  19. Cha, M.-K., Kim, H.-K., and Kim, I.-H., 1995, Thioredoxin-linked ‘‘thiol peroxidase’’ from periplasmic space of Escherichia coli. J. Biol. Chem. 270: 28635–28641.PubMedCrossRefGoogle Scholar
  20. Cha, M.-K., Kim, H.-K., and Kim, I.-H., 1996, Mutation and Mutagenesis of thiol peroxidase of Escherichia coli and a new type of thiol peroxidase family. J. Bacteriol. 178: 5610–5614.PubMedGoogle Scholar
  21. Cha, M.-K., Kim, W.-C., Lim, C.-J., Kim, K., and Kim, I.-H., 2004, Escherichia coli periplasmic thiol peroxidase acts as lipid hydroperoxide peroxidase and the principal antioxidative function during anaerobic growth. J. Biol. Chem. 279: 8769–8778.PubMedCrossRefGoogle Scholar
  22. Chae, H.Z., Robison, K., Poole, L.B., Church, G., Storz, G., and Rhee, S.G., 1994, Cloning and sequencing of thiol-specific antioxidant from mammalian brain: alkyl hydroperoxide reductase and thiol-specific antioxidant define a large family of antioxidant enzymes. Pro.c Nat.l Acad. Sci. USA 91: 7017–7021.CrossRefGoogle Scholar
  23. Charoenlap, N., Eiamphungporn, W., Nopmanee, C., Utamapongchai, S., Vattanaviboon, P., and Mongkolsuk, S., 2005, OxyR mediated compensatory expression between ahpC and katA and the significance of ahpC in protection from hydrogen peroxide in Xanthomonas campestris. FEMS Microbiol. Let.t 249: 73–78.CrossRefGoogle Scholar
  24. Chen, L., Keramati, L., and Helmann, J.D., 1995, Coordinate regulation of Bacillus subtilis peroxide stress genes by hydrogen peroxide and metal ions. Proc. Natl. Acad. Sci. USA 92: 8190–8194.PubMedCrossRefGoogle Scholar
  25. Chen, L., Xie, Q.-W., and Nathan, C., 1998, Alkyl hydroperoxide reductase subunit C (AhpC) protects bacterial and human cells against reactive nitrogen intermediates. Mol. Cell. 1: 795–805.PubMedCrossRefGoogle Scholar
  26. Choi, J., Choi, S., Choi, J., Cha, M.-K., Kim, I.-H., and Shin, W., 2003, Crystal structure of Escherichia coli thiol peroxidase in the oxidized state: insights into intramolecular disulfide formation and substrate binding in atypical 2-Cys peroxiredoxins. J. Biol. Chem. 278: 49478–49486.PubMedCrossRefGoogle Scholar
  27. Christman, M.F., Morgan, R.W., Jacobson, F.S., and Ames, B.M., 1985, Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell 41: 753–762.PubMedCrossRefGoogle Scholar
  28. Chuang, M.-H., Wu, M.-S., Lo, W.-L., Jaw-Town, L., Wong, C.-H., and Chiou, S.-H., 2006, The antioxidant protein alkylhydroperoxide reductase of Helicobacter pylori switches from a peroxide reductase to a molecular chaperone function. Proc. Natl. Acad. Sci. USA 103: 2552–2557.PubMedCrossRefGoogle Scholar
  29. Chuchue, T., Tanboon, W., Prapagdee, B., Dubbs, J.M., Vattanaviboon, P., and Mongkolsuk, S., 2006, ohrR and ohr are the primary sensor/regulator and protective genes against organic hydroperoxide stress in Agrobacterium tumefaciens. J. Bacteriol. 188: 842–851.PubMedCrossRefGoogle Scholar
  30. Comtois, S.L., Gidley, M.D., and Kelly, D.J., 2003, Role of the thioredoxin system and the thiol-peroxidases Tpx and Bcp in mediating resistance to oxidative and nitrosative stress in Helicobacter pylori. Microbiol. 149: 121–129.CrossRefGoogle Scholar
  31. Conter, A., Gagneaux, C., Magali, S., and Gutierrez, C., 2001, Survival of Escherichia coli during long-term starvation: effects of aeration, NaCl, and the rpoS and osmC gene products. Res. Microbiol. 152: 17–26.PubMedCrossRefGoogle Scholar
  32. Conter, A., Sturny, R., Gutierrez, C., and Cam, K., 2002, The RcsCB His-Asp phosphorelay system is essential to overcome chlorpromazine-induced stress in Escherichia coli. J. Bacterio.l 10: 2850–2853.CrossRefGoogle Scholar
  33. Cussiol, J.R.R., Alves, S.V., de Oliviera, M.A., and Netto, L.E.S., 2003, Organic hydroperoxide resistance gene encodes a thiol-dependent peroxidase. J. Biol. Chem. 278: 11570–11578.PubMedCrossRefGoogle Scholar
  34. Davalos-Garcia, M., Conter, A., Toesca, I., Gutierrez, C., and Cam, K., 2001, Regulation of osmC gene expression by the two-component system rcsB-rcsC in Escherichia coli. J. Bacteriol. 183: 5870–5876.PubMedCrossRefGoogle Scholar
  35. de Oliveira, M.A., Netto, L.E.S., Medrano, F.J., Barbosa, G., Alves, S.V., Cussiol, J.R.R., and Guimares, B.G., 2004, Crystallization and preliminary X-ray diffraction analysis of an oxidized state of Ohr from Xylella fastidiosa. Acta Crystallogr. D Biol. Crystallogr. 60: 337–339.CrossRefGoogle Scholar
  36. Deretic, V., Philipp, W., Dhandayuthapani, S., Mudd, M.H., Curcic, R., Garbe, T.R., Heym, B., Via, L.E., and Cole, S.T., 1995, Mycobacterium tuberculosis is a natural mutant with an inactivated oxidative-stress regulatory gene: implications for sensitivity to isoniazid. Mol. Microbiol. 17: 889–900.PubMedCrossRefGoogle Scholar
  37. Dhandayuthapani, S., Mudd, M.H., and Deretic, V., 1997, Interactions of OxyR with the promoter region of the oxyR and ahpC genes from Mycobacterium leprae and Mycobacterium tuberculosis. J. Bacteriol. 179: 2401–2409.PubMedGoogle Scholar
  38. Dhandayuthapani, S., Zhang, Y., Mudd, M.H., and Deretic, V., 1996, Oxidative stress response and its role in sensitivity to isoniazid in mycobacteria: characterization and inducibility of ahpC by peroxides in Mycobacterium smegmatis and lack of expression in M. aurum and M. tuberculosis. J. Bacteriol. 178: 3641–3649.PubMedGoogle Scholar
  39. Diaz, P.I., V, W., Corthals, G.L., and Rogers, A.H., 2004, Studies on NADH oxidase and alkyl hydroperoxide reductase produced by Porphyromonas gingivalis. Oral Microbiol. Immunol. 19: 137–143.PubMedCrossRefGoogle Scholar
  40. Dintilhac, A., and Claverys, J.P., 1997, The adc locus, which affects competence for genetic transformation in Streptococcus pneumoniae, encodes an ABC transporter with a putative lipoprotein homologous to a family of streptococcal adhesins. Res. Microbiol. 148: 119–131.PubMedCrossRefGoogle Scholar
