NsrR, GadE, and GadX Interplay in Repressing Expression of the Escherichia coli O157:H7 LEE Pathogenicity Island in Response to Nitric Oxide

PLoS Pathogens

Volumn 10, Issue 1, 2014, Pages

  Branchu, Priscilla ^a,c   Matrat, Stéphanie ^a   Vareille, Marjolaine ^a,d   Garrivier, Annie ^a   Durand, Alexandra ^a   Crépin, Sébastien ^b,e   Harel, Josée ^b   Jubelin, Grégory ^a   Gobert, Alain P ^a  

^a CEMAGREF   (France)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c UMR1319 MICALIS   (France)

^d INRA and University of Auvergne   (France)

^e UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARAC PROTEIN; DNA BINDING PROTEIN; ESCHERICHIA COLI PROTEIN; GADE PROTEIN, E COLI; GADX PROTEIN, E COLI; NITRIC OXIDE; NSRR PROTEIN, E COLI; TRANSCRIPTION FACTOR;

BACTERIUM ADHERENCE; BIOSYNTHESIS; EPITHELIUM CELL; ESCHERICHIA COLI O157; GENE EXPRESSION REGULATION; GENETICS; GENOMIC ISLAND; HELA CELL LINE; HUMAN; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

ARAC TRANSCRIPTION FACTOR; BACTERIAL ADHESION; DNA-BINDING PROTEINS; EPITHELIAL CELLS; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENOMIC ISLANDS; HELA CELLS; HUMANS; INTESTINAL MUCOSA; NITRIC OXIDE; TRANSCRIPTION FACTORS;

EID: 84893740053     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003874     Document Type: Article

References (43)

