1887

Microbial Genomics logo

Volume 1, Issue 4

Genome-wide analysis of the response to nitric oxide in uropathogenic CFT073 Open Access

Abstract

Uropathogenic (UPEC) is the causative agent of urinary tract infections. Nitric oxide (NO) is a toxic water-soluble gas that is encountered by UPEC in the urinary tract. Therefore, UPEC probably requires mechanisms to detoxify NO in the host environment. Thus far, flavohaemoglobin (Hmp), an NO denitrosylase, is the only demonstrated NO detoxification system in UPEC. Here we show that, in strain CFT073, the NADH-dependent NO reductase flavorubredoxin (FlRd) also plays a major role in NO scavenging. We generated a mutant that lacks all known and candidate NO detoxification pathways (Hmp, FlRd and the respiratory nitrite reductase, NrfA). When grown and assayed anaerobically, this mutant expresses an NO-inducible NO scavenging activity, pointing to the existence of a novel detoxification mechanism. Expression of this activity is inducible by both NO and nitrate, and the enzyme is membrane-associated. Genome-wide transcriptional profiling of UPEC grown under anaerobic conditions in the presence of nitrate (as a source of NO) highlighted various aspects of the response of the pathogen to nitrate and NO. Several virulence-associated genes are upregulated, suggesting that host-derived NO is a potential regulator of UPEC virulence. Chromatin immunoprecipitation and sequencing was used to evaluate the NsrR regulon in CFT073. We identified 49 NsrR binding sites in promoter regions in the CFT073 genome, 29 of which were not previously identified in K-12. NsrR may regulate some CFT073 genes that do not have homologues in K-12.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): ChIP-seq , nitric oxide , NsrR , RNA-seq and uropathogenic E. coli
© 2015 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution Noncommercial License which permits any noncommercial use, distribution, and reproduction in any medium, provided the source is credited.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000031
2015-10-13
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/mgen/1/4/mgen000031.html?itemId=/content/journal/mgen/10.1099/mgen.0.000031&mimeType=html&fmt=ahah

References

  1. Alefounder P. R., Ferguson S. J. 1980; The location of dissimilatory nitrite reductase and the control of dissimilatory nitrate reductase by oxygen in Paracoccus denitrificans . Biochem J 192:231–240 [View Article][PubMed]
     [Google Scholar]
  2. Alteri C. J., Smith S. N., Mobley H. L. 2009; Fitness of Escherichia coli during urinary tract infection requires gluconeogenesis and the TCA cycle. PLoS Pathog 5:e1000448 [View Article][PubMed]
     [Google Scholar]
  3. Bailey T. L., Elkan C. 1994; Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2:28–36[PubMed]
     [Google Scholar]
  4. Bodenmiller D. M., Spiro S. 2006; The yjeB (nsrR) gene of Escherichia coli encodes a nitric oxide-sensitive transcriptional regulator. J Bacteriol 188:874–881 [View Article][PubMed]
     [Google Scholar]
  5. Bower J. M., Mulvey M. A. 2006; Polyamine-mediated resistance of uropathogenic Escherichia coli to nitrosative stress. J Bacteriol 188:928–933 [View Article][PubMed]
     [Google Scholar]
  6. Bower J. M., Gordon-Raagas H. B., Mulvey M. A. 2009; Conditioning of uropathogenic Escherichia coli for enhanced colonization of host. Infect Immun 77:2104–2112 [View Article][PubMed]
     [Google Scholar]
  7. Branchu P., Matrat S., Vareille M., Garrivier A., Durand A., Crépin S., Harel J., Jubelin G., Gobert A. P. 2014; NsrR, GadE, and GadX interplay in repressing expression of the Escherichia coli O157:H7 LEE pathogenicity island in response to nitric oxide. PLoS Pathog 10:e1003874 [View Article][PubMed]