  41. Dolin, M.I., 1961, Cytochrome-independent electron transport enzymes of bacteria, in The bacteria Vol. 2 (Gunsalus, I.C. and Stanier, R.Y., eds), Academic Press Inc., New York, N.Y., USA, pp. 425–460.Google Scholar
  42. Domenech, P., Honore, N., Heym, B., and Cole, S.T., 2001, Role of OxyS of Mycobacterium tuberculosis in oxidative stress: overexpression confers increased sensitivity to organic hydroperoxides. Microbes. Infect. 3: 713–721.PubMedCrossRefGoogle Scholar
  43. Dorman, C.J., 2004, H-NS: a universal regulator for a dynamic genome. Nat Rev Microbiol 2: 391–400.PubMedCrossRefGoogle Scholar
  44. Dorsey, C.W., Tomaras, A.P., and Actis, L.A., 2006, Sequence and organization of pMAC, an Acinetobacter baumannii plasmid harboring genes involved in organic peroxide resistance. Plasmid 56: 112–123.PubMedCrossRefGoogle Scholar
  45. Dosanjh, N.S., Rawat, M., Chung, J.-H., and Av-Gay, Y., 2005, Thiol specific oxidative stress response in Mycobacteria. FEMS Microbiol. Lett. 249: 87–94.PubMedCrossRefGoogle Scholar
  46. Ellis, H.R., and Poole, L.B., 1997, Roles for the two cysteine residues of AhpC in catalysis of peroxide reduction by alkyl hydroperoxide reductase from Salmonella typhimurium. Biochemistry 36: 13349–13356.PubMedCrossRefGoogle Scholar
  47. Elsaghier, A., Nolan, A., Allen, B., and Ivanyi, J., 1992, Distinctive western blot antibody patterns induced by infection of mice with individual strains of the Mycobacterium avium complex. Immunol. 76: 355–361.Google Scholar
  48. Ernst, F.D., Bereswill, S., Waidner, B., Stoof, J., Mader, U., Kusters, J.G., Kuipers, E.J., Kist, M., van Vliet, A.H.M., and Homuth, G., 2005a, Transcriptional profiling of Helicobacter pylori Fur- and iron-regulated gene expression. Microbiol. 151: 533–546.CrossRefGoogle Scholar
  49. Ernst, F.D., Homuth, G., Stoof, J., Mader, U., Waidner, B., Kuipers, E.J., Kist, M., Kusters, J.G., Bereswill, S., and van Vliet, A.H.M., 2005b, Iron-responsive regulation of the Helicobacter pylori iron-cofactored superoxide dismutase SodB is mediated by Fur. J. Bacteriol. 187: 3687–3692.CrossRefGoogle Scholar
  50. Francis, K.P., and Gallagher, M.P., 1993, Light emission from a Mudlux transcriptional fusion in Salmonella typhimurium is stimulated by hydrogen peroxide and by interaction with the mouse macrophage cell line J774.2. Infect. Immun. 61: 640–649.PubMedGoogle Scholar
  51. Francis, K.P., Taylor, P.D., Inchley, C.J., and Gallagher, M.P., 1997, Identification of the ahp operon of Salmonella typhimurium as a macrophage-induced locus. J. Bacteriol. 179: 4046–4048.PubMedGoogle Scholar
  52. Fuangthong, M., Atichartpongkun, S., Mongkolsuk, S., and Helmann, D., 2001, OhrR is a repressor of ohrA, a key organic hydroperoxide resistance determinant in Bacillus subtilis. J. Bacteriol.. 183: 4134–4141.PubMedCrossRefGoogle Scholar
  53. Fuangthong, M., and Helmann, J.D., 2003, Recognition of DNA by three ferric uptake regulator (Fur) homologs in Bacillus subtilis. J. Bacteriol. 185: 6348–6357.PubMedCrossRefGoogle Scholar
  54. Fuangthong, M., and Helmann, D., 2002a, The OhrR repressor senses organic hydroperoxides by reversible formation of a cysteine-sulfenic acid derivative. Proc. Natl. Acad. Sci. USA 99: 6690–6695.CrossRefGoogle Scholar
  55. Fuangthong, M., Herbig, A.F., Bsat, N., and Helmann, D., 2002b, Regulation of the Bacillus subtilis fur and perR genes by PerR: not all members of the PerR regulon are peroxide inducible. J. Bacterio.l 184: 3276–3286.CrossRefGoogle Scholar
  56. Fukumori, F., and Kishii, M., 2001, Molecular cloning and transcriptional analysis of the alkyl hydroperoxide reductase genes from Pseudomonas putida KT2442. J. Gen. Appl. Microbiol. 47: 269–277.PubMedCrossRefGoogle Scholar
  57. Gancz, H., Censini, S., and Merrell, D.S., 2006, Iron and pH homeostasis intersect at the level of Fur regulation in the gastric pathogen Helicobacter pylori. Infect. Immun. 74: 602–614.PubMedCrossRefGoogle Scholar
  58. Ganeshkumar, N., Hannam, P.M., Kolenbrander, P.E., and McBride, B.C., 1991, Nucleotide sequence of a gene coding for a saliva-binding protein (SsaB) from Streptococcus sanguis 12 and possible role of the protein in coaggregation with actinomyces. Infect. Immun. 59: 1093–1099.PubMedGoogle Scholar
  59. Garbe, T.R., Kobayashi, M., and Yukawa, H., 2000, Indole-inducible proteins in bacteria suggest membrane and oxidant toxicity. Arch. Microbiol. 173: 78–82.PubMedCrossRefGoogle Scholar
  60. Gordia, S., and Gutierrez, C., 1996, Growth-phase-dependent expression of the osmotically inducible gene osmC of Escherichia coli K-12. Mol. Microbiol. 19: 729–736.PubMedCrossRefGoogle Scholar
  61. Greenberg, J.T., and Demple, B., 1988, Overproduction of peroxide-scavenging enzymes in Escherichia coli suppresses spontaneous mutagenesis and sensitivity to redox-cycling agents in oxyR-mutants. EMBO J. 7: 2611–2617.PubMedGoogle Scholar
  62. Gutierrez, C., Barondess, J., Manoil, C., and Beckwith, J., 1987, The use of transposon TnphoA to detect genes for cell envelope proteins subject to a common regulatory stimulus. Analysis of osmotically regulated genes in Escherichia coli. J. Mol. Biol. 195: 289–297.PubMedCrossRefGoogle Scholar
  63. Gutierrez, C., and Devedjian, J.C., 1991, Osmotic induction of gene osmC expression in Escherichia coli K12. J. Mol. Biol. 220: 959–973.PubMedCrossRefGoogle Scholar
  64. Hahn, J.-S., Oh, S.-Y., and Roe, J.-H., 2002, Role of OxyR as a peroxide-sensing positive regulator in Streptomyces coelicolor A3(2). J. Bacteriol. 184: 5214–5222.PubMedCrossRefGoogle Scholar
  65. Halliwell, B., and Gutteridge, J.M.C., 1984, Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem. J. 219: 1–14.PubMedGoogle Scholar
  66. Hausladen, A., Privalle, C.T., Keng, T., De Angelo, J., and Stamler, J.S., 1996, Nitrosative stress: activation of the transcription factor OxyR. Cell 86: 719–29.PubMedCrossRefGoogle Scholar
