1887

Abstract

The role of the HO-sensing transcriptional regulator OxyR in oxidative stress responses in was investigated. An deletion mutant was more sensitive to HO and -butyl hydroperoxide than was the WT strain, indicating that OxyR mediates the defensive system against HO and organic peroxide. Evidence presented herein suggests that in cells treated with exogenous HO, the oxidized form of OxyR activated expression of by binding to a palindromic sequence of the promoter region. Oxidized OxyR also induced expression of other antioxidant enzymes (KatA1, KatA2, KatA3 and OhrB1) and oxidative stress regulators (CatR, OhrR and σ). The thiol-oxidative stress regulator gene was regulated at the transcription level by OxyR. We conclude that OxyR is necessary to activate transcription of from the σ-dependent promoter to express an unstable larger isoform of σ during oxidative stress. In response to oxidative stress, OxyR facilitates rapid production of HO-scavenging enzymes to repair oxidative damage through direct regulation and cascaded regulation of CatR, OhrR and σ.

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2016-04-01
2019-10-14
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References

  1. Atichartpongkul S. , Loprasert S. , Vattanaviboon P. , Whangsuk W. , Helmann J. D. , Mongkolsuk S. . ( 2001;). Bacterial Ohr and OsmC paralogues define two protein families with distinct functions and patterns of expression. Microbiology 147: 1775–1782 [CrossRef] [PubMed].
    [Google Scholar]
  2. Bae J. B. , Park J. H. , Hahn M. Y. , Kim M. S. , Roe J. H. . ( 2004;). Redox-dependent changes in RsrA, an anti-sigma factor in Streptomyces coelicolor: zinc release and disulfide bond formation. J Mol Biol 335: 425–435 [CrossRef] [PubMed].
    [Google Scholar]
  3. Bierman M. , Logan R. , O'Brien K. , Seno E. T. , Rao R. N. , Schoner B. E. . ( 1992;). Plasmid cloning vectors for the conjugal transfer of DNA from Escherichia coli to Streptomyces spp. Gene 116: 43–49 [CrossRef] [PubMed].
    [Google Scholar]
  4. Burg R. W. , Miller B. M. , Baker E. E. , Birnbaum J. , Currie S. A. , Hartman R. , Kong Y. L. , Monaghan R. L. , Olson G. , other authors . ( 1979;). Avermectins, new family of potent anthelmintic agents: producing organism and fermentation. Antimicrob Agents Chemother 15: 361–367 [CrossRef] [PubMed].
    [Google Scholar]
  5. Chater K. F. . ( 1993;). Genetics of differentiation in Streptomyces . Annu Rev Microbiol 47: 685–711 [CrossRef] [PubMed].
    [Google Scholar]
  6. Christman M. F. , Storz G. , Ames B. N. . ( 1989;). OxyR, a positive regulator of hydrogen peroxide-inducible genes in Escherichia coli and Salmonella typhimurium, is homologous to a family of bacterial regulatory proteins. Proc Natl Acad Sci U S A 86: 3484–3488 [CrossRef] [PubMed].
    [Google Scholar]
  7. Dubbs J. M. , Mongkolsuk S. . ( 2012;). Peroxide-sensing transcriptional regulators in bacteria. J Bacteriol 194: 5495–5503 [CrossRef] [PubMed].
    [Google Scholar]
  8. Hahn J. S. , Oh S. Y. , Chater K. F. , Cho Y. H. , Roe J. H. . ( 2000;). H2O2-sensitive fur-like repressor CatR regulating the major catalase gene in Streptomyces coelicolor . J Biol Chem 275: 38254–38260 [CrossRef] [PubMed].
    [Google Scholar]
  9. Hahn J. S. , Oh S. Y. , Roe J. H. . ( 2002;). Role of OxyR as a peroxide-sensing positive regulator in Streptomyces coelicolor A3(2). J Bacteriol 184: 5214–5222 [CrossRef] [PubMed].
    [Google Scholar]
  10. Herbig A. F. , 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 [CrossRef] [PubMed].
    [Google Scholar]
  11. Ikeda H. , Kotaki H. , Tanaka H. , Omura S. . ( 1988;). Involvement of glucose catabolism in avermectin production by Streptomyces avermitilis. Antimicrob Agents Chemother 32: 282–284.[CrossRef]
    [Google Scholar]
  12. Imlay J. A. . ( 2013;). The molecular mechanisms and physiological consequences of oxidative stress: lessons from a model bacterium. Nat Rev Microbiol 11: 443–454 [CrossRef] [PubMed].
    [Google Scholar]
  13. Jiang L. , Liu Y. , Wang P. , Wen Y. , Song Y. , Chen Z. , Li J. . ( 2011;). Inactivation of the extracytoplasmic function sigma factor Sig6 stimulates avermectin production in Streptomyces avermitilis . Biotechnol Lett 33: 1955–1961 [CrossRef] [PubMed].
    [Google Scholar]
  14. Kang J. G. , Paget M. S. , Seok Y. J. , Hahn M. Y. , Bae J. B. , Hahn J. S. , Kleanthous C. , Buttner M. J. , Roe J. H. . ( 1999;). RsrA, an anti-sigma factor regulated by redox change. EMBO J 18: 4292–4298 [CrossRef] [PubMed].
    [Google Scholar]
  15. Kieser T. , Bibb M. J. , Buttner M. J. , Chater K. F. , Hopwood D. A. . ( 2000;). Practical Streptomyces Genetics The John Innes Foundation; Norwich, UK:.
    [Google Scholar]
  16. Kim M. S. , Hahn M. Y. , Cho Y. , Cho S. N. , Roe J. H. . ( 2009;). Positive and negative feedback regulatory loops of thiol-oxidative stress response mediated by an unstable isoform of σR in actinomycetes. Mol Microbiol 73: 815–825 [CrossRef] [PubMed].
    [Google Scholar]
  17. Kim M. S. , Dufour Y. S. , Yoo J. S. , Cho Y. B. , Park J. H. , Nam G. B. , Kim H. M. , Lee K. L. , Donohue T. J. , Roe J. H. . ( 2012;). Conservation of thiol-oxidative stress responses regulated by SigR orthologues in actinomycetes. Mol Microbiol 85: 326–344 [CrossRef] [PubMed].
    [Google Scholar]
  18. Kullik I. , Toledano M. B. , Tartaglia L. A. , Storz G. . ( 1995;). Mutational analysis of the redox-sensitive transcriptional regulator OxyR: regions important for oxidation and transcriptional activation. J Bacteriol 177: 1275–1284 [PubMed].
    [Google Scholar]
  19. MacNeil D. J. , Klapko L. M. . ( 1987;). Transformation of Streptomyces avermitilis by plasmid DNA. J Ind Microbiol 2: 209–218 [CrossRef].
    [Google Scholar]
  20. Mishra S. , Imlay J. . ( 2012;). Why do bacteria use so many enzymes to scavenge hydrogen peroxide?. Arch Biochem Biophys 525: 145–160 [CrossRef] [PubMed].
    [Google Scholar]
  21. Mongkolsuk S. , Praituan W. , Loprasert S. , Fuangthong M. , Chamnongpol S. . ( 1998;). 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 [PubMed].
    [Google Scholar]
  22. Oh S. Y. , Shin J. H. , Roe J. H. . ( 2007;). Dual role of OhrR as a repressor and an activator in response to organic hydroperoxides in Streptomyces coelicolor . J Bacteriol 189: 6284–6292 [CrossRef] [PubMed].
    [Google Scholar]
  23. Paget M. S. , Kang J. G. , Roe J. H. , Buttner M. J. . ( 1998;). σR, an RNA polymerase sigma factor that modulates expression of the thioredoxin system in response to oxidative stress in Streptomyces coelicolor A3(2). EMBO J 17: 5776–5782 [CrossRef] [PubMed].
    [Google Scholar]
  24. Paget M. S. , Bae J. B. , Hahn M. Y. , Li W. , Kleanthous C. , Roe J. H. , Buttner M. J. . ( 2001a;). Mutational analysis of RsrA, a zinc-binding anti-sigma factor with a thiol-disulphide redox switch. Mol Microbiol 39: 1036–1047 [CrossRef] [PubMed].
    [Google Scholar]
  25. Paget M. S. , Molle V. , Cohen G. , Aharonowitz Y. , Buttner M. J. . ( 2001b;). Defining the disulphide stress response in Streptomyces coelicolor A3(2): identification of the σR regulon. Mol Microbiol 42: 1007–1020 [CrossRef] [PubMed].
    [Google Scholar]
  26. Pomposiello P. J. , Bennik M. H. , Demple B. . ( 2001;). Genome-wide transcriptional profiling of the Escherichia coli responses to superoxide stress and sodium salicylate. J Bacteriol 183: 3890–3902 [CrossRef] [PubMed].
    [Google Scholar]
  27. Ramakers C. , Ruijter J. M. , Deprez R. H. , Moorman A. F. . ( 2003;). Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339: 62–66 [CrossRef] [PubMed].
    [Google Scholar]
  28. Seaver L. C. , Imlay J. A. . ( 2004;). Are respiratory enzymes the primary sources of intracellular hydrogen peroxide?. J Biol Chem 279: 48742–48750 [CrossRef] [PubMed].
    [Google Scholar]
  29. Storz G. , Tartaglia L. A. , Ames B. N. . ( 1990;). Transcriptional regulator of oxidative stress-inducible genes: direct activation by oxidation. Science 248: 189–194 [CrossRef] [PubMed].
    [Google Scholar]
  30. Sukchawalit R. , Loprasert S. , Atichartpongkul S. , 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 [CrossRef] [PubMed].
    [Google Scholar]
  31. Zhao J. L. , Wen Y. , Chen Z. , Song Y. , Li J. L. . ( 2007;). An adpA homologue in Streptomyces avermitilis is involved in regulation of morphogenesis and melanogenesis. Chin Sci Bull 52: 623–630 [CrossRef].
    [Google Scholar]
  32. Zheng M. , Aslund F. , Storz G. . ( 1998;). Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279: 1718–1722 [CrossRef] [PubMed].
    [Google Scholar]
  33. Zheng M. , Wang X. , Doan B. , Lewis K. A. , Schneider T. D. , Storz G. . ( 2001a;). Computation-directed identification of OxyR DNA binding sites in Escherichia coli . J Bacteriol 183: 4571–4579 [CrossRef] [PubMed].
    [Google Scholar]
  34. Zheng M. , Wang X. , Templeton L. J. , Smulski D. R. , LaRossa R. A. , Storz G. . ( 2001b;). DNA microarray-mediated transcriptional profiling of the Escherichia coli response to hydrogen peroxide. J Bacteriol 183: 4562–4570 [CrossRef] [PubMed].
    [Google Scholar]
  35. Zianni M. , Tessanne K. , Merighi M. , Laguna R. , Tabita F. R. . ( 2006;). Identification of the DNA bases of a DNase I footprint by the use of dye primer sequencing on an automated capillary DNA analysis instrument. J Biomol Tech 17: 103–113 [PubMed].
    [Google Scholar]
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