     [Google Scholar]
  8. Bryan A., Roesch P., Davis L., Moritz R., Pellett S., Welch R. A. 2006; Regulation of type 1 fimbriae by unlinked FimB- and FimE-like recombinases in uropathogenic Escherichia coli strain CFT073. Infect Immun 74:1072–1083 [View Article][PubMed]
     [Google Scholar]
  9. Clarke T. A., Mills P. C., Poock S. R., Butt J. N., Cheesman M. R., Cole J. A., Hinton J. C., Hemmings A. M., Kemp G., other authors. 2008; Escherichia coli cytochrome c nitrite reductase NrfA. Methods Enzymol 437:63–77 [View Article][PubMed]
     [Google Scholar]
  10. Cole J. A. 2012; Legless pathogens: how bacterial physiology provides the key to understanding pathogenicity. Microbiology 158:1402–1413 [View Article][PubMed]
     [Google Scholar]
  11. Connell I., Agace W., Klemm P., Schembri M., Mărild S., Svanborg C. 1996; Type 1 fimbrial expression enhances Escherichia coli virulence for the urinary tract. Proc Natl Acad Sci U S A 93:9827–9832 [View Article][PubMed]
     [Google Scholar]
  12. Constantinidou C., Hobman J. L., Griffiths L., Patel M. D., Penn C. W., Cole J. A., Overton T. W. 2006; A reassessment of the FNR regulon and transcriptomic analysis of the effects of nitrate, nitrite, NarXL, and NarQP as Escherichia coli K12 adapts from aerobic to anaerobic growth. J Biol Chem 281:4802–4815 [View Article][PubMed]
     [Google Scholar]
  13. Corker H., Poole R. K. 2003; Nitric oxide formation by Escherichia coli. Dependence on nitrite reductase, the NO-sensing regulator Fnr, and flavohemoglobin Hmp. J Biol Chem 278:31584–31592 [View Article][PubMed]
     [Google Scholar]
  14. Cruz-Ramos H., Crack J., Wu G., Hughes M. N., Scott C., Thomson A. J., Green J., Poole R. K. 2002; NO sensing by FNR: regulation of the Escherichia coli NO-detoxifying flavohaemoglobin, Hmp. EMBO J 21:3235–3244 [View Article][PubMed]
     [Google Scholar]
  15. D'Autréaux B., Touati D., Bersch B., Latour J. M., Michaud-Soret I. 2002; Direct inhibition by nitric oxide of the transcriptional ferric uptake regulation protein via nitrosylation of the iron. Proc Natl Acad Sci U S A 99:16619–16624 [View Article][PubMed]
     [Google Scholar]
  16. D'Autréaux B., Tucker N. P., Dixon R., Spiro S. 2005; A non-haem iron centre in the transcription factor NorR senses nitric oxide. Nature 437:769–772 [View Article][PubMed]
     [Google Scholar]
  17. da Costa P. N., Teixeira M., Saraiva L. M. 2003; Regulation of the flavorubredoxin nitric oxide reductase gene in Escherichia coli: nitrate repression, nitrite induction, and possible post-transcription control. FEMS Microbiol Lett 218:385–393 [View Article][PubMed]
     [Google Scholar]
  18. 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 [View Article][PubMed]
     [Google Scholar]
  19. Davidson A. L., Dassa E., Orelle C., Chen J. 2008; Structure, function, and evolution of bacterial ATP-binding cassette systems. Microbiol Mol Biol Rev 72:317–364 [View Article][PubMed]
     [Google Scholar]
  20. Efromovich S., Grainger D., Bodenmiller D., Spiro S. 2008; Genome-wide identification of binding sites for the nitric oxide-sensitive transcriptional regulator NsrR. Methods Enzymol 437:211–233 [View Article][PubMed]
     [Google Scholar]
  21. Fang F. C. 1997; Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J Clin Invest 99:2818–2825 [View Article][PubMed]
     [Google Scholar]
  22. Fang F. C., Vazquez-Torres A. 2002; Nitric oxide production by human macrophages: there's NO doubt about it. Am J Physiol Lung Cell Mol Physiol 282:L941–L943 [View Article][PubMed]
     [Google Scholar]