  67. Hecker, M., and Volker, A., 2001, General stress response of Bacillus subtilis and other bacteria. Adv. Microb. Physiol. 44: 35–91.PubMedCrossRefGoogle Scholar
  68. Helmann, J.D. (2002). OxyR: A molecular code for redox sensing. Sci STKE 157: PE46.Google Scholar
  69. Helmann, J.D., Wu, M., Fang, Winston, Gaballa, A., Kobel, P.A., Morshedi, M.M., Fawcett, P., and Paddon, C., 2003, The global transcriptional response of Bacillus subtilis to peroxide stress is coordinated by three transcription factors. J. Bacteriol. 185: 243–253.PubMedCrossRefGoogle Scholar
  70. Henikoff, S., Haughn, G.W., Calvo, J.M., and Wallace, J.C., 1988, A large family of bacterial activator proteins. Proc. Natl. Acad. Sci. USA 85: 6602–6606.PubMedCrossRefGoogle Scholar
  71. Herbig, A.F., and Helmann, J.D., 2001, Roles of metal ions and hydrogen peroxide in modulating the interaction of the Bacillus subtilis PerR peroxide regulon repressor with operator DNA. Mol. Microbiol. 41: 849–859.PubMedCrossRefGoogle Scholar
  72. Higuchi, M., Yamamoto, Y., and Kamio, Y., 2000, Molecular biology of oxygen tolerance in lactic acid bacteria: Functions of NADH oxidases and Dpr in oxidative stress. J. Biosci. Bioeng. 90: 484–493.PubMedGoogle Scholar
  73. Higuchi, M., Yamamoto, Y., Poole, L.B., Shimada, M., Satoh, Y., Takahashi, N., and Kamio, Y., 1999, Functions of two types of NADH oxidases in energy metabolism and oxidative stress of Streptococcus mutans. J. Bacteriol. 181: 5940–5947.PubMedGoogle Scholar
  74. Hillas, P.J., Soto del Alba, F., Oyarzabal, J., Wilks, A., and Ortiz de Montellano, P.R., 2000, The AhpC and AhpD antioxidant defense system of Mycobacterium tuberculosis. J. Biol. Chem. 275: 18801–18809.PubMedCrossRefGoogle Scholar
  75. Hoper, D., Bernhardt, J., and Hecker, M., 2006, Salt stress adaptation of Bacillus subtilis: a physiological proteomics approach. Proteomics 6: 1550–62.PubMedCrossRefGoogle Scholar
  76. Horsburgh, M.J., Clements, M.O., Crossley, H., Ingham, E., and Foster, S.J., 2001, PerR controls oxidative stress resistance and iron storage proteins and is required for virulence in Staphylococcus aureus. Infect. Immun. 69: 3744–3754.PubMedCrossRefGoogle Scholar
  77. Imlay, J.A., 2003, Pathways of oxidative damage. Annu. Rev. Microbiol. 57: 395–418.PubMedCrossRefGoogle Scholar
  78. Jacobson, F.S., Morgan, R.W., Christman, M.F., and Ames, B.M., 1989, An alkyl hydroperoxide reductase induced by oxidative stress in Salmonella typhimurium and Escherichia coli: genetic characterization and cloning of ahp. J. Bacteriol. 171: 2049–2055.PubMedGoogle Scholar
  79. Jaeger, T., Budde, H., Flohé, L., Menge, U., Singh, M., Trujillo, M., and Radi, R., 2004, Multiple thioredoxin-mediated routes to detoxify hydroperoxides in Mycobacterium tuberculosis. Arch. Biochem. Biophy.s 423: 182–191.CrossRefGoogle Scholar
  80. Jakubovics, N.S., Smith, A.W., and Jenkinson, H.F., 2002, Oxidative stress tolerance is manganese (Mn2+) regulated in Streptococcus gordonii. Microbiol. 148: 3255–3263.Google Scholar
  81. Johnson, N.A., Liu, Y., and Fletcher, H.M., 2004, Alkyl hydroperoxide peroxidase subunit C (ahpC) protects against organic peroxides but does not affect the virulence of Porphyromonas gingivalis W83. Oral Microbiol. Immunol. 19: 233–239.PubMedCrossRefGoogle Scholar
  82. Jungblut, P.R., Bumann, D., Haas, G., Zimny-Arndt, U., Holland, P., Lamer, S., Siejak, F., Aebischer, A., and Meyer, T.F., 2000, Comparative proteome analysis of Helicobacter pylori. Mol. Microbiol. 36: 710–725.PubMedCrossRefGoogle Scholar
  83. Karupiah, G., Hunt, N.H., King, N.J., and Chaudhri, G., 2000, NADPH oxidase, Nramp1 and nitric oxide synthase 2 in the host antimicrobial response. Rev. Immunogenet. 2: 387–415.PubMedGoogle Scholar
  84. Kim, S., Oog, Merchant, K., Nudelman, R., Beyer, W.F.J., Keng, T., DeAngelo, J., Hausladen, A., and Stamler, J.S., 2002, OxyR: a molecular code for redox-related signaling. Cell 109: 383–396.PubMedCrossRefGoogle Scholar
  85. King, K.Y., Horenstein, J.A., and Caparon, M.G., 2000, Aerotolerance and peroxide resistance in peroxidase and PerR mutants of Streptococcus pyogenes. J. Bacteriol. 182: 5290–5299.PubMedCrossRefGoogle Scholar
  86. Klomsiri, C., Panmanee, W., Dharmsthiti, S., Vattanaviboon, P., and Mongkolsuk, S., 2005, Novel roles of ohrR-ohr in Xanthomonas sensing, metabolism, and physiological adaptive response to lipid hydroperoxide. J. Bacteriol. 187: 3277–3281.PubMedCrossRefGoogle Scholar
  87. Kolenbrander, P.E., Andersen, R.N., Baker, R.A., and Jenkinson, H.F., 1998, The adhesion-associated sca operon in Streptococcus gordonii encodes an inducible high-affinity ABC transporter for Mn2+ uptake. J. Bacteriol. 180: 290–295.PubMedGoogle Scholar
  88. Krayl, M., Benndorf, D., Loffhagen, N., and Babel, W., 2003, Use of proteomics and physiological characteristics to elucidate ecotoxic effects of methyl tert-butyl ether in Pseudomonas putida KT2440. Proteomics 3: 1544–1552.PubMedCrossRefGoogle Scholar
  89. Kullik, I., Toledano, M.B., Tartaglia, L.A., and Storz, G., 1995, Mutational analysis of the redox-sensitive transcriptional regulator OxyR: regions important for oxidation and transcriptional activation. J. Bacteriol. 177: 1285–1291.PubMedGoogle Scholar
  90. Lambert, L.A., Ashbire, K., Blankenhorn, D., and Slonczewski, J.L., 1997, Proteins induced in Escherichia coli by benzoic acid. J. Bacteriol. 179: 7595–7599.PubMedGoogle Scholar
  91. Leblanc, L., Leboeuf, C., Leroi, F., Hartke, A., and Yanick, A., 2003, Comparison between NaCl tolerance response and acclimation to cold temperature in Shewanella putrefaciens. Curr. Microbiol. 46: 157–167.PubMedCrossRefGoogle Scholar
  92. Lee, C., Lee, S., Mi, Mukhopadhyay, P., Kim, S., Jun, Lee, S., Chul, Ahn, W.-S., Yu, M.-H., Storz, G., and Ryu, S., Eon, 2004, Redox regulation of OxyR requires specific disulfide bond formation involving a rapid kinetic reaction path. Nat. Struc. Biol. 11: 1179–1185.CrossRefGoogle Scholar
