969
Views
0
CrossRef citations to date
0
Altmetric
Review Article

Genomic island-encoded regulatory proteins in enterohemorrhagic Escherichia coli O157:H7

, , , , , & ORCID Icon show all
Article: 2313407 | Received 24 Oct 2023, Accepted 23 Jan 2024, Published online: 15 Feb 2024

References

  • Karmali MA. Infection by verocytotoxin-producing Escherichia coli. Clin Microbiol Rev. 1989;2(1):15‒38. doi: 10.1128/CMR.2.1.15
  • Caprioli A, Morabito S, Brugere H, et al. Enterohaemorrhagic Escherichia coli: emerging issues on virulence and modes of transmission. Vet Res. 2005;36(3):289‒311. doi: 10.1051/vetres:2005002
  • Watanabe H. Pathogenesis of enterohaemorrhagic Escherichia coli infection. Nihon Rinsho. 2012;70:1318‒1322.
  • Berger CN, Sodha SV, Shaw RK, et al. Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ Microbiol. 2010;12(9):2385‒2397. doi: 10.1111/j.1462-2920.2010.02297.x
  • Rangel JM, Sparling PH, Crowe C, et al. Epidemiology of Escherichia coli O157:H7 Outbreaks, United States, 1982–2002. Emerg Infect Dis. 2005;11(4):603‒609. doi: 10.3201/eid1104.040739
  • Schmid-Hempel P, Frank SA, Manchester M. Pathogenesis, virulence, and infective dose. PLoS Pathog. 2007;3(10):1372‒1373. doi: 10.1371/journal.ppat.0030147
  • Franzin FM, Sircili MP. Locus of enterocyte effacement: a pathogenicity island involved in the virulence of enteropathogenic and enterohemorragic Escherichia coli subjected to a complex network of gene regulation. Biomed Res Int. 2015;2015:534738. doi: 10.1155/2015/534738
  • Slater SL, Sågfors AM, Pollard DJ, et al. The type III secretion system of pathogenic Escherichia coli. Curr Top Microbiol Immunol. 2018:51‒72. doi: 10.1007/82_2018_116
  • McDaniel TK, Jarvis KG, Donnenberg MS, et al. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci U S A. 1995;92(5):1664‒1668. doi: 10.1073/pnas.92.5.1664
  • Hayashi T, Makino K, Ohnishi M, et al. Complete genome sequence of enterohemorrhagic Escherichia coli O157: H7 and genomic comparison with a laboratory strain K-12. DNA Res. 2001;8(1):11‒22. doi: 10.1093/dnares/8.1.11
  • Jiang L, Yang W, Jiang X, et al. Virulence-related O islands in enterohemorrhagic Escherichia coli O157: H7. Gut Microbes. 2021;13(1):1992237. doi: 10.1080/19490976.2021.1992237
  • Xu Y, Xu X, Lan R, et al. An O island 172 encoded RNA helicase regulates the motility of Escherichia coli O157: H7. PLoS One. 2013;8(6):e64211. doi: 10.1371/journal.pone.0064211
  • Connolly JPR, O’Boyle N, Turner NCA, et al. Distinct intraspecies virulence mechanisms regulated by a conserved transcription factor. Proc Natl Acad Sci U S A. 2019;116(39):19695‒19704. doi: 10.1073/pnas.1903461116
  • Mellies JL, Barron AM, Carmona AM. Enteropathogenic and enterohemorrhagic Escherichia coli virulence gene regulation. Infect Immun. 2007;75(9):4199‒4210. doi: 10.1128/IAI.01927-06
  • Yang B, Feng L, Wang F, et al. Enterohemorrhagic Escherichia coli senses low biotin status in the large intestine for colonization and infection. Nat Commun. 2015;6(1):6592. doi: 10.1038/ncomms7592
  • Sharma VK, Zuerner RL. Role of hha and ler in transcriptional regulation of the esp operon of enterohemorrhagic Escherichia coli O157: H7. J Bacteriol. 2004;186(21):7290‒7301. doi: 10.1128/JB.186.21.7290-7301.2004
