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Volume 159, Issue Pt_10

serovar Typhimurium BaeSR two-component system positively regulates in response to ciprofloxacin Free

Abstract

In response to antibiotics, bacteria activate regulatory systems that control the expression of genes that participate in detoxifying these compounds, like multidrug efflux systems. We previously demonstrated that the BaeSR two-component system from serovar Typhimurium (. Typhimurium) participates in the detection of ciprofloxacin, a bactericidal antibiotic, and in the positive regulation of , an efflux pump implicated in antibiotic resistance. In the present work, we provide further evidence for a role of the . Typhimurium BaeSR two-component system in response to ciprofloxacin treatment and show that it regulates expression. We demonstrate that, in the absence of BaeSR, the transcript levels of and the activity of its gene product are lower. Using electrophoretic mobility shift assays and transcriptional fusions, we demonstrate that BaeR regulates by a direct interaction with the promoter region.

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2013-10-01
2024-04-19
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References

  1. Appia-Ayme C., Patrick E., Sullivan M. J., Alston M. J., Field S. J., AbuOun M., Anjum M. F., Rowley G. ( 2011). Novel inducers of the envelope stress response BaeSR in Salmonella Typhimurium: BaeR is critically required for tungstate waste disposal. PLoS ONE 6:e23713 [View Article][PubMed]
     [Google Scholar]
  2. Baranova N., Nikaido H. ( 2002). The baeSR two-component regulatory system activates transcription of the yegMNOB (mdtABCD) transporter gene cluster in Escherichia coli and increases its resistance to novobiocin and deoxycholate. J Bacteriol 184:4168–4176 [View Article][PubMed]
     [Google Scholar]
  3. Batchelor E., Goulian M. ( 2003). Robustness and the cycle of phosphorylation and dephosphorylation in a two-component regulatory system. Proc Natl Acad Sci U S A 100:691–696 [View Article][PubMed]
     [Google Scholar]
  4. Beauchamp C., Fridovich I. ( 1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287 [View Article][PubMed]
     [Google Scholar]
  5. Cai S. J., Inouye M. ( 2002). EnvZ-OmpR interaction and osmoregulation in Escherichia coli. . J Biol Chem 277:24155–24161 [View Article][PubMed]
     [Google Scholar]
  6. Cambau E., Gutmann L. ( 1993). Mechanisms of resistance to quinolones. Drugs 45:Suppl. 315–23 [View Article][PubMed]
     [Google Scholar]
  7. De la Cruz M. A., Fernández-Mora M., Guadarrama C., Flores-Valdez M. A., Bustamante V. H., Vázquez A., Calva E. ( 2007). LeuO antagonizes H-NS and StpA-dependent repression in Salmonella enterica ompS1. . Mol Microbiol 66:727–743 [View Article][PubMed]
     [Google Scholar]
  8. Drlica K., Zhao X. ( 1997). DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol Mol Biol Rev 61:377–392[PubMed]
     [Google Scholar]
  9. Durand S., Storz G. ( 2010). Reprogramming of anaerobic metabolism by the FnrS small RNA. Mol Microbiol 75:1215–1231 [View Article][PubMed]
     [Google Scholar]
  10. Fang F. C., DeGroote M. A., Foster J. W., Bäumler A. J., Ochsner U., Testerman T., Bearson S., Giárd J. C., Xu Y. & other authors ( 1999). Virulent Salmonella typhimurium has two periplasmic Cu, Zn-superoxide dismutases. Proc Natl Acad Sci U S A 96:7502–7507 [View Article][PubMed]
     [Google Scholar]
  11. Figueroa-Bossi N., Bossi L. ( 1999). Inducible prophages contribute to Salmonella virulence in mice. Mol Microbiol 33:167–176 [View Article][PubMed]
     [Google Scholar]
  12. Gil F., Ipinza F., Fuentes J., Fumeron R., Villarreal J. M., Aspée A., Mora G. C., Vásquez C. C., Saavedra C. ( 2007). The ompW (porin) gene mediates methyl viologen (paraquat) efflux in Salmonella enterica serovar Typhimurium. Res Microbiol 158:529–536 [View Article][PubMed]