  93. Lee, J.-W., and Helmann, J.D., 2006, The PerR transcription factor senses H2O2 by metal-catalysed histidine oxidation. Nature 440: 363–367.PubMedCrossRefGoogle Scholar
  94. Lesniak, J., Barton, W.A., and Nikolov, D.B., 2002, Structural and functional characterization of the Pseudomonas hydroperoxide resistance protein Ohr. EMBO J. 21: 6649–6659.PubMedCrossRefGoogle Scholar
  95. Lesniak, J., Barton, W.A., and Nikolov, D.B., 2003, Structural and functional features of the Escherichia coli hydroperoxide resistance protein OsmC. Protein Sci. 12: 2838–2843.PubMedCrossRefGoogle Scholar
  96. Liu, S.X., Athar, M., Lippai, I., Waldren, C., and Hei, T.K., 2001, Induction of oxyradicals by arsenic: implication for mechanism of genotoxicity. Proc. Natl. Acad. Sci. USA 98: 1643–1648.PubMedCrossRefGoogle Scholar
  97. Loo, C.Y., Mitrakul, K., Jaafar, S., Gyurko, C., Hughes, C.V., and Ganeshkumar, N., 2004, Role of a nosX homolog in Streptococcus gordonii in aerobic growth and biofilm formation. J. Bacteriol. 186: 8183–8206.CrossRefGoogle Scholar
  98. Loprasert, S., Artichartpongkun, S., Whangsuk, W., and Mongkolsuk, S., 1997, Isolation and analysis of the Xanthomonas alkyl hydroperoxide reductase and the peroxide sensor regulator genes ahpC and ahpF-oxyR-orfX. J. Bacteriol. 179: 3944–3949.PubMedGoogle Scholar
  99. Loprasert, S., Fuangthong, M., Whangsuk, W., Atichartpongkun, S., and Mongkolsuk, S., 2000, Molecular and physiological analysis of an OxyR-regulated ahpC promoter in Xanthomonas campestris pv. phaseoli. Mol. Microbiol. 37: 1504–1514.PubMedCrossRefGoogle Scholar
  100. Loprasert, S., Sallabhan, R., Whangsuk, W., and Mongkolsuk, S., 2003, Compensatory increase in ahpC gene expression and its role in protecting Burkholderia pseudomallei against reactive nitrogen intermediates. Arch. Microbiol. 180: 498–502.PubMedCrossRefGoogle Scholar
  101. Loprasert, S., Whangsuk, W., Sallabhan, R., and Mongkolsuk, S., 2004, DpsA protects the human pathogen Burkholderia pseudomallei against organic hydroperoxide. Arch. Microbio.l 182: 96–101.CrossRefGoogle Scholar
  102. Lundström, A.M., and Bolin, I., 2000, A 26kDa protein of Helicobacter pylori shows alkyl hydroperoxide reductase (AhpC) activity and the mono-cistronic transcription of the gene is affected by pH. Microb. Patho.g 29: 257–266.CrossRefGoogle Scholar
  103. Lundström, A.M., Sundaeus, V., and Bolin, I., 2001, The 26-kilodalton, AhpC homologue, of Helicobacter pylori is also produced by other Helicobacter species. Helicobacter 6: 44–54.PubMedCrossRefGoogle Scholar
  104. Maalej, S., Dammak, I., and Dukan, S., 2006, The impairment of superoxide dismutase coordinates the derepression of the PerR regulon in the response of Staphylococcus aureus to HOCl stress. Microbiol. 152: 855–861.CrossRefGoogle Scholar
  105. Majdalani, N., and Gottesman, S., 2005, The Rcs phosphorelay: a complex signal transduction system. Ann. Rev. Microbiol. 59: 379–405.CrossRefGoogle Scholar
  106. Manca, C., Paul, S., Barry, C.E.I., Freedman, V.H., and Kaplan, G., 1999, Mycobacterium tuberculosis catalase and peroxidase activities and resistance to oxidative killing in human monocytes in vitro. Infect. Immun. 67: 74–79.PubMedGoogle Scholar
  107. Maness, P.-C., Smolinski, S., Blake, D.M., Huang, Z., Wolfrum, E.J., and Jacoby, W.A., 1999, Bactericidal activity of photocatalytic TiO(2) reaction: toward an understanding of its killing mechanism. Appl. Environ. Microbiol. 65: 4094–4098.PubMedGoogle Scholar
  108. Master, S.S., Springer, B., Sander, P., Boettger, E.C., Deretic, V., and Timmins, G.S., 2002, Oxidative stress response genes in Mycobacterium tuberculosis: role of ahpC in resistance to peroxynitrite and stage-specific survival in macrophages. Microbiol. 148: 3139–3144.Google Scholar
  109. Meunier-Jamin, C., Kapp, U., Leonard, G.A., and McSweeney, S., 2004, The structure of the organic hydroperoxide resistance protein from Deinococcus radiodurans. Do conformational changes facilitate recycling of the redox disulfide. J. Biol. Chem. 279: 25830–25837.PubMedCrossRefGoogle Scholar
  110. Michan, C., Manchado, M., Dorado, G., and Pueyo, C., 1999, In vivo transcription of the Escherichia coli oxyR regulon as a function of growth phase and in response to oxidative stress. J. Bacteriol. 181: 2759–2764.PubMedGoogle Scholar
  111. Mongkolsuk, S., and Helmann, J., D., 2002, Regulation of inducible peroxide stress responses. Mol. Microbiol. 45: 9–15.PubMedCrossRefGoogle Scholar
  112. Mongkolsuk, S., Loprasert, S., Whangsuk, W., Fuangthong, M., and Atichartpongkun, S., 1997, Characterization of transcription organization and analysis of unique expression patterns of an alkyl hydroperoxide reductase C gene (ahpC) and the peroxide regulator operon ahpF-oxyR-orfX from Xanthomonas campestris pv. phaseoli. J. Bacteriol. 179: 3950–3955.PubMedGoogle Scholar
  113. Mongkolsuk, S., Praituan, W., Loprasert, S., Fuangthong, M., and Chamnongpol, S., 1998a, Identification and characterization of a new organic hydroperoxide resistance (ohr) gene with a novel pattern of oxidative stress regulation from Xanthomonas campestris pv. phaseoli. J. Bacteriol. 180: 2636–2643.Google Scholar
  114. Mongkolsuk, S., Sukchawalit, R., Loprasert, S., Praituan, W., and Upaichit, A., 1998b, Construction and physiological analysis of a Xanthomonas mutant to examine the role of the oxyR gene in oxidant-induced protection against peroxide killing. J. Bacteriol. 180: 3988–3991.Google Scholar
  115. Mongkolsuk, S., Whangsuk, W., Fuangthong, M., and Loprasert, S., 2000a, Mutations in oxyR resulting in peroxide resistance in Xanthomonas campestris. J. Bacteriol. 182: 3846–3849.CrossRefGoogle Scholar
  116. Mongkolsuk, S., Whangsuk, W., Vattanaviboon, P., Loprasert, S., and Fuangthong, M., 2000b, A Xanthomonas alkyl hydroperoxide reductase subunit C (ahpC) mutant showed an altered peroxide stress response and complex regulation of the compensatory response of peroxide detoxification enzymes. J. Bacteriol. 182: 6845–6849.CrossRefGoogle Scholar
  117. Morgan, R.W., Christman, M.F., Jacobson, F.S., Storz, G., and Ames, B.M., 1986, Hydrogen peroxide-inducible proteins in Salmonella typhimurium overlap with heat shock and other stress proteins. Proc. Natl. Acad. Sci. USA 83: 8059–8063.PubMedCrossRefGoogle Scholar
  118. Morrissey, J.A., Cockayne, A., Brummell, K., and Williams, P., 2004, The staphylococcal ferritins are differentially regulated in response to iron and manganese and via PerR and Fur. Infect. Immun. 72: 972–979.PubMedCrossRefGoogle Scholar
  119. Mostertz, J., Scharf, C., Hecker, M., and Homuth, G., 2004, Transcriptome and proteome analysis of Bacillus subtilis gene expression in response to superoxide and peroxide stress. Microbiol. 150: 497–512.CrossRefGoogle Scholar
  120. Mukhopadhyay, S., Miller, R.D., and Summersgill, J.T., 2004, Analysis of altered protein expression patterns of Chlamydia pneumoniae by an integrated proteome-works system. J. Proteome Res. 3: 878–883.PubMedCrossRefGoogle Scholar
  121. Nathan, C., and Shiloh, M.U., 2000, Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. USA 97: 8841–8848.PubMedCrossRefGoogle Scholar
  122. Newman, E.B., and Lin, R., 1995, Leucine-responsive regulatory protein: a global regulator of gene expression in E. coli. Ann. Rev. Microbiol. 49: 747–775.CrossRefGoogle Scholar
  123. Ochsner, U.A., Hassett, D.J., and Vasil, M.L., 2001, Genetic and physiological characterization of ohr, encoding a protein involved in organic hydroperoxide resistance in Pseudomonas aeruginosa. J. Bacteriol. 183: 773–778.PubMedCrossRefGoogle Scholar
  124. Ochsner, U.A., Vasil, M.L., Eyad, A., Kislay, P., and Hassett, D.J., 2000, Role of the Pseudomonas aeruginosa oxyR-recG operon in oxidative stress defense and DNA repair: OxyR-dependent regulation of katB-ankB, ahpB, and ahpC-ahpF. J. Bacteriol. 182: 4533–44.PubMedCrossRefGoogle Scholar
  125. Ohara, N., Kikuchi, Y., Shoji, M., Naito, M., and Nakayama, K., 2006, Superoxide dismutase-encoding gene of the obligate anaerobe Porphyromonas gingivalis is regulated by the redox-sensing transcription activator OxyR. Microbiol. 152: 955–966.CrossRefGoogle Scholar
  126. Okano, S., Shibata, Y., Shiroza, T., and Abiko, Y., 2006, Proteomics-based analysis of a counter-oxidative stress system in Porphyromonas gingivalis. Proteomics 6: 251–258.PubMedCrossRefGoogle Scholar
  127. Olczak, A.A., Olson, J.W., and Maier, R.J., 2002, Oxidative-stress resistance mutants of Helicobacter pylori. J. Bacteriol. 184: 3186–3193.PubMedCrossRefGoogle Scholar
  128. Olczak, A.A., Seyler, R.W., Olson, J.W., and Maier, R.J., 2003, Association of Helicobacter pylori antioxidant activities with host colonization proficiency. Infect. Immun. 71: 580–583.PubMedCrossRefGoogle Scholar
  129. Old, I.G., Phillips, S.E.V., Stockley, P.G., and Saint Girons, I., 1991, Regulation of methionine biosynthesis in the Enterobacteriaceae. Prog. Biophys. Mol. Biol. 56: 145–185.PubMedCrossRefGoogle Scholar
  130. Oliveira, M.A., Guimares, B.G., Cussiol, J.R.R., Medrano, F.J., Gozzo, F.C., and Netto, L.E.S., 2006, Structural insights into enzyme-substrate interaction and characterization of enzymatic intermediates of organic hydroperoxide resistance protein from Xylella fastidiosa. J. Mol. Biol. 359: 433–435.PubMedCrossRefGoogle Scholar
  131. Olsen, I., Reitan, L.J., Holstad, G., and Wiker, H.G., 2000, Alkyl hydroperoxide reductases C and D are major antigens constitutively expressed by Mycobacterium avium subsp. paratuberculosis. Infect. Immun. 68: 801–808.CrossRefGoogle Scholar
  132. Olsen, I., Tryland, M., Wiker, H.G., and Reitan, L.J., 2001, AhpC, AhpD, and a secreted 14-kilodalton antigen from Mycobacterium avium subsp. paratuberculosis distinguish between paratuberculosis and bovine tuberculosis in an enzyme-linked immunosorbent assay. Clin. Diagn. Lab. Immunol. 8: 797–801.PubMedGoogle Scholar
  133. Oram, D., Marra, Avdalovic, A., and Holmes, R.K., 2002, Construction and characterization of transposon insertion mutations in Corynebacterium diphtheriae that affect expression of the diphtheria toxin repressor (DtxR). J. Bacteriol. 184: 5723–5732.CrossRefGoogle Scholar
  134. Pagan-Ramos, E., Master, S.S., Pritchett, C.L., Reimschuessel, R., Trucksis, M., Timmins, G.S., and Deretic, V., 2006, Molecular and physiological effects of mycobacterial oxyR inactivation. J. Bacteriol. 188: 2674–2680.PubMedCrossRefGoogle Scholar
  135. Pagan-Ramos, E., Song, J., McFalone, M., Mudd, M.H., and Deretic, V., 1998, Oxidative stress response and characterization of the oxyR-ahpC and furA-katG loci in Mycobacterium marinum. J. Bacteriol. 180: 4856–4864.PubMedGoogle Scholar
  136. Paget, M.S., and Buttner, M.J., 2003, Thiol-based regulatory switches. Ann. Rev. Genet. 37: 91–121.PubMedCrossRefGoogle Scholar
  137. 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.PubMedCrossRefGoogle Scholar
  138. 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.PubMedCrossRefGoogle Scholar
  139. Park, S., You, X., and Imlay, J.A., 2005, Substantial DNA damage from submicromolar intracellular hydrogen peroxide detected in Hpx- mutants of Escherichia coli. Proc. Natl. Acad. Sci. USA 102: 9317–9322.PubMedCrossRefGoogle Scholar
  140. Parsonage, D., Youngblood, D.S., Ganapathy, N.S., Wood, Z.A., Karpus, A.P., and Poole, L.B., 2005, Analysis of the link between enzymatic activity and oligomeric state in AhpC, a bacterial peroxiredoxin. Biochemistry 44: 10583–10592.PubMedCrossRefGoogle Scholar
  141. Pomposiello, P.J., and Demple, B., 2002, Global adjustment of microbial physiology during free radical stress. Adv. Microb. Physiol. 46: 319–341.PubMedCrossRefGoogle Scholar