  • Liu Y, Liu B, Yang P, et al. LysR-type transcriptional regulator OvrB encoded in O island 9 drives enterohemorrhagic Escherichia coli O157:H7 virulence. Virulence. 2019;10(1):783‒792. doi: 10.1080/21505594.2019.1661721
  • Liu B, Wang J, Wang L, et al. Transcriptional activator OvrA encoded in O island 19 modulates virulence gene expression in enterohemorrhagic Escherichia coli O157:H7. J Infect Dis. 2020;221:820‒829. doi: 10.1093/infdis/jiz458
  • Hernandez-Doria JD, Sperandio V. Bacteriophage transcription factor Cro regulates virulence gene expression in enterohemorrhagic Escherichia coli. Cell Host Microbe. 2018;23(5):607‒617.e6. doi: 10.1016/j.chom.2018.04.007
  • Tobe T, Ando H, Ishikawa H, et al. Dual regulatory pathways integrating the RcsC–RcsD–RcsB signalling system control enterohaemorrhagic Escherichia coli pathogenicity. Mol Microbiol. 2005;58(1):320‒333. doi: 10.1111/j.1365-2958.2005.04828.x
  • Flockhart AF, Tree JJ, Xu X, et al. Identification of a novel prophage regulator in Escherichia coli controlling the expression of type III secretion. Mol Microbiol. 2012;83(1):208‒223. doi: 10.1111/j.1365-2958.2011.07927.x
  • D’Souza SE, Ginsberg MH, Plow EF. Arginyl-glycyl-aspartic acid (RGD): A cell adhesion motif. Trends Biochem Sci. 1991;16:246‒250. doi: 10.1016/0968-0004(91)90096-e
  • Kendall MM, Rasko DA, Sperandio V. The LysR-type regulator QseA regulates both characterized and putative virulence genes in enterohaemorrhagic Escherichia coli O157: H7. Mol Microbiol. 2010;76(5):1306‒1321. doi: 10.1111/j.1365-2958.2010.07174.x
  • Luzader DH, Willsey GG, Wargo MJ, et al. The type three secretion system 2-encoded regulator EtrB modulates enterohemorrhagic Escherichia coli virulence gene expression. Infect Immun. 2016;84(9):2555‒2565. doi: 10.1128/IAI.00407-16
  • Liu Y, Han R, Wang J, et al. Magnesium sensing regulates intestinal colonization of enterohemorrhagic Escherichia coli O157:H7. MBio. 2020;11(6):11. doi: 10.1128/mBio.02470-20
  • Feng L, Yang B, Xu Y, et al. Elucidation of a complete mechanical signaling and virulence activation pathway in enterohemorrhagic Escherichia coli. Cell Rep. 2022;39(1):110614. doi: 10.1016/j.celrep.2022.110614
  • Islam MS, Bingle LE, Pallen MJ, et al. Organization of the LEE1 operon regulatory region of enterohaemorrhagic Escherichia coli O157: H7 and activation by GrlA. Mol Microbiol. 2011;79(2):468‒483. doi: 10.1111/j.1365-2958.2010.07460.x
  • Padavannil A, Jobichen C, Mills E, et al. Structure of GrlR–GrlA complex that prevents GrlA activation of virulence genes. Nat Commun. 2013;4(1):2546. doi: 10.1038/ncomms3546
  • Bender JK, Praszkier J, Wakefield MJ, et al. Involvement of PatE, a prophage-encoded AraC-like regulator, in the transcriptional activation of acid resistance pathways of enterohemorrhagic Escherichia coli strain EDL933. Appl Environ Microbiol. 2012;78(15):5083‒5092. doi: 10.1128/AEM.00617-12
  • Tree JJ, Roe AJ, Flockhart A, et al. 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. 2011;80(5):1349‒1365. doi: 10.1111/j.1365-2958.2011.07650.x
  • Darwin KH, Miller VL. InvF is required for expression of genes encoding proteins secreted by the SPI1 type III secretion apparatus in salmonella typhimurium. J Bacteriol. 1999;181(16):4949‒4954. doi: 10.1128/JB.181.16.4949-4954.1999
