Salmonella enterica serovar Typhimurium BaeSR two-component system positively regulates sodA in response to ciprofloxacin

Microbiology (United Kingdom)

Volumn 159, Issue PART 10, 2013, Pages 2049-2057

  Guerrero, P ^a   Collao, B ^a   Alvarez R ^a   Salinas, H ^a   Morales, E H ^b,c   Calderon I L ^a   Saavedra, C P ^a   Gil, F ^a  

^a UNIVERSIDAD ANDRÉS BELLO   (Chile)

^b UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CIPROFLOXACIN; SODIUM CARBONATE; SUPEROXIDE DISMUTASE;

AMBER MUTANT; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; EFFUSION; FOWL TYPHOID; GEL MOBILITY SHIFT ASSAY; GENE PRODUCT; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PUMP; REPORTER GENE; RNA ISOLATION; SALMONELLA TYPHIMURIUM;

ANTI-BACTERIAL AGENTS; ARTIFICIAL GENE FUSION; BACTERIAL PROTEINS; CIPROFLOXACIN; DNA, BACTERIAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE KNOCKOUT TECHNIQUES; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN KINASES; SALMONELLA TYPHIMURIUM; SUPEROXIDE DISMUTASE; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

EID: 84884782526     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.066787-0     Document Type: Article

References (45)

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.
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.
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.
4. Beauchamp, C. & Fridovich, I. (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44, 276-287.
5. Cai, S. J. & Inouye, M. (2002). EnvZ-OmpR interaction and osmoregulation in Escherichia coli. J Biol Chem 277, 24155-24161.
6. Cambau, E. & Gutmann, L. (1993). Mechanisms of resistance to quinolones. Drugs 45 (Suppl. 3), 15-23.
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.
8. Drlica, K. & Zhao, X. (1997). DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol Mol Biol Rev 61, 377-392.
9. Durand, S. & Storz, G. (2010). Reprogramming of anaerobic metabolism by the FnrS small RNA. Mol Microbiol 75, 1215-1231.
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.
11. Figueroa-Bossi, N. & Bossi, L. (1999). Inducible prophages contribute to Salmonella virulence in mice. Mol Microbiol 33, 167-176.
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.
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.
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.
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.
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/OmpXlike protein, which are regulated by BaeR of a two-component system. Antimicrob Agents Chemother 49, 3955-3958.
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.
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.
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.
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.
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.
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.
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.
24. Liu, Y. & Imlay, J. A. (2013). Cell death from antibiotics without the involvement of reactive oxygen species. Science 339, 1210-1213.
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.
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.
27. Miller, J. H. (1972). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
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.
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.
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.
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.
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.
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.
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.
35. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29, 45e.
36. Piddock, L. J. (2002). Fluoroquinolone resistance in Salmonella serovars isolated from humans and food animals. FEMS Microbiol Rev 26, 3-16.
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.
38. Rosner, J. L. & Martin, R. G. (2013). Reduction of cellular stress by TolCdependent efflux pumps in Escherichia coli indicated by BaeSR and CpxARP activation of spy in efflux mutants. J Bacteriol 195, 1042-1050.
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.
40. Stock, A. M., Robinson, V. L. & Goudreau, P. N. (2000). Twocomponent signal transduction. Annu Rev Biochem 69, 183-215.
41. Touati, D. (1983). Cloning and mapping of the manganese superoxide dismutase gene (sodA) of Escherichia coli K-12. J Bacteriol 155, 1078-1087.
42. Walsh, C. (2000). Molecular mechanisms that confer antibacterial drug resistance. Nature 406, 775-781.
43. Wang, D. & Fierke, C. A. (2013). The BaeSR regulon is involved in defense against zinc toxicity in E. coli. Metallomics 5, 372-383.
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.
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.