     [Google Scholar]
  13. Gil F., Hernández-Lucas I., Polanco R., Pacheco N., Collao B., Villarreal J. M., Nardocci G., Calva E., Saavedra C. P. ( 2009). SoxS regulates the expression of the Salmonella enterica serovar Typhimurium ompW gene. Microbiology 155:2490–2497 [View Article][PubMed]
     [Google Scholar]
  14. Goswami M., Mangoli S. H., Jawali N. ( 2006). Involvement of reactive oxygen species in the action of ciprofloxacin against Escherichia coli. . Antimicrob Agents Chemother 50:949–954 [View Article][PubMed]
     [Google Scholar]
  15. Guerrero P., Collao B., Morales E. H., Calderón I. L., Ipinza F., Parra S., Saavedra C. P., Gil F. ( 2012). Characterization of the BaeSR two-component system from Salmonella Typhimurium and its role in ciprofloxacin-induced mdtA expression. Arch Microbiol 194:453–460 [View Article][PubMed]
     [Google Scholar]
  16. Hu W. S., Li P.-C., Cheng C.-Y. ( 2005). Correlation between ceftriaxone resistance of Salmonella enterica serovar Typhimurium and expression of outer membrane proteins OmpW and Ail/OmpX-like protein, which are regulated by BaeR of a two-component system. Antimicrob Agents Chemother 49:3955–3958 [View Article][PubMed]
     [Google Scholar]
  17. Jakubowski W., Biliński T., Bartosz G. ( 2000). Oxidative stress during aging of stationary cultures of the yeast Saccharomyces cerevisiae. . Free Radic Biol Med 28:659–664 [View Article][PubMed]
     [Google Scholar]
  18. Kaldalu N., Mei R., Lewis K. ( 2004). Killing by ampicillin and ofloxacin induces overlapping changes in Escherichia coli transcription profile. Antimicrob Agents Chemother 48:890–896 [View Article][PubMed]
     [Google Scholar]
  19. Keren I., Wu Y., Inocencio J., Mulcahy L. R., Lewis K. ( 2013). Killing by bactericidal antibiotics does not depend on reactive oxygen species. Science 339:1213–1216 [View Article][PubMed]
     [Google Scholar]
  20. Kohanski M. A., Dwyer D. J., Hayete B., Lawrence C. A., Collins J. J. ( 2007). A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130:797–810 [View Article][PubMed]
     [Google Scholar]
  21. Korshunov S. S., Imlay J. A. ( 2002). A potential role for periplasmic superoxide dismutase in blocking the penetration of external superoxide into the cytosol of Gram-negative bacteria. Mol Microbiol 43:95–106 [View Article][PubMed]
     [Google Scholar]
  22. Leblanc S. K., Oates C. W., Raivio T. L. ( 2011). Characterization of the induction and cellular role of the BaeSR two-component envelope stress response of Escherichia coli. . J Bacteriol 193:3367–3375 [View Article][PubMed]
     [Google Scholar]
  23. Lindner B., Wiese A., Brandenburg K., Seydel U., Dalhoff A. ( 2002). Lack of interaction of fluoroquinolones with lipopolysaccharides. Antimicrob Agents Chemother 46:1568–1570 [View Article][PubMed]
     [Google Scholar]
  24. Liu Y., Imlay J. A. ( 2013). Cell death from antibiotics without the involvement of reactive oxygen species. Science 339:1210–1213 [View Article][PubMed]
     [Google Scholar]
  25. Martin R. G., Bartlett E. S., Rosner J. L., Wall M. E. ( 2008). Activation of the Escherichia coli marA/soxS/rob regulon in response to transcriptional activator concentration. J Mol Biol 380:278–284 [View Article][PubMed]
     [Google Scholar]
  26. Massé E., Gottesman S. ( 2002). A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. . Proc Natl Acad Sci U S A 99:4620–4625 [View Article][PubMed]
     [Google Scholar]
  27. Miller J. H. ( 1972). Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
     [Google Scholar]
  28. Nagakubo S., Nishino K., Hirata T., Yamaguchi A. ( 2002). The putative response regulator BaeR stimulates multidrug resistance of Escherichia coli via a novel multidrug exporter system, MdtABC. J Bacteriol 184:4161–4167 [View Article][PubMed]
     [Google Scholar]