  142. Poole, L.B., Higuchi, M., Shimada, M., Calzi, M., Li, and Kamio, Y., 2000a, Streptococcus mutans H2O2-forming NADH oxidase is an alkyl hydroperoxide reductase protein. Free Rad. Biol. Med. 28: 108–120.CrossRefGoogle Scholar
  143. Poole, L.B., Reynolds, C.M., Wood, Z.A., Karpus, A.P., Ellis, H.R., and Li Calzi, M., 2000b, AhpF and other NADH:peroxiredoxin oxidoreductases, homologues of low Mr thioredoxin reductase. Eur. J. Biochem. 267: 6126–6133.CrossRefGoogle Scholar
  144. Pym, A.S., Domenech, P., Honore, N., Song, J., Deretic, V., and Cole, S.T., 2001, Regulation of catalase-peroxidase (KatG) expression, isoniazid sensitivity and virulence by furA of Mycobacterium tuberculosis. Mol. Microbiol. 40: 879–889.PubMedCrossRefGoogle Scholar
  145. Rahav-Manor, O., Carmel, O., Karpel, R., Taglicht, D., Glaser, G., Schuldiner, S., and Padan, E., 1992, NhaR, a protein homologous to a family of bacterial regulatory proteins (LysR), regulates nhaA, the sodium proton antiporter gene in Escherichia coli. J. Biol. Chem. 267: 10433–10438.PubMedGoogle Scholar
  146. Rankin, S., Li, Z., and Isberg, R.R., 2002, Macrophage-induced genes of Legionella pneumophila: protection from reactive intermediates and solute imbalance during intracellular growth. Infect. Immun. 70: 3637–3648.PubMedCrossRefGoogle Scholar
  147. Rehse, P.H., Ohshima, N., Nodake, Y., and Tahirov, T.H., 2004, Crystallographic structure and biochemical analysis of the Thermus thermophilus osmotically inducible protein C. J. Mol. Biol. 338: 959–968.PubMedCrossRefGoogle Scholar
  148. Rho, B.-S., Hung, L.-W., Holton, J.M., Vigil, D., Kim, S.-I., Park, M.S., Terwillinger, T.C., and Pedelacq, J.-D., 2006, Functional and Structural Characterization of a Thiol Peroxidase from Mycobacterium tuberculosis. J. Mol. Biol. 361: 850–863.PubMedCrossRefGoogle Scholar
  149. Rickman, L., Scott, C., Hunt, D.M., Hutchinson, T., Menendez, M.C., Whalan, R., Hinds, J., Colston, M.J., Green, J., and Buxton, R.S., 2005, A member of the cAMP receptor protein family of transcription regulators in Mycobacterium tuberculosis is required for virulence in mice and controls transcription of the rpfA gene coding for a resuscitation promoting factor. Mol. Microbiol. 56: 1274–1286.PubMedCrossRefGoogle Scholar
  150. Rince, A., Giard, J.-C., Pichereau, V., Flahaut, S., and Auffray, Y., 2001, Identification and characterization of gsp65, an organic hydroperoxide resistance (ohr) gene encoding a general stress protein in Enterococcus faecalis. J. Bacteriol. 183: 1482–1488.PubMedCrossRefGoogle Scholar
  151. Rocha, E.R., Owens, G.J., and Smith, C.J., 2000, The redox-sensitive transcriptional activator OxyR regulates the peroxide response regulon in the obligate anaerobe Bacteroides fragilis. J. Bacteriol. 182: 5059–5069.PubMedCrossRefGoogle Scholar
  152. Rocha, E.R., and Smith, C.J., 1998, Characterization of a peroxide-resistant mutant of the anaerobic bacterium Bacteroides fragilis. J. Bacteriol. 180: 5906–5912.PubMedGoogle Scholar
  153. Rocha, E.R., and Smith, C.J., 1999, Role of the alkyl hydroperoxide reductase (ahpCF) gene in oxidative stress defense of the obligate anaerobe Bacteroides fragilis. J. Bacteriol. 181: 5701–5710.PubMedGoogle Scholar
  154. Rosenkrands, I., King, A., Weldingh, K., Moniatte, M., Moertz, E., and Andersen, P., 2000a, Towards the proteome of Mycobacterium tuberculosis. Electrophoresis 21: 3740–3756.CrossRefGoogle Scholar
  155. Rosenkrands, I., Weldingh, K., Jacobsen, S., Hansen, C.V., Florio, W., Gianetri, I., and Andersen, P., 2000b, Mapping and identification of Mycobacterium tuberculosis proteins by two-dimensional gel electrophoresis, microsequencing and immunodetection. Electrophoresis 21: 935–48.CrossRefGoogle Scholar
  156. Rozwarski, D.A., Grant, G.A., Barton, D.H.R., Jacobs, W.R.J., and Sacchettini, J.C., 1998, Modification of the NADH of the isoniazid target (InhA) from Mycobacterium tuberculosis. Science 279: 98–102.PubMedCrossRefGoogle Scholar
  157. Schell, M.A., 1993, Molecular biology of the LysR family of transcriptional regulators. Ann. Rev. Microbiol. 47: 597–626.CrossRefGoogle Scholar
  158. Seaver, L.C., and Imlay, J.A., 2001, Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J. Bacteriol. 183: 7173–7181.PubMedCrossRefGoogle Scholar
  159. Semchyshyn, H., Bagnyukova, T., Storey, K., and Storey, V., 2005, Hydrogen peroxide increases the activities of soxRS regulon enzymes and the levels of oxidized proteins and lipids in Escherichia coli. Cell Biol. Int. 70: 424–431.Google Scholar
  160. Shao, F., Bader, M.W., Jalob, U., and Bardwell, J.C.A., 2000, DsbG, a protein disulfide isomerase with chaperone activity. J. Biol. Chem. 275: 13349–13352.PubMedCrossRefGoogle Scholar
  161. Shea, R.J., and Mulks, M.H., 2002, ohr, Encoding an organic hydroperoxide reductase, is an in vivo-induced gene in Actinobacillus pleuropneumoniae. Infect. Immun. 70: 794–802.PubMedCrossRefGoogle Scholar
  162. Sherman, D.R., Mdhluli, K., Hickey, M.J., Arain, T.M., M., M.S., Barry, C.E.I., and Stover, C.K., 1996, Compensatory ahpC gene expression in isoniazid-resistant Mycobacterium tuberculosis. Science 272: 1641–1643.PubMedCrossRefGoogle Scholar
  163. Sherman, D.R., Mdhluli, K., Hickey, M.J., Barry, C.E.I., and Stover, C.K., 1999, AhpC, oxidative stress and drug resistance in Mycobacterium tuberculosis. Biofactors 10: 211–217.PubMedCrossRefGoogle Scholar
  164. Sherman, D.R., Sabo, P.J., Hickey, M.J., Arain, T.M., Mahairas, G.G., Yuan, Y., Barry, C.E.I., and Stover, C.K., 1995, Disparate responses to oxidative stress in saprophytic and pathogenic mycobacteria. Proc. Natl. Acad. Sci. USA 92: 6625–6629.PubMedCrossRefGoogle Scholar
  165. Shi, S., and Ehrt, S., 2006, Dihydrolipoamide acyltransferase is critical for Mycobacterium tuberculosis pathogenesis. Infect. Immun. 74: 56–63.PubMedCrossRefGoogle Scholar
