OmpW is cooperatively upregulated by mara and SoxS in response to menadione

Microbiology (United Kingdom)

Volumn 159, Issue 4, 2013, Pages 715-725

  Collao, B ^a   Morales, E H ^a   Gil, F ^a   Calderon I L ^a   Saavedra, C P ^a  

^a UNIVERSIDAD ANDRÉS BELLO   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

ARAC PROTEIN; BACTERIAL PROTEIN; MARA PROTEIN; MENADIONE; OMPW PROTEIN; ROB PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; GENE FUSION; GENETIC TRANSCRIPTION; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SALMONELLA ENTERICA; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; UPREGULATION; WILD TYPE;

BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; PROMOTER REGIONS, GENETIC; SALMONELLA TYPHIMURIUM; TRANS-ACTIVATORS; UP-REGULATION; VITAMIN K 3;

SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 84875750599     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.066050-0     Document Type: Article

References (55)

1. 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.
2. Chollet, R., Bollet, C., Chevalier, J., Malléa, M., Pagès, J.-M. & Davin-Regli, A. (2002). mar Operon involved in multidrug resistance of Enterobacter aerogenes. Antimicrob Agents Chemother 46, 1093-1097.
3. Chollet, R., Chevalier, J., Bollet, C., Pages, J.-M. & Davin-Regli, A. (2004). RamA is an alternate activator of the multidrug resistance cascade in Enterobacter aerogenes. Antimicrob Agents Chemother 48, 2518-2523.
4. Collao, B., Morales, E.H., Gil, F., Polanco, R., Calderón, I. L. & Saavedra, C. P. (2012). Differential expression of the transcription factors MarA, Rob, and SoxS of Salmonella Typhimurium in response to sodium hypochlorite: down-regulation of rob by MarA and SoxS. Arch Microbiol 194, 933-942.
5. De la Cruz, M. A., Fernández-Mora, M., Guadarrama, C., Flores-sValdez, 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.
6. Ebel-Tsipis, J., Fox, M. S. & Botstein, D. (1972). Generalized transduction by bacteriophage P22 in Salmonella typhimurium. II. Mechanism of integration of transducing DNA. J Mol Biol 71, 449- 469.
7. Fujikawa, M., Kobayashi, K. & Kozawa, T. (2012). Direct oxidation of the [2Fe-2S] cluster in SoxR protein by superoxide: distinct differential sensitivity to superoxide-mediated signal transduction. J Biol Chem 287, 35702-35708.
8. 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.
9. 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.
10. Giró, M., Carrillo, N. & Krapp, A. R. (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.
11. 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.
12. Groisman, E. A. & Ochman, H. (1994). How to become a pathogen. Trends Microbiol 2, 289-294.
13. Gu, M. & Imlay, J. A. (2011). The SoxRS response of Escherichia coli is directly activated by redox-cycling drugs rather than by superoxide. Mol Microbiol 79, 1136-1150.
14. Hassan, H. M. & Fridovich, I. (1979). Paraquat and Escherichia coli. Mechanism of production of extracellular superoxide radical. J Biol Chem 254, 10846-10852.
15. Hong, H., Patel, D. R., Tamm, L. K. & van den Berg, B. (2006). The outer membrane protein OmpW forms an eight-stranded β-barrel with a hydrophobic channel. J Biol Chem 281, 7568-7577.
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. Imlay, J. A. (2008). Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77, 755-776.
18. Jair, K. W., Martin, R. G., Rosner, J. L., Fujita, N., Ishihama, A. & Wolf, R. E., Jr (1995). Purification and regulatory properties of MarA protein, a transcriptional activator of Escherichia coli multiple antibiotic and superoxide resistance promoters. J Bacteriol 177, 7100-7104.
19. Jair, K. W., Yu, X., Skarstad, K., Thöny, B., Fujita, N., Ishihama, A. & Wolf, R. E., Jr (1996). Transcriptional activation of promoters of the superoxide and multiple antibiotic resistance regulons by Rob, a binding protein of the Escherichia coli origin of chromosomal replication. J Bacteriol 178, 2507-2513.
20. Jalajakumari, M. B. & Manning, P. A. (1990). Nucleotide sequence of the gene, ompW, encoding a 22kDa immunogenic outer membrane protein of Vibrio cholerae. Nucleic Acids Res 18, 2180.
21. Jeanteur, D., Lakey, J. H. & Pattus, F. (1991). The bacterial porin superfamily: sequence alignment and structure prediction. Mol Microbiol 5, 2153-2164.
22. Johnston, J. W., Shamsulddin, H., Miller, A.-F. & Apicella, M. A. (2010). Sialic acid transport and catabolism are cooperatively regulated by SiaR and CRP in nontypeable Haemophilus influenza. BMC Microbiol 10, 240.
23. Kato, T., Watanabe, M. & Ohta, T. (1994). Induction of the SOS response and mutations by reactive oxygen-generating compounds in various Escherichia coli mutants defective in the mutM, mutY or soxRS loci. Mutagenesis 9, 245-251.
24. Kim, B. S., Hwang, J., Kim, M. H. & Choi, S. H. (2011). Cooperative regulation of the Vibrio vulnificus nan gene cluster by NanR protein, cAMP receptor protein, and N-acetylmannosamine 6-phosphate. J Biol Chem 286, 40889-40899.
25. 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.
26. Krapp, A. R., Humbert, M. V. & Carrillo, N. (2011). The soxRS response of Escherichia coli can be induced in the absence of oxidative stress and oxygen by modulation of NADPH content. Microbiology 157, 957-965.
27. Kwon, H. J., Bennik, M. H., Demple, B. & Ellenberger, T. (2000). Crystal structure of the Escherichia coli Rob transcription factor in complex with DNA. Nat Struct Biol 7, 424-430.
28. Lee, P. E., Demple, B. & Barton, J. K. (2009). DNA-mediated redox signaling for transcriptional activation of SoxR. Proc Natl Acad Sci U S A 106, 13164-13168.
29. Li, Z. & Demple, B. (1994). SoxS, an activator of superoxide stress genes in Escherichia coli. Purification and interaction with DNA. J Biol Chem 269, 18371-18377.
30. Li, Z. & Demple, B. (1996). Sequence specificity for DNA binding by Escherichia coli SoxS and Rob proteins. Mol Microbiol 20, 937-945.
31. Martin, R. G. & Rosner, J. L. (2002). Genomics of the marA/soxS/rob regulon of Escherichia coli: identification of directly activated promoters by application of molecular genetics and informatics to microarray data. Mol Microbiol 44, 1611-1624.
32. 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.
33. 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.
34. 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.
35. McMurry, L. M. & Levy, S. B. (2010). Evidence that regulatory protein MarA of Escherichia coli represses rob by steric hindrance. J Bacteriol 192, 3977-3982.
36. Michán, C., Manchado, M. & Pueyo, C. (2002). SoxRS downregulation of rob transcription. J Bacteriol 184, 4733-4738.
37. Morales, E.H., Calderón, I. L., Collao, B., Gil, F., Porwollik, S., McClelland, M. & Saavedra, C. P. (2012). Hypochlorous acid and hydrogen peroxide-induced negative regulation of Salmonella enterica serovar Typhimurium ompW by the response regulator ArcA. BMC Microbiol 12, 63.
38. Morimyo, M. (1988). Isolation and characterization of methyl viologensensitive mutants of Escherichia coli K-12. J Bacteriol 170, 2136-2142.
39. 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.
40. Nikaido, H. (1996). Multidrug efflux pumps of Gram-negative bacteria. J Bacteriol 178, 5853-5859.
41. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29, e45.
42. 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.
43. 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.
44. Scandalios, J. G. (2002). Oxidative stress responses-what have genome-scale studies taught us? Genome Biol 3, REVIEWS1019.
45. Selke, M., Meens, J., Springer, S., Frank, R. & Gerlach, G. F. (2007). Immunization of pigs to prevent disease in humans: construction and protective efficacy of a Salmonella enterica serovar Typhimurium live negative-marker vaccine. Infect Immun 75, 2476-2483.
46. Semchyshyn, H., Bagnyukova, T., Storey, K. & Lushchak, 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 29, 898-902.
47. Son, B., Liu, Y. & Kroos, L. (2011). Combinatorial regulation by MrpC2 and FruA involves three sites in the fmgE promoter region during Myxococcus xanthus development. J Bacteriol 193, 2756-2766.
48. Storz, G. & Imlay, J. A. (1999). Oxidative stress. Curr Opin Microbiol 2, 188-194.
49. Tobes, R. & Ramos, J. L. (2002). AraC-XylS database: a family of positive transcriptional regulators in bacteria. Nucleic Acids Res 30, 318-321.
50. Vasil'Eva, S. V., Stupakova, M. V., Lobysheva, I. I., Mikoyan, V. D. & Vanin, A. F. (2001). Activation of the Escherichia coli SoxRS-regulon by nitric oxide and its physiological donors. Biochemistry (Mosc) 66, 984-988.
51. 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.
52. Wickstrum, J. R., Santangelo, T. J. & Egan, S. M. (2005). Cyclic AMP receptor protein and RhaR synergistically activate transcription from the L-rhamnose-responsive rhaSR promoter in Escherichia coli. J Bacteriol 187, 6708-6718.
53. Xu, C., Wang, S., Ren, H., Lin, X., Wu, L. & Peng, X. (2005). Proteomic analysis on the expression of outer membrane proteins of Vibrio alginolyticus at different sodium concentrations. Proteomics 5, 3142- 3152.
54. Zgurskaya, H. I. & Nikaido, H. (2000). Multidrug resistance mechanisms: drug efflux across two membranes. Mol Microbiol 37, 219-225.
55. Zhang, A., Rosner, J. L. & Martin, R. G. (2008). Transcriptional activation by MarA, SoxS and Rob of two tolC promoters using one binding site: a complex promoter configuration for tolC in Escherichia coli. Mol Microbiol 69, 1450-1455.