  29. Nagasawa S., Ishige K., Mizuno T. ( 1993). Novel members of the two-component signal transduction genes in Escherichia coli. . J Biochem 114:350–357[PubMed]
     [Google Scholar]
  30. Niederhoffer E. C., Naranjo C. M., Bradley K. L., Fee J. A. ( 1990). Control of Escherichia coli superoxide dismutase (sodA and sodB) genes by the ferric uptake regulation (fur) locus. J Bacteriol 172:1930–1938[PubMed]
     [Google Scholar]
  31. Nishino K., Honda T., Yamaguchi A. ( 2005). Genome-wide analyses of Escherichia coli gene expression responsive to the BaeSR two-component regulatory system. J Bacteriol 187:1763–1772 [View Article][PubMed]
     [Google Scholar]
  32. Nishino K., Nikaido E., Yamaguchi A. ( 2007). Regulation of multidrug efflux systems involved in multidrug and metal resistance of Salmonella enterica serovar Typhimurium. J Bacteriol 189:9066–9075 [View Article][PubMed]
     [Google Scholar]
  33. Pankey G. A., Sabath L. D. ( 2004). Clinical relevance of bacteriostatic versus bactericidal mechanisms of action in the treatment of Gram-positive bacterial infections. Clin Infect Dis 38:864–870 [View Article][PubMed]
     [Google Scholar]
  34. Partridge J. D., Bodenmiller D. M., Humphrys M. S., Spiro S. ( 2009). NsrR targets in the Escherichia coli genome: new insights into DNA sequence requirements for binding and a role for NsrR in the regulation of motility. Mol Microbiol 73:680–694 [View Article][PubMed]
     [Google Scholar]
  35. Pfaffl M. W. ( 2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:45e [View Article][PubMed]
     [Google Scholar]
  36. Piddock L. J. ( 2002). Fluoroquinolone resistance in Salmonella serovars isolated from humans and food animals. FEMS Microbiol Rev 26:3–16[PubMed] [CrossRef]
     [Google Scholar]
  37. 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 [View Article][PubMed]
     [Google Scholar]
  38. Rosner J. L., Martin R. G. ( 2013). Reduction of cellular stress by TolC-dependent efflux pumps in Escherichia coli indicated by BaeSR and CpxARP activation of spy in efflux mutants. J Bacteriol 195:1042–1050 [View Article][PubMed]
     [Google Scholar]
  39. Smirnova G., Samoilova Z., Muzyka N., Oktyabrsky O. ( 2012). Influence of plant polyphenols and medicinal plant extracts on antibiotic susceptibility of Escherichia coli. . J Appl Microbiol 113:192–199 [View Article][PubMed]
     [Google Scholar]
  40. Stock A. M., Robinson V. L., Goudreau P. N. ( 2000). Two-component signal transduction. Annu Rev Biochem 69:183–215 [View Article][PubMed]
     [Google Scholar]
  41. Touati D. ( 1983). Cloning and mapping of the manganese superoxide dismutase gene (sodA) of Escherichia coli K-12. J Bacteriol 155:1078–1087[PubMed]
     [Google Scholar]
  42. Walsh C. ( 2000). Molecular mechanisms that confer antibacterial drug resistance. Nature 406:775–781 [View Article][PubMed]
     [Google Scholar]
  43. Wang D., Fierke C. A. ( 2013). The BaeSR regulon is involved in defense against zinc toxicity in E. coli. . Metallomics 5:372–383 [View Article][PubMed]
     [Google Scholar]
  44. Yamamoto K., Ogasawara H., Ishihama A. ( 2008). Involvement of multiple transcription factors for metal-induced spy gene expression in Escherichia coli. . J Biotechnol 133:196–200 [View Article][PubMed]
     [Google Scholar]
  45. Yu P. ( 2007). Enhancing survival of Escherichia coli by increasing the periplasmic expression of Cu,Zn superoxide dismutase from Saccharomyces cerevisiae. . Appl Microbiol Biotechnol 76:867–871 [View Article][PubMed]
     [Google Scholar]
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Salmonellaenterica serovar Typhimurium BaeSR two-component system positively regulates sodA in response to ciprofloxacin
Microbiology 159, 2049 (2013); https://doi.org/10.1099/mic.0.066787-0
/content/journal/micro/10.1099/mic.0.066787-0
/content/journal/micro/10.1099/mic.0.066787-0
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