  23. Farris M., Grant A., Richardson T. B., O'Connor C. D. 1998; BipA: a tyrosine-phosphorylated GTPase that mediates interactions between enteropathogenic Escherichia coli (EPEC) and epithelial cells. Mol Microbiol 28:265–279 [View Article][PubMed]
     [Google Scholar]
  24. Filenko N., Spiro S., Browning D. F., Squire D., Overton T. W., Cole J., Constantinidou C. 2007; The NsrR regulon of Escherichia coli K-12 includes genes encoding the hybrid cluster protein and the periplasmic, respiratory nitrite reductase. J Bacteriol 189:4410–4417 [View Article][PubMed]
     [Google Scholar]
  25. Gardner P. R. 2005; Nitric oxide dioxygenase function and mechanism of flavohemoglobin, hemoglobin, myoglobin and their associated reductases. J Inorg Biochem 99:247–266 [View Article][PubMed]
     [Google Scholar]
  26. Gardner A. M., Gardner P. R. 2002; Flavohemoglobin detoxifies nitric oxide in aerobic, but not anaerobic, Escherichia coli. Evidence for a novel inducible anaerobic nitric oxide-scavenging activity. J Biol Chem 277:8166–8171 [View Article][PubMed]
     [Google Scholar]
  27. Gardner A. M., Helmick R. A., Gardner P. R. 2002; Flavorubredoxin, an inducible catalyst for nitric oxide reduction and detoxification in Escherichia coli . J Biol Chem 277:8172–8177 [View Article][PubMed]
     [Google Scholar]
  28. Godaly G., Bergsten G., Hang L., Fischer H., Frendéus B., Lundstedt A. C., Samuelsson M., Samuelsson P., Svanborg C. 2001; Neutrophil recruitment, chemokine receptors, and resistance to mucosal infection. J Leukoc Biol 69:899–906[PubMed]
     [Google Scholar]
  29. Gomes C. M., Vicente J. B., Wasserfallen A., Teixeira M. 2000; Spectroscopic studies and characterization of a novel electron-transfer chain from Escherichia coli involving a flavorubredoxin and its flavoprotein reductase partner. Biochemistry 39:16230–16237 [View Article][PubMed]
     [Google Scholar]
  30. Gomes C. M., Giuffrè A., Forte E., Vicente J. B., Saraiva L. M., Brunori M., Teixeira M. 2002; A novel type of nitric-oxide reductase. Escherichia coli flavorubredoxin. J Biol Chem 277:25273–25276 [View Article][PubMed]
     [Google Scholar]
  31. Green L. C., Ruiz de Luzuriaga K., Wagner D. A., Rand W., Istfan N., Young V. R., Tannenbaum S. R. 1981; Nitrate biosynthesis in man. Proc Natl Acad Sci U S A 78:7764–7768 [View Article][PubMed]
     [Google Scholar]
  32. Gunsalus R. P. 1992; Control of electron flow in Escherichia coli: coordinated transcription of respiratory pathway genes. J Bacteriol 174:7069–7074[PubMed]
     [Google Scholar]
  33. Guyer D. M., Radulovic S., Jones F. E., Mobley H. L. 2002; Sat, the secreted autotransporter toxin of uropathogenic Escherichia coli, is a vacuolating cytotoxin for bladder and kidney epithelial cells. Infect Immun 70:4539–4546 [View Article][PubMed]
     [Google Scholar]
  34. Hagan E. C., Lloyd A. L., Rasko D. A., Faerber G. J., Mobley H. L. 2010; Escherichia coli global gene expression in urine from women with urinary tract infection. PLoS Pathog 6:e1001187 [View Article][PubMed]
     [Google Scholar]
  35. Haugen B. J., Pellett S., Redford P., Hamilton H. L., Roesch P. L., Welch R. A. 2007; In vivo gene expression analysis identifies genes required for enhanced colonization of the mouse urinary tract by uropathogenic Escherichia coli strain CFT073 dsdA . Infect Immun 75:278–289 [View Article][PubMed]
     [Google Scholar]
  36. Hausladen A., Privalle C. T., Keng T., DeAngelo J., Stamler J. S. 1996; Nitrosative stress: activation of the transcription factor OxyR. Cell 86:719–729 [View Article][PubMed]
     [Google Scholar]
  37. Hausladen A., Gow A., Stamler J. S. 2001; Flavohemoglobin denitrosylase catalyzes the reaction of a nitroxyl equivalent with molecular oxygen. Proc Natl Acad Sci U S A 98:10108–10112 [View Article][PubMed]
     [Google Scholar]
