SoxS regulates the expression of the serovar Typhimurium gene Free

Abstract

OmpW of serovar Typhimurium has been described as a minor porin involved in osmoregulation, and is also affected by environmental conditions. Biochemical and genetic evidence from our laboratory indicates that OmpW is involved in efflux of and resistance towards paraquat (PQ), and its expression has been shown to be activated in response to oxidative stress. In this study we have explored expression in response to PQ. Primer extension and transcriptional fusions showed that its expression was induced in the presence of PQ. analyses suggested a putative binding site for the SoxS transcriptional factor at the regulatory region. Electrophoretic mobility shift assays (EMSAs) and footprinting experiments showed that SoxS binds at a region that starts close to −54 and ends at about −197 upstream of the transcription start site. Transcriptional fusions support the relevance of this region in activation. The SoxS site is in the forward orientation and its location suggests that the gene has a class I SoxS-dependent promoter.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.027433-0
2009-08-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/8/2490.html?itemId=/content/journal/micro/10.1099/mic.0.027433-0&mimeType=html&fmt=ahah

References

  1. Aono R., Tsukagoshi N., Yamamoto M. 1998; Involvement of outer membrane protein TolC, a possible member of the mar- sox regulon, in maintenance and improvement of organic solvent tolerance of Escherichia coli K-12. J Bacteriol 180:938–944
    [Google Scholar]
  2. Barbosa T. M., Levy S. B. 2000; Differential expression of over 60 chromosomal genes in Escherichia coli by constitutive expression of MarA. J Bacteriol 182:3467–3474
    [Google Scholar]
  3. Benz R., Bauer K. 1988; Permeation of hydrophilic molecules through the outer membrane of Gram-negative bacteria. Eur J Biochem 176:1–9
    [Google Scholar]
  4. Chatfield S. N., Dorman C. J., Hayward C., Dougan G. 1991; Role of ompR-dependent genes in Salmonella typhimurium virulence: mutants deficient in both ompC and ompF are attenuated in vivo. Infect Immun 59:449–452
    [Google Scholar]
  5. Cohen S. P., McMurry L. M., Levy S. B. 1988; marA locus causes decreased expression of OmpF porin in multiple-antibiotic resistant (Mar) mutants of Escherichia coli . J Bacteriol 170:5416–5422
    [Google Scholar]
  6. Datsenko K. A., Wanner B. L. 2000; One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640–6645
    [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
    [Google Scholar]
  8. Delihas N., Forst S. 2001; MicF: an antisense RNA gene involved in response of Escherichia coli to global stress factor. J Mol Biol 313:1–12
    [Google Scholar]
  9. Dupont M., James C. E., Chevalier J., Pagès J. M. 2007; An early response to environmental stress involves regulation of OmpX and OmpF, two enterobacterial outer membrane pore-forming proteins. Antimicrob Agents Chemother 51:3190–3198
    [Google Scholar]
  10. Fawcett W. P., Wolf R. E. Jr 1994; Purification of a MalE–SoxS fusion protein and identification of the control sites of Escherichia coli superoxide-inducible genes. Mol Microbiol 14:669–679
    [Google Scholar]
  11. Fawcett W. P., Wolf R. E. Jr 1995; Genetic definition of the Escherichia coli zwf ‘soxbox’, the DNA binding site for SoxS-mediated induction of glucose 6-phosphate dehydrogenase in response to superoxides. J Bacteriol 177:1742–1750
    [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
    [Google Scholar]
  13. Giró M., Carrillo N., Krapp A. 2006; Glucose-6-phosphate dehydrogenase and ferredoxin-NADP(H) reductase contribute to damage repair during the soxRS response of Escherichia coli . Microbiology 152:1119–1128
    [Google Scholar]
  14. Greenberg J. T., Monach P. A., Chou J. H., Josephy P. D., 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
    [Google Scholar]
  15. Griffith K. L., Wolf R. E. Jr 2001; Systematic mutagenesis of the DNA binding sites for SoxS in the Escherichia coli zwf and fpr promoters: identifying nucleotides required for DNA binding and transcription activation. Mol Microbiol 40:1141–1154
    [Google Scholar]
  16. Groisman E. A., Ochman H. 1994; How to become a pathogen. Trends Microbiol 2:289–294
    [Google Scholar]
  17. Hassan H. M., Fridovich I. 1979; Paraquat and Escherichia coli . J Biol Chem 254:10846–10852
    [Google Scholar]
  18. Hernández-Lucas I., Gallego-Hernández A. L., Encarnación S., Fernández-Mora M., Martínez-Batallar A. G., Salgado H., Oropeza R., Calva E. 2008; The LysR-type transcriptional regulator LeuO controls the expression of several genes in Salmonella enterica serovar Typhi. J Bacteriol 190:1658–1670
    [Google Scholar]