  166. Shin, D.H., Choi, I.-G., Busso, D., Jancarik, J., Yokota, H., Kim, R., and Kim, S.-H., 2004, Structure of OsmC from Escherichia coli: a salt-shock-induced protein. Acta Crystallogr. D Biol. Crystallogr. 60: 903–911.PubMedCrossRefGoogle Scholar
  167. Slonczewski, J.L., Mcgee, D.J., Phillips, J., Kirkpatrick, C., and Mobley, H.L.T., 2000, pH-dependent protein profiles of Helicobacter pylori analyzed by two-dimensional gels. Helicobacter 5: 240–247.PubMedCrossRefGoogle Scholar
  168. Spatafora, G., Van Hoeven, N., Wagner, K., and Fives-Taylor, P., 2002, Evidence that ORF3 at the Streptococcus parasanguis fimA locus encodes a thiol-specific antioxidant. Microbiol. 148: 755–762.Google Scholar
  169. Springer, B., Sander, P., Zahrt, T., McFalone, M., Song, J., Papavinasasundaram, K.G., Colston, M.J., Boettger, E., and Deretic, V., 2001, Silencing of oxidative stress response in Mycobacterium tuberculosis: expression patterns of ahpC in virulent and avirulent strains and effect of ahpC inactivation. Infect. Immun. 69: 5967–5973.PubMedCrossRefGoogle Scholar
  170. Stancik, L.M., Stancik, D.M., Schmidt, B., Barnhart, D.M., Yoncheva, Y., N., and Slonczewski, J.L., 2002, pH-dependent expression of periplasmic proteins and amino acid catabolism in Escherichia coli. J. Bacteriol. 184: 4246–4258.PubMedCrossRefGoogle Scholar
  171. Staudinger, B.J., Oberdoerster, M.A., Lewis, P.J., and Rosen, H., 2002, mRNA expression profiles for Escherichia coli ingested by normal and phagocyte oxidase-deficient human neutrophils. J. Clin. Invest. 110: 1151–1163.PubMedGoogle Scholar
  172. Storz, G., Christman, M.F., Sies, H., and Ames, B.M., 1987, Spontaneous mutagenesis and oxidative damage to DNA in Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 84: 8917–8921.PubMedCrossRefGoogle Scholar
  173. Storz, G., Jacobson, F.S., Tartaglia, L.A., Morgan, R.W., Silveira, L.A., and Ames, B.M., 1989, An alkyl hydroperoxide reductase induced by oxidative stress in Salmonella typhimurium and Escherichia coli: genetic characterization and cloning of ahp. J. Bacteriol. 171: 2049–2055.PubMedGoogle Scholar
  174. Storz, G., Tartaglia, L.A., and Ames, B.M., 1990, Transcriptional regulator of oxidative stress inducible genes: direct activation by oxidation. Science 248: 189–194.PubMedCrossRefGoogle Scholar
  175. Storz, G., and Zheng, M., 2000, Oxidative stress, in Bacterial stress responses (torz, G. and Hengge-Aronis, R., eds.), American Society for Microbiology Press, Washington, DC, USA, pp. 47–59.Google Scholar
  176. Sturny, R., Cam, K., Gutierrez, C., and Conter, A., 2003, NhaR and RcsB independently regulate the osmCp1 promoter of Escherichia coli at overlapping regulatory sites. J. Bacteriol. 185: 4298–4304.PubMedCrossRefGoogle Scholar
  177. Sukchawalit, R., Loprasert, S., Atichartpongkun, S., and Mongkolsuk, S., 2001, Complex regulation of the organic hydroperoxide resistance gene (ohr) from Xanthomonas involves OhrR, a novel organic peroxide-inducible negative regulator, and posttranscriptional modifications. J. Bacteriol. 183: 4405–4412.PubMedCrossRefGoogle Scholar
  178. Tai, S.S., and Zhu, Y., Yi, 1995, Cloning of a Corynebacterium diphtheriae iron-repressible gene that shares sequence homology with the AhpC subunit of alkyl hydroperoxide reductase of Salmonella typhimurium. J. Bacteriol. 177: 3512–3517.PubMedGoogle Scholar
  179. Tartaglia, L.A., Storz, G., and Ames, B.M., 1989, Identification and molecular analysis of oxyR-regulated promoters important for the bacterial adaptation to oxidative stress. J. Mol. Biol. 210: 709–719.PubMedCrossRefGoogle Scholar
  180. Tartaglia, L.A., Storz, G., Brodsky, M.H., Lai, A., and Ames, B.M., 1990, Alkyl hydroperoxide reductase from Salmonella typhimurium. Sequence and homology to thioredoxin reductase and other flavoprotein disulfide oxidoreductases. J. Biol. Chem. 265: 10535–10540.PubMedGoogle Scholar
  181. Taylor, P.D., Inchley, C.J., and Gallagher, M.P., 1998, The Salmonella typhimurium AhpC polypeptide is not essential for virulence in BALB/c mice but is recognized as an antigen during infection. Infect. Immun. 66: 3207–3217.Google Scholar
  182. Tellez-Sosa, J., Soberon, N., Vega-Segura, A., Torres-Marquez, M.E., and Cevallos, M.A., 2002, The Rhizobium etli cyaC product: characterization of a novel adenylate cyclase class. J. Bacteriol. 184: 3560–3568.PubMedCrossRefGoogle Scholar
  183. Toesca, I., Perard, C., Bouvier, J., Gutierrez, C., and Conter, A., 2001, The transcriptional activator NhaR is responsible for the osmotic induction of osmC(P1), a promoter of the stress-inducible gene osmC in Escherichia coli. Microbiol. 147: 2795–2803.Google Scholar
  184. Toledano, M.B., Kullik, I., Trinh, F., Baird, P.T., Schneider, T.D., and Storz, G., 1994, Redox-dependent shift of OxyR-DNA contacts along an extended DNA-binding site: a mechanism for differential promoter selection. Cell 78: 897–909.PubMedCrossRefGoogle Scholar
  185. van Vliet, A.H.M., Baillon, M.-L.A., Penn, C.W., and Ketley, J.M., 1999, Campylobacter jejuni contains two fur homologs: characterization of iron-responsive regulation of peroxide stress defense genes by the PerR repressor. J. Bacteriol. 181: 6371–6376.PubMedGoogle Scholar
  186. Vattanaviboon, P., Whangsuk, W., Panmanee, W., Klomsiri, C., Dharmsthiti, S., and Mongkolsuk, S., 2002, Evaluation of the roles that alkyl hydroperoxide reductase and Ohr play in organic peroxide-induced gene expression and protection against organic peroxides in Xanthomonas campestris. Biochem. Biophys. Res. Commun. 299: 177–182.PubMedCrossRefGoogle Scholar
  187. Verneuil, N., Le Breton, Y., Hartke, A., Auffray, Y., and Giard, J.-C., 2004a, Identification of a new oxidative stress transcriptional regulator in Enterococcus faecalis. Lait. 84: 69–76.CrossRefGoogle Scholar
  188. Verneuil, N., Sanguinetti, M., Le Breton, Y., Posteraro, B., Fadda, G., Auffray, Y., Hartke, A., and Giard, J.-C., 2004b, Effects of the Enterococcus faecalis hypR gene encoding a new transcriptional regulator on oxidative stress response and intracellular survival within macrophages. Infect. Immun. 72: 4424–4431.CrossRefGoogle Scholar
  189. Verneuil, N., Rince, A., Sanguinetti, M., Auffray, Y., Hartke, A., and Giard, J.-C., 2005, Implication of hypR in the virulence and oxidative stress response of Enterococcus faecalis. FEMS Microbiol. Let.t 252: 137–141.CrossRefGoogle Scholar
  190. Volker, U., Maul, B., and Hecker, M., 1998, One of two osmC homologs in Bacillus subtilis is part of the sigmaB-dependent general stress regulon. J. Bacteriol. 180: 4212–4218.PubMedGoogle Scholar
  191. Wan, X.-Y., Zhou, Y., Yan, Z.-Y., Wang, H.-L., Hou, Y.-D., and Jin, D.-Y., 1997, Scavengase p20: a novel family of bacterial antioxidant enzymes. FEBS Lett. 407: 32–36.PubMedCrossRefGoogle Scholar
  192. Wang, G., Conover, R.C., Benoit, S., Olczak, A.A., Olson, J.W., Johnson, M.K., and Maier, R.J., 2004, Role of a bacterial organic hydroperoxide detoxification system in preventing catalase inactivation. J. Biol. Chem. 279: 51908–51914.PubMedCrossRefGoogle Scholar
  193. Wang, G., Conover, R.C., Olczak, A.A., Alamuri, P., Johnson, M.K., and Maier, R.J., 2005, Oxidative stress defense mechanisms to counter iron-promoted DNA damage in Helicobacter pylori. Free Rad. Res. 39: 1183–1191.CrossRefGoogle Scholar
  194. Wang, G., and P., D.M., 1998, Heat shock response enhances acid tolerance of Escherichia coli O157:H7. Lett Appl Microbiol 26: 31–34.Google Scholar
  195. Weldingh, K., Rosenkrands, I., Jacobsen, S., Rasmussen, P.B., Elhay, M.J., and Andersen, P., 1998, Two-dimensional electrophoresis for analysis of Mycobacterium tuberculosis culture filtrate and purification and characterization of six novel proteins. Infect. Immun. 66: 3492–3500.PubMedGoogle Scholar
  196. 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.PubMedGoogle Scholar
  197. Williams, C.H., Arscott, L.D., Müller, S., Lennon, B.W., Ludwig, M.L., Wang, P.-F., Veine, D.M., Becker, K., and Schirmer, R.H., 2000, Thioredoxin reductase two modes of catalysis have evolved. Eur. J. Biochem. 267: 6110–6117.PubMedCrossRefGoogle Scholar
  198. Wilson, T., de lisle, G.W., Marcinkeviciene, J.A., Blanchard, J.S., and Collins, D.M., 1998, Antisense RNA to ahpC, an oxidative stress defence gene involved in isoniazid resistance, indicates that AhpC of Mycobacterium bovis has virulence properties. Microbiol. 144: 2687–2695.CrossRefGoogle Scholar
  199. Windle, H.J., Ang, Y.S., Athie-Morales, V., McManus, R., and Kelleher, D., 2006, Human peripheral and gastric lymphocyte responses to Helicobacter pylori NapA and AhpC differ in infected and uninfected individuals. Gut 54: 25–32.CrossRefGoogle Scholar
  200. Wood, Z.A., Poole, L.B., Hantgan, R.R., and Karpus, A.P., 2002, Dimers to doughnuts: redox-sensitive oligomerization of 2-cysteine peroxiredoxins. Biochemistry 41: 5493–5504.PubMedCrossRefGoogle Scholar
  201. Wood, Z.A., Schroeder, E., Harris, J.R., and Poole, L.B., 2003, Structure, mechanism and regulation of peroxiredoxins. Trends Biochem. Sci. 28: 32–40.PubMedCrossRefGoogle Scholar
  202. Yamaguchi, R., Matsuo, K., Yamazaki, A., Takahashi, M., Fukasawa, Y., Wada, M., and Abe, C., 1992, Cloning and expression of the gene for the Avi-3 antigen of Mycobacterium avium and mapping of its epitopes. Infect. Immun. 60: 1210–1216.PubMedGoogle Scholar
  203. Yamamoto, Y., 2000a, Molecular biology of oxygen tolerance in lactic acid bacteria: Functions of NADH oxidases and Dpr in oxidative stress. Biosci Biotech Biochem 90: 484–493.Google Scholar
  204. Yamamoto, Y., Higuchi, M., Poole, L.B., and Kamio, Y., 2000b, Role of the dpr product in oxygen tolerance in Streptococcus mutans. J. Bacteriol. 182: 3740–3747.CrossRefGoogle Scholar
  205. Zarht, T.C., and Deretic, V., 2002, Reactive nitrogen and oxygen intermediates and bacterial defenses: unusual adaptations in Mycobacterium tuberculosis. Antioxid. Redox Signal. 4: 141–159.CrossRefGoogle Scholar
  206. Zhang, Y., Dhandayuthapani, S., and Deretic, V., 1996, Molecular basis for the exquisite sensitivity of Mycobacterium tuberculosis to isoniazid. Proc. Natl. Acad. Sci. USA 93: 13212–13216.PubMedCrossRefGoogle Scholar
  207. Zhang, Y., Heym, B., Allen, B., Young, D., and Cole, S., 1992, The catalase-peroxidase gene and isoniazid resistance of Mycobacterium tuberculosis. Nature 358: 591–593.PubMedCrossRefGoogle Scholar
  208. Zhao, X., Yu, H., Yu, S., Wang, F., Sacchettini, J.C., and Magliozzo, R.S., 2006, Hydrogen peroxide-mediated isoniazid activation catalyzed by Mycobacterium tuberculosis catalase-peroxidase (KatG) and its S315T mutant. Biochemistry 45: 4131–4140.PubMedCrossRefGoogle Scholar
  209. Zheng, M., Aslund, F., and Storz, G., 1998, Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279: 1718–1721.PubMedCrossRefGoogle Scholar
  210. Zheng, M., and Storz, G., 2000, Redox sensing by prokaryotic transcription factors. Biochem. Pharmacol. 59: 1–6.PubMedCrossRefGoogle Scholar
  211. Zheng, M., Wang, X., Doan, B., Lewis, K.A., and Schneider, T.D., 2001a, Computation-directed identification of OxyR DNA binding sites in Escherichia coli. J. Bacteriol. 183: 4571–4591.CrossRefGoogle Scholar
  212. Zheng, M., Wang, X., Templeton, L.J., Smulski, D.R., LaRossa, R.A., and Storz, G., 2001b, DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J. Bacteriol. 183: 4562–4570.CrossRefGoogle Scholar
  213. Zhou, Y., Wan, X.-Y., Wang, H.-L., Yan, Z.-Y., Hou, Y.-D., and Jin, D.-Y., 1997, Bacterial scavengase p20 is structurally and functionally related to peroxiredoxins. Biochem. Biophys. Res. Commun. 233: 848–852.PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • James M. Dubbs
    • 1
  • Skorn Mongkolsuk
    • 1
    • 2
  1. 1.Laboratory of BiotechnologyChulabhorn Research InstituteLak SiThailand
  2. 2.Department of Biotechnology,Faculty of ScienceMahidol UniversityBangkokThailand

Personalised recommendations