  38. Hertz G. Z., Stormo G. D. 1999; Identifying DNA and protein patterns with statistically significant alignments of multiple sequences. Bioinformatics 15:563–577 [View Article][PubMed]
     [Google Scholar]
  39. Huang D. W., Sherman B. T., Tan Q., Collins J. R., Alvord W. G., Roayaei J., Stephens R., Baseler M. W., Lane H. C., Lempicki R. A. 2007; The DAVID Gene Functional Classification Tool: a novel biological module-centric algorithm to functionally analyze large gene lists. Genome Biol 8:R183 [View Article][PubMed]
     [Google Scholar]
  40. Hutchings M. I., Mandhana N., Spiro S. 2002; The NorR protein of Escherichia coli activates expression of the flavorubredoxin gene norV in response to reactive nitrogen species. J Bacteriol 184:4640–4643 [View Article][PubMed]
     [Google Scholar]
  41. Hyduke D. R., Jarboe L. R., Tran L. M., Chou K. J., Liao J. C. 2007; Integrated network analysis identifies nitric oxide response networks and dihydroxyacid dehydratase as a crucial target in Escherichia coli . Proc Natl Acad Sci U S A 104:8484–8489 [View Article][PubMed]
     [Google Scholar]
  42. Jann K., Jann B. 1992; Capsules of Escherichia coli, expression and biological significance. Can J Microbiol 38:705–710 [View Article][PubMed]
     [Google Scholar]
  43. Ji X. B., Hollocher T. C. 1988; Reduction of nitrite to nitric oxide by enteric bacteria. Biochem Biophys Res Commun 157:106–108 [View Article][PubMed]
     [Google Scholar]
  44. Justino M. C., Vicente J. B., Teixeira M., Saraiva L. M. 2005; New genes implicated in the protection of anaerobically grown Escherichia coli against nitric oxide. J Biol Chem 280:2636–2643 [View Article][PubMed]
     [Google Scholar]
  45. Kaboré A. F., Simard M., Bergeron M. G. 1999; Local production of inflammatory mediators in an experimental model of acute obstructive pyelonephritis. J Infect Dis 179:1162–1172 [View Article][PubMed]
     [Google Scholar]
  46. Kim Y. M., Bergonia H. A., Müller C., Pitt B. R., Watkins W. D., Lancaster J. R. Jr 1995; Loss and degradation of enzyme-bound heme induced by cellular nitric oxide synthesis. J Biol Chem 270:5710–5713 [View Article][PubMed]
     [Google Scholar]
  47. Lane M. C., Lockatell V., Monterosso G., Lamphier D., Weinert J., Hebel J. R., Johnson D. E., Mobley H. L. 2005; Role of motility in the colonization of uropathogenic Escherichia coli in the urinary tract. Infect Immun 73:7644–7656 [View Article][PubMed]
     [Google Scholar]
  48. Langmead B., Trapnell C., Pop M., Salzberg S. L. 2009; Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25 [View Article][PubMed]
     [Google Scholar]
  49. Leng N., Dawson J. A., Thomson J. A., Ruotti V., Rissman A. I., Smits B. M., Haag J. D., Gould M. N., Stewart R. M., Kendziorski C. 2013; EBSeq: an empirical Bayes hierarchical model for inference in RNA-seq experiments. Bioinformatics 29:1035–1043 [View Article][PubMed]
     [Google Scholar]
  50. Lewis V. G., Ween M. P., McDevitt C. A. 2012; The role of ATP-binding cassette transporters in bacterial pathogenicity. Protoplasma 249:919–942 [View Article][PubMed]
     [Google Scholar]
  51. Li B., Dewey C. N. 2011; RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323 [View Article][PubMed]
     [Google Scholar]
  52. Lidder S., Webb A. J. 2013; Vascular effects of dietary nitrate (as found in green leafy vegetables and beetroot) via the nitrate–nitrite–nitric oxide pathway. Br J Clin Pharmacol 75:677–696[PubMed]
     [Google Scholar]
  53. Lin H. Y., Bledsoe P. J., Stewart V. 2007; Activation of yeaR-yoaG operon transcription by the nitrate-responsive regulator NarL is independent of oxygen-responsive regulator Fnr in Escherichia coli K-12. J Bacteriol 189:7539–7548 [View Article][PubMed]