  • Zhang L, Chaudhuri RR, Constantinidou C, et al. Regulators encoded in the Escherichia coli type III secretion system 2 gene cluster influence expression of genes within the locus for enterocyte effacement in enterohemorrhagic E. coli O157: H7. Infect Immun. 2004;72(12):7282‒7293. doi: 10.1128/IAI.72.12.7282-7293.2004
  • Ren CP, Chaudhuri RR, Fivian A, et al. The ETT2 gene cluster, encoding a second type III secretion system from Escherichia coli, is present in the majority of strains but has undergone widespread mutational attrition. J Bacteriol. 2004;186(11):3547‒3560. doi: 10.1128/JB.186.11.3547-3560.2004
  • Wang S, Xu X, Liu X, et al. Escherichia coli type III secretion system 2 regulator EtrA promotes virulence of avian pathogenic Escherichia coli. Microbiol (Reading). 2017;163(10):1515‒1524. doi: 10.1099/mic.0.000525
  • Yang B, Wang S, Huang J, et al. Transcriptional activator GmrA, encoded in genomic island OI-29, controls the motility of enterohemorrhagic Escherichia coli O157: H7. Front Microbiol. 2018;9:338. doi: 10.3389/fmicb.2018.00338
  • Iyoda S, Koizumi N, Satou H, et al. The GrlR-GrlA regulatory system coordinately controls the expression of flagellar and LEE-encoded type III protein secretion systems in enterohemorrhagic Escherichia coli. J Bacteriol. 2006;188(16):5682‒5692. doi: 10.1128/JB.00352-06
  • Allison SE, Silphaduang U, Mascarenhas M, et al. Novel repressor of Escherichia coli O157: H7 motility encoded in the putative fimbrial cluster OI-1. J Bacteriol. 2012;194(19):5343‒5352. doi: 10.1128/JB.01025-12
  • Yang J, Russell TW, Hocking DM, et al. Control of acid resistance pathways of enterohemorrhagic Escherichia coli strain EDL933 by PsrB, a prophage-encoded AraC-like regulator. Infect Immun. 2015;83(1):346‒353. doi: 10.1128/IAI.02758-14
  • Morgan JK, Carroll RK, Harro CM, et al. Global regulator of virulence a (GrvA) coordinates expression of discrete pathogenic mechanisms in enterohemorrhagic Escherichia coli through interactions with GadW-GadE. J Bacteriol. 2016;198(3):394‒409. doi: 10.1128/JB.00556-15
  • Cordeiro TN, Schmidt H, Madrid C, et al. Indirect DNA readout by an H-NS related protein: Structure of the DNA complex of the C-terminal domain of Ler. PLoS Pathog. 2011;7(11):e1002380. doi: 10.1371/journal.ppat.1002380
  • Elliott SJ, Yu J, Kaper JB, et al. The cloned locus of enterocyte effacement from enterohemorrhagic Escherichia coli O157: H7 is unable to confer the attaching and effacing phenotype upon E. coli K-12. Infect Immun. 1999;67(8):4260‒4263. doi: 10.1128/IAI.67.8.4260-4263.1999
  • McDaniel TK, Kaper JB. A cloned pathogenicity island from enteropathogenic Escherichia coli confers the attaching and effacing phenotype on E. coli K-12. Mol Microbiol. 1997;23(2):399‒407. doi: 10.1046/j.1365-2958.1997.2311591.x
  • Habdas BJ, Smart J, Kaper JB, et al. The LysR-type transcriptional regulator QseD alters type three secretion in enterohemorrhagic Escherichia coli and motility in K-12 Escherichia coli. J Bacteriol. 2010;192(14):3699‒3712. doi: 10.1128/JB.00382-10
  • Maddocks SE, Oyston PCF. Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiol (Reading). 2008;154(12):3609‒3623. doi: 10.1099/mic.0.2008/022772-0
  • Hall BM, Vaughn EE, Begaye AR, et al. Reengineering Cro protein functional specificity with an evolutionary code. J Mol Biol. 2011;413(5):914‒928. doi: 10.1016/j.jmb.2011.08.056
  • Kuper C, Jung K. CadC-mediated activation of the cadBA promoter in Escherichia coli. J Mol Microbiol Biotechnol. 2005;10:26‒39. doi: 10.1159/000090346
  • Tukel C, Akcelik M, de Jong MF, et al. MarT activates expression of the MisL autotransporter protein of Salmonella enterica serotype Typhimurium. J Bacteriol. 2007;189(10):3922‒3926. doi: 10.1128/JB.01746-06
  • Morgan JK, Vendura KW, Stevens SM, et al. RcsB determines the locus of enterocyte effacement (LEE) expression and adherence phenotype of Escherichia coli O157: H7 spinach outbreak strain TW14359 and coordinates bicarbonate-dependent LEE activation with repression of motility. Microbiol (Reading). 2013;159(Pt_11):2342‒2353. doi: 10.1099/mic.0.070201-0
  • Shen S, Mascarenhas M, Morgan R, et al. Identification of four fimbria-encoding genomic islands that are highly specific for verocytotoxin-producing Escherichia coli serotype O157 strains. J Clin Microbiol. 2005;43(8):3840‒3850. doi: 10.1128/JCM.43.8.3840-3850.2005
  • Cooper KK, Mandrell RE, Louie JW, et al. Comparative genomics of enterohemorrhagic Escherichia coli O145: H28 demonstrates a common evolutionary lineage with Escherichia coli O157: H7. BMC Genomics. 2014;15(1):17. doi: 10.1186/1471-2164-15-17
  • Jaureguy F, Landraud L, Passet V, et al. Phylogenetic and genomic diversity of human bacteremic Escherichia coli strains. BMC Genomics. 2008;9(1):560. doi: 10.1186/1471-2164-9-560
  • Lostroh CP, Lee CA. The Salmonella pathogenicity island-1 type III secretion system. Microbes Infect. 2001;3(14–15):1281‒1291. doi: 10.1016/s1286-4579(01)01488-5
  • Baikalov I, Schroder I, Kaczor-Grzeskowiak M, et al. Structure of the Escherichia coli response regulator NarL. Biochemistry. 1996;35(34):11053‒11061. doi: 10.1021/bi960919o
  • Yuan J, Jin F, Glatter T, et al. Osmosensing by the bacterial PhoQ/PhoP two-component system. Proc Natl Acad Sci U S A. 2017;114(50):E10792–E10798. doi: 10.1073/pnas.1717272114
  • Deng W, Puente JL, Gruenheid S, et al. Dissecting virulence: systematic and functional analyses of a pathogenicity island. Proc Natl Acad Sci U S A. 2004;101(10):3597‒3602. doi: 10.1073/pnas.0400326101
  • Iyoda S, Watanabe H. ClpXP protease controls expression of the type III protein secretion system through regulation of RpoS and GrlR levels in enterohemorrhagic Escherichia coli. J Bacteriol. 2005;187(12):4086‒4094. doi: 10.1128/JB.187.12.4086-4094.2005
  • Saitoh T, Iyoda S, Yamamoto S, et al. Transcription of the ehx enterohemolysin gene is positively regulated by GrlA, a global regulator encoded within the locus of enterocyte effacement in enterohemorrhagic Escherichia coli. J Bacteriol. 2008;190(14):4822‒4830. doi: 10.1128/JB.00231-08
  • Jimenez R, Cruz-Migoni SB, Huerta-Saquero A, et al. Molecular characterization of GrlA, a specific positive regulator of ler expression in enteropathogenic Escherichia coli. J Bacteriol. 2010;192(18):4627‒4642. doi: 10.1128/JB.00307-10