1. Karmali MA, Gannon V, Sargeant JM, (2010) Verocytotoxin-producing Escherichia coli (VTEC). Vet Microbiol 140: 360-370.
2. McDaniel TK, Jarvis KG, Donnenberg MS, Kaper JB, (1995) A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci U S A 92: 1664-1668.
3. Garmendia J, Phillips AD, Carlier MF, Chong Y, Schuller S, et al. (2004) TccP is an enterohaemorrhagic Escherichia coli O157:H7 type III effector protein that couples Tir to the actin-cytoskeleton. Cell Microbiol 6: 1167-1183.
4. Gruenheid S, Sekirov I, Thomas NA, Deng W, O'Donnell P, et al. (2004) Identification and characterization of NleA, a non-LEE-encoded type III translocated virulence factor of enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol 51: 1233-1249.
5. Hauf N, Chakraborty T, (2003) Suppression of NF-kappa B activation and proinflammatory cytokine expression by Shiga toxin-producing Escherichia coli. J Immunol 170: 2074-2082.
6. Gobert AP, Coste A, Guzman CA, Vareille M, Hindre T, et al. (2008) Modulation of chemokine gene expression by Shiga-toxin producing Escherichia coli belonging to various origins and serotypes. Microbes Infect 10: 159-165.
7. Collington GK, Booth IW, Donnenberg MS, Kaper JB, Knutton S, (1998) Enteropathogenic Escherichia coli virulence genes encoding secreted signalling proteins are essential for modulation of Caco-2 cell electrolyte transport. Infect Immun 66: 6049-6053.
8. Tree JJ, Roe AJ, Flockhart A, McAteer SP, Xu X, et al. (2011) Transcriptional regulators of the GAD acid stress island are carried by effector protein-encoding prophages and indirectly control type III secretion in enterohemorrhagic Escherichia coli O157:H7. Mol Microbiol 80: 1349-1365.
9. Deng W, Puente JL, Gruenheid S, Li Y, Vallance BA, et al. (2004) Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci U S A 101: 3597-3602.
10. Elliott SJ, Sperandio V, Giron JA, Shin S, Mellies JL, et al. (2000) The locus of enterocyte effacement (LEE)-encoded regulator controls expression of both LEE- and non-LEE-encoded virulence factors in enteropathogenic and enterohemorrhagic Escherichia coli. Infect Immun 68: 6115-6126.
11. Sperandio V, Mellies JL, Delahay RM, Frankel G, Crawford JA, et al. (2000) Activation of enteropathogenic Escherichia coli (EPEC) LEE2 and LEE3 operons by Ler. Mol Microbiol 38: 781-793.
12. Bhatt S, Romeo T, Kalman D, (2011) Honing the message: post-transcriptional and post-translational control in attaching and effacing pathogens. Trends Microbiol 19: 217-224.
13. Ma Z, Richard H, Tucker DL, Conway T, Foster JW, (2002) Collaborative regulation of Escherichia coli glutamate-dependent acid resistance by two AraC-like regulators, GadX and GadW (YhiW). J Bacteriol 184: 7001-7012.
14. Tucker DL, Tucker N, Ma Z, Foster JW, Miranda RL, et al. (2003) Genes of the GadX-GadW regulon in Escherichia coli. J Bacteriol 185: 3190-3201.
15. Hommais F, Krin E, Coppee JY, Lacroix C, Yeramian E, et al. (2004) GadE (YhiE): a novel activator involved in the response to acid environment in Escherichia coli. Microbiology 150: 61-72.
16. Kailasan Vanaja S, Bergholz TM, Whittam TS, (2009) Characterization of the Escherichia coli O157:H7 Sakai GadE regulon. J Bacteriol 191: 1868-1877.
17. Vareille M, de Sablet T, Hindre T, Martin C, Gobert AP, (2007) Nitric oxide inhibits Shiga-toxin synthesis by enterohemorrhagic Escherichia coli. Proc Natl Acad Sci U S A 104: 10199-10204.
18. Bodenmiller DM, Spiro S, (2006) The yjeB (nsrR) gene of Escherichia coli encodes a nitric oxide-sensitive transcriptional regulator. J Bacteriol 188: 874-881.
19. Vareille M, Rannou F, Thelier N, Glasser AL, de Sablet T, et al. (2008) Heme oxygenase-1 is a critical regulator of nitric oxide production in enterohemorrhagic Escherichia coli-infected human enterocytes. J Immunol 180: 5720-5726.
20. Tatsuno I, Nagano K, Taguchi K, Rong L, Mori H, et al. (2003) Increased adherence to Caco-2 cells caused by disruption of the yhiE and yhiF genes in enterohemorrhagic Escherichia coli O157:H7. Infect Immun 71: 2598-2606.
21. Shin S, Castanie-Cornet MP, Foster JW, Crawford JA, Brinkley C, et al. (2001) An activator of glutamate decarboxylase genes regulates the expression of enteropathogenic Escherichia coli virulence genes through control of the plasmid-encoded regulator, Per. Mol Microbiol 41: 1133-1150.
22. Sayed AK, Odom C, Foster JW, (2007) The Escherichia coli AraC-family regulators GadX and GadW activate gadE, the central activator of glutamate-dependent acid resistance. Microbiology 153: 2584-2592.
23. Tramonti A, Visca P, De Canio M, Falconi M, De Biase D, (2002) Functional characterization and regulation of gadX, a gene encoding an AraC/XylS-like transcriptional activator of the Escherichia coli glutamic acid decarboxylase system. J Bacteriol 184: 2603-2613.
24. Sperandio V, Mellies JL, Nguyen W, Shin S, Kaper JB, (1999) Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc Natl Acad Sci U S A 96: 15196-15201.
25. Sperandio V, Li CC, Kaper JB, (2002) Quorum-sensing Escherichia coli regulator A: a regulator of the LysR family involved in the regulation of the locus of enterocyte effacement pathogenicity island in enterohemorrhagic E. coli. Infect Immun 70: 3085-3093.
26. Porter ME, Mitchell P, Free A, Smith DG, Gally DL, (2005) The LEE1 promoters from both enteropathogenic and enterohemorrhagic Escherichia coli can be activated by PerC-like proteins from either organism. J Bacteriol 187: 458-472.
27. Lodato PB, Kaper JB, (2009) Post-transcriptional processing of the LEE4 operon in enterohaemorrhagic Escherichia coli. Mol Microbiol 71: 273-290.
28. Haack KR, Robinson CL, Miller KJ, Fowlkes JW, Mellies JL, (2003) Interaction of Ler at the LEE5 (tir) operon of enteropathogenic Escherichia coli. Infect Immun 71: 384-392.
29. Partridge JD, Bodenmiller DM, Humphrys MS, 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.
30. Lee DJ, Minchin SD, Busby SJ, (2012) Activating transcription in bacteria. Annu Rev Microbiol 66: 125-152.
31. Busby S, Ebright RH, (1999) Transcription activation by catabolite activator protein (CAP). J Mol Biol 293: 199-213.
32. Bougdour A, Lelong C, Geiselmann J, (2004) Crl, a low temperature-induced protein in Escherichia coli that binds directly to the stationary phase sigma subunit of RNA polymerase. J Biol Chem 279: 19540-19550.
33. Rodionov DA, Dubchak IL, Arkin AP, Alm EJ, Gelfand MS, (2005) Dissimilatory metabolism of nitrogen oxides in bacteria: comparative reconstruction of transcriptional networks. PLoS Comput Biol 1: e55.
34. Filenko N, Spiro S, Browning DF, Squire D, Overton TW, et al. (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.
35. Karlinsey JE, Bang IS, Becker LA, Frawley ER, Porwollik S, et al. (2012) The NsrR regulon in nitrosative stress resistance of Salmonella enterica serovar Typhimurium. Mol Microbiol 85: 1179-1193.
36. Tucker NP, Hicks MG, Clarke TA, Crack JC, Chandra G, et al. (2008) The transcriptional repressor protein NsrR senses nitric oxide directly via a [2Fe-2S] cluster. PLoS One 3: e3623.
37. Tucker NP, Le Brun NE, Dixon R, Hutchings MI, (2010) There's NO stopping NsrR, a global regulator of the bacterial NO stress response. Trends Microbiol 18: 149-156.
38. Iyoda S, Watanabe H, (2004) Positive effects of multiple pch genes on expression of the locus of enterocyte effacement genes and adherence of enterohaemorrhagic Escherichia coli O157:H7 to HEp-2 cells. Microbiology 150: 2357-2571.
39. O'Brien AO, Lively TA, Chen ME, Rothman SW, Formal SB, (1983) Escherichia coli O157:H7 strains associated with haemorrhagic colitis in the United States produce a Shigella dysenteriae 1 (SHIGA) like cytotoxin. Lancet 1: 702.
40. Beloin C, Valle J, Latour-Lambert P, Faure P, Kzreminski M, et al. (2004) Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol 51: 659-674.
41. Datsenko KA, Wanner BL, (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.
42. Large TM, Walk ST, Whittam TS, (2005) Variation in acid resistance among shiga toxin-producing clones of pathogenic Escherichia coli. Appl Environ Microbiol 71: 2493-2500.
43. Lanois A, Jubelin G, Givaudan A, (2008) FliZ, a flagellar regulator, is at the crossroads between motility, haemolysin expression and virulence in the insect pathogenic bacterium Xenorhabdus. Mol Microbiol 68: 516-533.