     [Google Scholar]
  54. Lundberg J. O., Ehrén I., Jansson O., Adolfsson J., Lundberg J. M., Weitzberg E., Alving K., Wiklund N. P. 1996; Elevated nitric oxide in the urinary bladder in infectious and noninfectious cystitis. Urology 48:700–702 [View Article][PubMed]
     [Google Scholar]
  55. Mills P. C., Rowley G., Spiro S., Hinton J. C., Richardson D. J. 2008; A combination of cytochrome c nitrite reductase (NrfA) and flavorubredoxin (NorV) protects Salmonella enterica serovar Typhimurium against killing by NO in anoxic environments. Microbiology 154:1218–1228 [View Article][PubMed]
     [Google Scholar]
  56. Mobley H. L., Green D. M., Trifillis A. L., Johnson D. E., Chippendale G. R., Lockatell C. V., Jones B. D., Warren J. W. 1990; Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. Infect Immun 58:1281–1289[PubMed]
     [Google Scholar]
  57. Mowat C. G., Gazur B., Campbell L. P., Chapman S. K. 2010; Flavin-containing heme enzymes. Arch Biochem Biophys 493:37–52 [Mills et al., 2008 0002] [View Article]
     [Google Scholar]
  58. Mukhopadhyay P., Zheng M., Bedzyk L. A., LaRossa R. A., Storz G. 2004; Prominent roles of the NorR and Fur regulators in the Escherichia coli transcriptional response to reactive nitrogen species. Proc Natl Acad Sci U S A 101:745–750 [View Article][PubMed]
     [Google Scholar]
  59. Myers K. S., Yan H., Ong I. M., Chung D., Liang K., Tran F., Keleş S., Landick R., Kiley P. J. 2013; Genome-scale analysis of Escherichia coli FNR reveals complex features of transcription factor binding. PLoS Genet 9:e1003565 [View Article][PubMed]
     [Google Scholar]
  60. Mysorekar I. U., Mulvey M. A., Hultgren S. J., Gordon J. I. 2002; Molecular regulation of urothelial renewal and host defenses during infection with uropathogenic Escherichia coli . J Biol Chem 277:7412–7419 [View Article][PubMed]
     [Google Scholar]
  61. Neidhardt F. C., Bloch P. L., Smith D. F. 1974; Culture medium for enterobacteria. J Bacteriol 119:736–747[PubMed]
     [Google Scholar]
  62. 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]
  63. Poljakovic M., Svensson M. L., Svanborg C., Johansson K., Larsson B., Persson K. 2001; Escherichia coli-induced inducible nitric oxide synthase and cyclooxygenase expression in the mouse bladder and kidney. Kidney Int 59:893–904 [View Article][PubMed]
     [Google Scholar]
  64. Pomposiello P. J., Demple B. 2001; Redox-operated genetic switches: the SoxR and OxyR transcription factors. Trends Biotechnol 19:109–114 [View Article][PubMed]
     [Google Scholar]
  65. Poock S. R., Leach E. R., Moir J. W., Cole J. A., Richardson D. J. 2002; Respiratory detoxification of nitric oxide by the cytochrome c nitrite reductase of Escherichia coli . J Biol Chem 277:23664–23669 [View Article][PubMed]
     [Google Scholar]
  66. Prohl C., Wackwitz B., Vlad D., Unden G. 1998; Functional citric acid cycle in an arcA mutant of Escherichia coli during growth with nitrate under anoxic conditions. Arch Microbiol 170:1–7 [View Article][PubMed]
     [Google Scholar]
  67. Pullan S. T., Gidley M. D., Jones R. A., Barrett J., Stevanin T. M., Read R. C., Green J., Poole R. K. 2007; Nitric oxide in chemostat-cultured Escherichia coli is sensed by Fnr and other global regulators: unaltered methionine biosynthesis indicates lack of S nitrosation. J Bacteriol 189:1845–1855 [View Article][PubMed]
     [Google Scholar]
  68. Radomski J. L., Palmiri C., Hearn W. L. 1978; Concentrations of nitrate in normal human urine and the effect of nitrate ingestion. Toxicol Appl Pharmacol 45:63–68 [View Article][PubMed]
     [Google Scholar]
  69. Ren B., Zhang N., Yang J., Ding H. 2008; Nitric oxide-induced bacteriostasis and modification of iron–sulphur proteins in Escherichia coli . Mol Microbiol 70:953–964[PubMed]
     [Google Scholar]
  70. Rodionov D. A., Dubchak I. L., Arkin A. P., Alm E. J., Gelfand M. S. 2005; Dissimilatory metabolism of nitrogen oxides in bacteria: comparative reconstruction of transcriptional networks. PLOS Comput Biol 1:e55 [View Article][PubMed]
     [Google Scholar]
  71. Roos V., Klemm P. 2006; Global gene expression profiling of the asymptomatic bacteriuria Escherichia coli strain 83972 in the human urinary tract. Infect Immun 74:3565–3575 [View Article][PubMed]
     [Google Scholar]
  72. Roos V., Nielsen E. M., Klemm P. 2006; Asymptomatic bacteriuria Escherichia coli strains: adhesins, growth and competition. FEMS Microbiol Lett 262:22–30 [View Article][PubMed]
     [Google Scholar]
  73. Rowe S., Hodson N., Griffiths G., Roberts I. S. 2000; Regulation of the Escherichia coli K5 capsule gene cluster: evidence for the roles of H-NS, BipA, and integration host factor in regulation of group 2 capsule gene clusters in pathogenic E. coli . J Bacteriol 182:2741–2745 [View Article][PubMed]
     [Google Scholar]
  74. Seo S. W., Kim D., Latif H., O'Brien E. J., Szubin R., Palsson B. O. 2014; Deciphering Fur transcriptional regulatory network highlights its complex role beyond iron metabolism in Escherichia coli . Nat Commun 5:4910 [View Article][PubMed]
     [Google Scholar]
  75. Silaghi-Dumitrescu R., Coulter E. D., Das A., Ljungdahl L. G., Jameson G. N., Huynh B. H., Kurtz D. M. Jr 2003; A flavodiiron protein and high molecular weight rubredoxin from Moorella thermoacetica with nitric oxide reductase activity. Biochemistry 42:2806–2815 [View Article][PubMed]
     [Google Scholar]
  76. Silaghi-Dumitrescu R., Ng K. Y., Viswanathan R., Kurtz D. M. Jr 2005; A flavo-diiron protein from Desulfovibrio vulgaris with oxidase and nitric oxide reductase activities. Evidence for an in vivo nitric oxide scavenging function. Biochemistry 44:3572–3579 [View Article][PubMed]
     [Google Scholar]
  77. Smith S. D., Wheeler M. A., Foster H. E. Jr, Weiss R. M. 1996; Urinary nitric oxide synthase activity and cyclic GMP levels are decreased with interstitial cystitis and increased with urinary tract infections. J Urol 155:1432–1435 [View Article][PubMed]
     [Google Scholar]
  78. Snyder J. A., Haugen B. J., Buckles E. L., Lockatell C. V., Johnson D. E., Donnenberg M. S., Welch R. A., Mobley H. L. 2004; Transcriptome of uropathogenic Escherichia coli during urinary tract infection. Infect Immun 72:6373–6381 [View Article][PubMed]
     [Google Scholar]
  79. Spiro S. 2007; Regulators of bacterial responses to nitric oxide. FEMS Microbiol Rev 31:193–211 [View Article][PubMed]
     [Google Scholar]
  80. Spiro S. 2011; Nitric oxide stress in Escherichia coli and Salmonella . Stress Response in Pathogenic Bacteria48–67Edited by Kidd S. Wallingford: CABI;[PubMed] [CrossRef]
     [Google Scholar]
  81. Stern A. M., Hay A. J., Liu Z., Desland F. A., Zhang J., Zhong Z., Zhu J. 2012; The NorR regulon is critical for Vibrio cholerae resistance to nitric oxide and sustained colonization of the intestines. MBio 3:e00013–12 [View Article][PubMed]
     [Google Scholar]
  82. Stevanin T. M., Ioannidis N., Mills C. E., Kim S. O., Hughes M. N., Poole R. K. 2000; Flavohemoglobin Hmp affords inducible protection for Escherichia coli respiration, catalyzed by cytochromes bo’ or bd, from nitric oxide. J Biol Chem 275:35868–35875 [View Article][PubMed]
     [Google Scholar]
  83. Stewart V. 1993; Nitrate regulation of anaerobic respiratory gene expression in Escherichia coli . Mol Microbiol 9:425–434 [View Article][PubMed]
     [Google Scholar]
  84. Subashchandrabose S., Hazen T. H., Brumbaugh A. R., Himpsl S. D., Smith S. N., Ernst R. D., Rasko D. A., Mobley H. L. 2014; Host-specific induction of Escherichia coli fitness genes during human urinary tract infection. Proc Natl Acad Sci U S A 111:18327–18332 [View Article][PubMed]
     [Google Scholar]
  85. Sutherland P., McAlister-Henn L. 1985; Isolation and expression of the Escherichia coli gene encoding malate dehydrogenase. J Bacteriol 163:1074–1079[PubMed]
     [Google Scholar]
  86. Svensson L., Marklund B. I., Poljakovic M., Persson K. 2006; Uropathogenic Escherichia coli and tolerance to nitric oxide: the role of flavohemoglobin. J Urol 175:749–753 [View Article][PubMed]
     [Google Scholar]
  87. Svensson L., Poljakovic M., Säve S., Gilberthorpe N., Schön T., Strid S., Corker H., Poole R. K., Persson K. 2010; Role of flavohemoglobin in combating nitrosative stress in uropathogenic Escherichia coli – implications for urinary tract infection. Microb Pathog 49:59–66 [View Article][PubMed]
     [Google Scholar]
  88. Tucker N. P., D'Autréaux B., Studholme D. J., Spiro S., Dixon R. 2004; DNA binding activity of the Escherichia coli nitric oxide sensor NorR suggests a conserved target sequence in diverse proteobacteria. J Bacteriol 186:6656–6660 [View Article][PubMed]
     [Google Scholar]
  89. Tucker N. P., Le Brun N. E., Dixon R., Hutchings M. I. 2010; There's NO stopping NsrR, a global regulator of the bacterial NO stress response. Trends Microbiol 18:149–156 [View Article][PubMed]
     [Google Scholar]
  90. van Wonderen J. H., Burlat B., Richardson D. J., Cheesman M. R., Butt J. N. 2008; The nitric oxide reductase activity of cytochrome c nitrite reductase from Escherichia coli . J Biol Chem 283:9587–9594 [View Article][PubMed]
     [Google Scholar]
  91. Vine C. E., Cole J. A. 2011a; Nitrosative stress in Escherichia coli: reduction of nitric oxide. Biochem Soc Trans 39:213–215 [View Article][PubMed]
     [Google Scholar]
  92. Vine C. E., Cole J. A. 2011b; Unresolved sources, sinks, and pathways for the recovery of enteric bacteria from nitrosative stress. FEMS Microbiol Lett 325:99–107 [View Article][PubMed]
     [Google Scholar]
  93. Welch R. A., Burland V., Plunkett G. III, Redford P., Roesch P., Rasko D., Buckles E. L., Liou S. R., Boutin A., other authors. 2002; Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli . Proc Natl Acad Sci U S A 99:17020–17024 [View Article][PubMed]
     [Google Scholar]
  94. Wheeler M. A., Smith S. D., García-Cardeña G., Nathan C. F., Weiss R. M., Sessa W. C. 1997; Bacterial infection induces nitric oxide synthase in human neutrophils. J Clin Invest 99:110–116 [View Article][PubMed]
     [Google Scholar]
  95. Yu H., Sato E. F., Nagata K., Nishikawa M., Kashiba M., Arakawa T., Kobayashi K., Tamura T., Inoue M. 1997; Oxygen-dependent regulation of the respiration and growth of Escherichia coli by nitric oxide. FEBS Lett 409:161–165 [View Article][PubMed]
     [Google Scholar]
  96. Zhang Y., Liu T., Meyer C. A., Eeckhoute J., Johnson D. S., Bernstein B. E., Nusbaum C., Myers R. M., Brown M., other authors. 2008; Model-based analysis of ChIP-Seq (MACS). Genome Biol 9:R137 [View Article][PubMed]
     [Google Scholar]
  97. Mehta, H.H., Liu, Y., Zhang, M.Q. & Spiro, S. Gene Expression Omnibus GSE69830 (2015).
  98. Mehta, H.H., Liu, Y., Zhang, M.Q. & Spiro, S. Gene Expression Omnibus GSE69829 (2015).
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000031
Loading
Genome-wide analysis of the response to nitric oxide in uropathogenic Escherichia coli CFT073
M Gen 1, e000031 (2015); https://doi.org/10.1099/mgen.0.000031
/content/journal/mgen/10.1099/mgen.0.000031
/content/journal/mgen/10.1099/mgen.0.000031
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error