  19. Ho E. M., Chang H. W., Kim S. I., Kahng H. Y., Oh K. H. 2004; Analysis of TNT (2,4,6-trinitrotoluene)-inducible cellular responses and stress shock proteome in Stenotrophomonas sp. OK-5. Curr Microbiol 49:346–352
    [Google Scholar]
  20. Imlay J. A. 2008; Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77:755–776
    [Google Scholar]
  21. Jeanteur D., Lakey J. H., Pattus F. 1991; The bacterial porin superfamily: sequence alignment and structure prediction. Mol Microbiol 5:2153–2164
    [Google Scholar]
  22. Klebba P. E. 2002; Mechanism of maltodextrin transport through LamB. Res Microbiol 153:417–424
    [Google Scholar]
  23. Koebnik R., Locher K. P., Van Gelder P. 2000; Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37:239–253
    [Google Scholar]
  24. Li Z., Demple B. 1994; SoxS, an activator of superoxide stress genes in Escherichia coli . J Biol Chem 269:18371–18377
    [Google Scholar]
  25. Li Z., Demple B. 1996; Sequence specificity for DNA binding by Escherichia coli SoxS and Rob proteins. Mol Microbiol 20:937–945
    [Google Scholar]
  26. Martin R. G., Gillette W. K., Rhee S., Rosner J. L. 1999; Structural requirements for marbox function in transcriptional activation of mar/sox/rob regulon promoters in Escherichia coli: sequence, orientation and spatial relationship to the core promoter. Mol Microbiol 34:431–441
    [Google Scholar]
  27. Martin R. G., Gillette W. K., Rosner J. L. 2000; Promoter discrimination by the related transcriptional activators MarA and SoxS: differential regulation by differential binding. Mol Microbiol 35:623–634
    [Google Scholar]
  28. Meyer P. N., Wilmes-Riesenberg M. R., Stathopoulos C., Curtiss R. III 1998; Virulence of a Salmonella typhimurium OmpD mutant. Infect Immun 66:387–390
    [Google Scholar]
  29. Morimyo M. 1988; Isolation and characterization of methyl viologen-sensitive mutants of Escherichia coli K-12. J Bacteriol 170:2136–2142
    [Google Scholar]
  30. Nandi B., Nandy R. K., Sarkar A., Ghose A. C. 2005; Structural features, properties and regulation of the outer-membrane protein W (OmpW) of Vibrio cholerae . Microbiology 151:2975–2986
    [Google Scholar]
  31. Nikaido H. 1996; Multidrug efflux pumps of Gram-negative bacteria. J Bacteriol 178:5853–5859
    [Google Scholar]
  32. Paterson E. S., Boucher S. E., Lambert I. B. 2002; Regulation of the nfsA gene in Escherichia coli by SoxS. J Bacteriol 184:51–58
    [Google Scholar]
  33. Pomposiello P. J., Demple B. 2000; Identification of SoxS-regulated genes in Salmonella enterica serovar Typhimurium. J Bacteriol 182:23–29
    [Google Scholar]
  34. Pomposiello P. J., Bennik M. H. J., Demple B. 2001; Genome-wide transcriptional profiling of the Escherichia coli responses to superoxide stress and sodium salicylate. J Bacteriol 183:3890–3902
    [Google Scholar]
  35. Pomposiello P. J., Koutsolioutsou A., Carrasco D., Demple B. 2003; SoxRS-regulated expression and genetic analysis of the yggX gene of Escherichia coli . J Bacteriol 185:6624–6632
    [Google Scholar]
  36. Rodríguez-Morales O., Fernández-Mora M., Hernández-Lucas I., Vázquez A., Puente J. L., Calva E. 2006; Salmonella enterica serovar Typhimurium ompS1 and ompS2 mutants are attenuated for virulence in mice. Infect Immun 74:1398–1402
    [Google Scholar]
  37. Scandalios J. G. 2002; Oxidative stress responses – what have genome-scale studies taught us?. Genome Biol 3: REVIEWS1019
    [Google Scholar]
  38. Storz G., Imlay J. A. 1999; Oxidative stress. Curr Opin Microbiol 2:188–194
    [Google Scholar]
  39. van der Straaten T., Zulianello L., van Diepen A., Granger D. L., Janssen R., van Dissel J. T. 2004; Salmonella enterica serovar Typhimurium RamA, intracellular oxidative stress response, and bacterial virulence. Infect Immun 72:996–1003
    [Google Scholar]
  40. Weiss M. S., Abele U., Weckesser J., Welte W., Schiltz E., Schulz G. E. 1991; Molecular architecture and electrostatic properties of a bacterial porin. Science 254:1627–1630
    [Google Scholar]
  41. Xu C., Wang S., Ren H., Lin X., Wu L. 2005; Protein analysis on the expression of outer membrane proteins of Vibrio alginolyticus at different sodium concentrations. Proteomics 5:3142–3152
    [Google Scholar]
  42. Yankovskaya V., Horsefield R., Törnroth S., Luna-Chavez C., Myoshi H., Léger C., Byrne B., Cecchini G., Iwata S. 2003; Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 299:700–704
    [Google Scholar]
  43. Zgurskaya H. I., Nikaido H. 2000; Multidrug resistance mechanism: drug efflux across two membranes. Mol Microbiol 37:219–225
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.027433-0
Loading
/content/journal/micro/10.1099/mic.0.027433-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed