Hypochlorous acid and hydrogen peroxide-induced negative regulation of Salmonella enterica serovar Typhimurium ompW by the response regulator ArcA

BMC Microbiology

Volumn 12, Issue , 2012, Pages

  Morales, Eduardo H ^a   Calderán, Iván L ^a   Collao, Bernardo ^a   Gil, Fernando ^a   Porwollik, Steffen ^b   McClelland, Michael ^b,c   Saavedra, Claudia P ^a  

^a UNIVERSIDAD ANDRÉS BELLO   (Chile)

^b Vaccine Research Institute of San Diego   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROGEN PEROXIDE; HYPOCHLOROUS ACID; PROTEOLIPOSOME; OUTER MEMBRANE PROTEIN;

ARCA GENE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BINDING SITE; BIOINFORMATICS; CONCENTRATION (PARAMETERS); EXPOSURE; GEL MOBILITY SHIFT ASSAY; NONHUMAN; OUTER MEMBRANE; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALMONELLA TYPHIMURIUM; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OXIDATIVE STRESS; REGULATOR GENE;

ARCA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

BACTERIAL OUTER MEMBRANE PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REGULATOR; HYDROGEN PEROXIDE; HYPOCHLOROUS ACID; OXIDATIVE STRESS; PROMOTER REGIONS, GENETIC; SALMONELLA TYPHIMURIUM;

EID: 84861362033     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-12-63     Document Type: Article

References (51)

1. Fridovich I, The biology of oxygen radicals. Science 1978 201 875 880
2. Bacterial adaptation to oxidative stress: implications for pathogenesis and interaction with phagocytic cells. Hassett D, Cohen M, FASEB J 1989 3 2574 2582 2556311 (Pubitemid 20013271)
3. Identification of sodC encoding periplasmic [CuZn]-superoxide dismutase in Salmonella. Canvin J, Langford PR, Wilks KE, Kroll JS, FEMS Microbiol Lett 1996 136 215 220 10.1111/j.1574-6968.1996.tb08052.x 8869506 (Pubitemid 26080366)
4. Oxidative stress. Storz G, Imlay JA, Curr Opin Microbiol 1999 2 188 194 10.1016/S1369-5274(99)80033-2 10322176 (Pubitemid 29176944)
5. Myeloperoxidase: Hydrogen Peroxide, Chloride Antimicrobial System: Nitrogen-Chlorine Derivatives of Bacterial Components in Bactericidal Action Against Escherichia coli. Thomas E, Infect Immun 1979 23 522 531 217834 (Pubitemid 9116220)
6. Human Neutrophils Use the Myeloperoxidase-Hydrogen Peroxide-Chloride System to Chlorinate but Not Nitrate Bacterial Proteins during Phagocytosis. Rosen H, Crowley J, Heinecke J, J Biol Chem 2002 277 30463 30468 10.1074/jbc.M202331200 12060654 (Pubitemid 34970737)
7. Inside the Neutrophil Phagosome: Oxidants, Myeloperoxidase and Bacterial Killing. Hampton M, Kettle A, Winterbourn C, Blood 1998 92 3007 3017 9787133 (Pubitemid 28492304)
8. Pathways of Oxidative Damage. Imlay J, Annu Rev Microbiol 2003 57 395 418 10.1146/annurev.micro.57.030502.090938 14527285 (Pubitemid 37392949)
9. Hydrogen peroxide fluxes and compartmentalization inside growingEscherichia coli. Seaver LC, Imlay JA, J Bacteriol 2001 183 7182 7189 10.1128/JB.183.24.7182-7189.2001 11717277 (Pubitemid 33121852)
10. Decreased cellular permeability to H2O2protectsSaccharomyces cerevisiaecells in stationary phase against oxidative stress. Sousa-Lopes A, Antunes F, Cyrne L, Marinho HS, FEBS Lett 2004 578 152 156 10.1016/j.febslet. 2004.10.090 15581633 (Pubitemid 39576117)
11. Acid Adaptation SensitizesSalmonellaTyphimurium to Hypochlorous Acid. Leyer G, Johnson E, Appl Environ Microbiol 1997 63 461 467 9023924
12. Response regulator ArcA ofSalmonella entericaserovar Typhimurium downregulates the expression of OmpD, a porin facilitating uptake of hydrogen peroxide. Calderán IL, Morales E, Caro NJ, Chahuán CA, Collao B, Gil F, Villareal JM, Ipinza F, Mora GC, Saavedra CP, Res Microbiol 2011 162 214 222 10.1016/j.resmic.2010.11.001 21144897
13. Multidrug efflux pumps of gram-negative bacteria. Nikaido H, J Bacteriol 1996 178 5853 5859 8830678 (Pubitemid 26337766)
14. -barrel membrane proteins. Shulz GE, Curr Opin Struct Biol 2000 10 443 447 10.1016/S0959-440X(00)00120-2 10981633 (Pubitemid 30496799)
15. Klebba P, The Porinologist. J. Bacteriol. 2005 187 8232 8236
16. Expression, crystallization and preliminary X-ray crystallographic studies of the outer membrane protein OmpW fromEscherichia coli. Albrecht R, Zeth K, Soding J, Lupas A, Linke D, Acta Cryst. 2006 62 415 418
17. The outer membrane protein OmpW forms an eight-stranded beta-barrel with a hydrophobic channel. Hong H, Patel DR, Tamm LK, Van den Berg B, J Biol Chem 2006 281 7568 7577 10.1074/jbc.M512365200 16414958 (Pubitemid 43847527)
18. Nucleotide sequence of the geneompW, encoding a 22kDa immunogenic outer membrane protein ofVibrio cholerae. Jalajakumari MB, Manning PA, Nucleic Acids Res 1990 18 2180 10.1093/nar/18.8.2180 2336399 (Pubitemid 20171556)
19. Structural features, properties and regulation of the outer-membrane protein W (OmpW) ofVibrio cholerae. Bisweswar N, Nandy RK, Sarkar A, Ghose AC, Microbiology 2005 151 2975 2986 10.1099/mic.0.27995-0 16151208 (Pubitemid 41309568)
20. The ompW (porin) gene mediates methyl viologen (paraquat) efflux in Salmonella enterica serovar Typhimurium. Gil F, Ipinza P, Fuentes J, Fumeron R, Villareal JM, Aspée A, Mora GC, Vásquez CC, Saavedra C, Res Microbiol 2007 158 529 536 10.1016/j.resmic.2007.05.004 17618087 (Pubitemid 47187665)
21. Transcriptomic Responses ofSalmonella entericSerovars Enteritidis and Typhimurium to Chlorine-Based Oxidative Stress. Wang S, Phillippy A, Deng K, Rui X, Li Z, Tortorello ML, Zhang W, Appl Environ Microbiol 2010 76 5013 5024 10.1128/AEM.00823-10 20562293
22. Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins inSalmonella typhimurium. Christman MF, Morgan RW, Jacobson FS, Ames BN, Cell 1985 41 753 762 10.1016/S0092-8674(85)80056-8 2988786 (Pubitemid 15243382)
23. Positive control of a global antioxidant defense regulon activated by superoxide-generating agents inEscherichia coli. Greenberg JT, Monach P, Chou JH, Josephy PD, Demple B, Proc Natl Acad Sci 1990 87 6181 6185 10.1073/pnas.87.16.6181 1696718 (Pubitemid 20258980)
24. The global regulator ArcA controls resistance to reactive nitrogen and oxygen intermediates inSalmonella entericaserovar Enteritidis. Lu S, Killoran PB, Fang FC, Riley LW, Infect Immun 2002 70 451 461 10.1128/IAI.70.2.451-461. 2002 11796570 (Pubitemid 34083801)
25. The ArcA regulon and oxidative stress resistance inHaemophilus influenzae. Wong SM, Alugupalli KR, Ram S, Akerley BJ, Mol Microbiol 2007 64 1375 1390 10.1111/j.1365-2958.2007.05747.x 17542927 (Pubitemid 46849025)
26. Role of the ArcAB two-component system in the resistance ofEscherichia colito reactive oxygen stress. Loui C, Chang AC, Lu S, BMC Microbiol 2009 9 183 10.1186/1471-2180-9-183 19715602
27. Analysis of the ArcA regulon in anaerobically grown Salmonella enterica sv. Evans MR, Fink RC, Vazquez-Torres A, Porwollik S, Jones-Carson J, McClelland M, Hassan HM, Typhimurium. BMC Microbiol 2011 21 11 58
28. ThearcBgene ofEscherichia coliencodes a sensor-regulator protein for anaerobic repression of the arc modulon. Iuchi S, Matsuda Z, Fujiwara T, Lin EC, Mol Microbiol 1990 4 715 727 10.1111/j.1365-2958.1990.tb00642.x 2201868 (Pubitemid 20180863)
29. Identification of a quinone-sensitive redox switch in the ArcB sensor kinase. Malpica R, Franco B, Rodriguez C, Kwon O, Georgellis D, Proc Natl Acad Sci 2004 101 13318 13323 10.1073/pnas.0403064101 15326287 (Pubitemid 39209663)
30. The ArcB Sensor Kinase ofEscherichia coliAutophosphorylates by an Intramolecular Reaction. Pẽa-Sandoval G, Georgellis D, J Bacteriol 2010 192 1735 1739 10.1128/JB.01401-09 20097862
31. Purification and phosphorylation of the Arc regulatory components ofEscherichiacoli. Iuchi S, Lin EC, J Bacteriol 1992 174 5617 5623 1512197
32. In vitro phosphorylation study of the arc two-component signal transduction system ofEscherichia coli. Georgellis D, Lynch AS, Lin EC, J Bacteriol 1997 179 5429 5435 9286997 (Pubitemid 27387612)
33. Phosphorelay as the Sole Physiological Route of Signal Transmission by the Arc Two-Component system ofEscherichia coli. Kwon O, Georgellis D, Lin EC, J Bacteriol 2000 182 3858 3862 10.1128/JB.182.13.3858-3862.2000 10851007 (Pubitemid 30413043)
34. Transcriptional control mediated by the ArcA two-component response regulator protein ofEscherichia coli: characterization of DNA binding at target promoters. Lynch AS, Lin EC, J Bacteriol 1996 178 6238 6249 8892825 (Pubitemid 26365705)
35. Multimerization of Phosphorylated and Non-phosphorylated ArcA is Necessary for the Response Regulator Function of the Arc Two-Component Signal Transduction System. Jeon Y, Lee Y, Han J, Kim J, Hwang D, J Biol Chem 2001 276 40873 40879 10.1074/jbc.M104855200 11527965
36. Quinones as the Redox Signal for the Arc Two-Component System of Bacteria. Georgellis D, Kwon O, Lin EC, Science 2001 292 2314 2316 10.1126/science.1059361 11423658 (Pubitemid 32568050)
37. Requirement of ArcA for Redox Regulation inEscherichia coliunder Microaerobic but Not Anaerobic or Aerobic Conditions. Alexeeva S, Hellingwerf K, Mattos JT, J Bacteriol 2003 185 204 209 10.1128/JB.185.1.204-209.2003 12486057 (Pubitemid 36008838)
38. The ArcBA Two-Component System ofEscherichia coliIs Regulated by the Redox State of both the Ubiquinone and the Menaquinone Pool. Bekker M, Alexeeva S, Laan W, Sawers G, Mattos JT, Hellingwerf K, J Bacteriol 2010 191 746 754
39. Shahzad Asif HM, SysMO-SUMO, Sanguinetti G, Teixeira de Mattos J, Poole RK, Green J: Transcript Profiling and Inference ofEscherichia coliK-12 ArcA Activity across the Range of Physiologically Relevant Oxygen Concentrations. Rolfe MD, Ter Beek A, Graham AI, Trotter EW, J Biol Chem 2011 286 10147 10154 10.1074/jbc.M110.211144 21252224
40. Role of porins in sensitivity of Escherichia coli to antibacterial activity of the lactoperoxidase enzyme system. De Spiegeleer P, Sermon J, Vanoirbeek K, Aertsen A, Michiels CW, Appl Environ Microbiol 2005 71 3512 3518 10.1128/AEM.71.7.3512-3518.2005 16000755 (Pubitemid 40980514)
41. Virtual Footprint and PRODORIC: an integrative framework for regulon prediction in prokaryotes. Münch R, Hiller K, Grote A, Scheer M, Klein J, Schobert M, Jahn D, Bioinformatics 2005 21 4187 4189 10.1093/bioinformatics/ bti635 16109747 (Pubitemid 41672111)
42. SoxS regulates the expression of theSalmonella entericaserovar TyphimuriumompWgene. Gil F, Hernández-Lucas I, Polanco R, Pacheco N, Collao B, Villareal JM, Nardocci G, Calva E, Saavedra CP, Microbiology 2009 155 2490 2497 10.1099/mic.0.027433-0 19460824
43. Tuning of the porin expression under anaerobic growth conditions by his-to-Asp cross-phosphorelay through both the EnvZ-osmosensor and ArcB-anaerosensor inEscherichia coli. Matsubara M, Kitaoka SI, Takeda SI, Mizuno T, Genes Cells 2000 5 555 569 10.1046/j.1365-2443.2000.00347.x 10947842 (Pubitemid 30602698)
44. Hypochlorous Acid Activates the Heat Shock and soxRS Systems ofEscherichia coli. Dukan S, Dadon S, Smulski DR, Belkin S, Appl Environ Microbiol 1996 62 4003 4008 8899987 (Pubitemid 26371496)
45. A dual-signaling mechanism mediated by the ArcB hybrid sensor kinase containing the histidine-containing phosphotransfer domain inEscherichia coli. Matsushika A, Mizuno T, J Bacteriol 1998 180 3973 3977 9683496 (Pubitemid 28361595)
46. One-step inactivation of chromosomal genes inEscherichia coliK-12 using PCR products. Datsenko KA, Wanner BL, Proc Natl Acad Sci 2000 97 6640 6645 10.1073/pnas.120163297 10829079 (Pubitemid 30412767)
47. A new mathematical model for relative quantification in real-time RT-PCR. Pfaffl MW, Nucleic Acids Res 2001 29 45 10.1093/nar/29.9.e45 11328886
48. A btwo-component phosphotransfer network involving ArcB, ArcA, and RssB coordinates synthesis and proteolysis of S (RpoS) in E. coli. Mika F, Hengge R, Genes Dev 2005 19 2770 2781 10.1101/gad.353705 16291649 (Pubitemid 41627942)
49. Lipoic Acid Protects Efficiently Only against a Specific Form of Peroxynitrite-induced Damage. Rezk BM, Haenen G, van der Vijgh W, Bast A, J Biol Chem 2004 279 9693 9697 14701855 (Pubitemid 38372566)
50. Porin channels in Escherichia coli: studies with liposomes reconstituted from purified proteins. Nikaido H, Rosenberg EY, J Bacteriol 1983 153 241 252 6294049 (Pubitemid 13119861)
51. Kinetics of peroxidation of linoleic acid incorporated into DPPC vesicles initiated by the thermal decomposition of 2,2'-azobis(2-amidinopropane) dihydrochloride. Cubillos MA, Lissi EA, Abuin EB, Chem Phys Lipids 2001 112 41 46 10.1016/S0009-3084(01)00161-X 11518571 (Pubitemid 32772780)