  • Lara-Ochoa C, Huerta-Saquero A, Medrano-Lopez A, et al. GrlR, a negative regulator in enteropathogenic E. coli, also represses the expression of LEE virulence genes independently of its interaction with its cognate partner GrlA. Front Microbiol. 2023;14:1063368. doi: 10.3389/fmicb.2023.1063368
  • Gallegos MT, Schleif R, Bairoch A, et al. Arac/XylS family of transcriptional regulators. Microbiol Mol Biol Rev. 1997;61(4):393‒410. doi: 10.1128/mmbr.61.4.393-410.1997
  • Yang J, Hart E, Tauschek M, et al. Bicarbonate-mediated transcriptional activation of divergent operons by the virulence regulatory protein, RegA, from citrobacter rodentium. Mol Microbiol. 2008;68(2):314‒327. doi: 10.1111/j.1365-2958.2008.06171.x
  • Liu R, Ochman H. Stepwise formation of the bacterial flagellar system. Proc Natl Acad Sci U S A. 2007;104(17):7116‒7121. doi: 10.1073/pnas.0700266104
  • Mahajan A, Currie CG, Mackie S, et al. An investigation of the expression and adhesion function of H7 flagella in the interaction of Escherichia coli O157: H7 with bovine intestinal epithelium. Cell Microbiol. 2009;11(1):121‒137. doi: 10.1111/j.1462-5822.2008.01244.x
  • Claret L, Hughes C. Functions of the subunits in the FlhD(2)C(2) transcriptional master regulator of bacterial flagellum biogenesis and swarming. J Mol Biol. 2000;303(4):467‒478. doi: 10.1006/jmbi.2000.4149
  • Liu X, Matsumura P. The FlhD/FlhC complex, a transcriptional activator of the Escherichia coli flagellar class II operons. J Bacteriol. 1994;176(23):7345‒7351. doi: 10.1128/jb.176.23.7345-7351.1994
  • Wang S, Fleming RT, Westbrook EM, et al. Structure of the Escherichia coli FlhDC complex, a prokaryotic heteromeric regulator of transcription. J Mol Biol. 2006;355(4):798‒808. doi: 10.1016/j.jmb.2005.11.020
  • Chevance FF, Hughes KT. Coordinating assembly of a bacterial macromolecular machine. Nat Rev Microbiol. 2008;6(6):455‒465. doi: 10.1038/nrmicro1887
  • Kitagawa R, Takaya A, Yamamoto T. Dual regulatory pathways of flagellar gene expression by ClpXP protease in enterohaemorrhagic Escherichia coli. Microbiol (Reading). 2011;157(11):3094‒3103. doi: 10.1099/mic.0.051151-0
  • Foster JW. Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol. 2004;2(11):898‒907. doi: 10.1038/nrmicro1021
  • Zhao B, Houry WA. Acid stress response in enteropathogenic gammaproteobacteria: an aptitude for survival. This paper is one of a selection of papers published in this special issue entitled “Canadian Society of Biochemistry, molecular & cellular biology 52nd annual meeting — protein folding: principles and diseases” and has undergone the Journal’s usual peer review process. Biochem Cell Biol. 2010;88(2):301–17. doi: 10.1139/o09-182
  • Foster JW. When protons attack: microbial strategies of acid adaptation. Curr Opin Microbiol. 1999;2(2):170‒174. doi: 10.1016/S1369-5274(99)80030-7
  • Castanie-Cornet MP, Penfound TA, Smith D, et al. Control of acid resistance in Escherichia coli. J Bacteriol. 1999;181(11):3525‒3535. doi: 10.1128/JB.181.11.3525-3535.1999
  • Bearson S, Bearson B, Foster JW. Acid stress responses in enterobacteria. FEMS Microbiol Lett. 1997;147(2):173‒180. doi: 10.1111/j.1574-6968.1997.tb10238.x
  • Gajiwala KS, Burley SK. HDEA, a periplasmic protein that supports acid resistance in pathogenic enteric bacteria 1 1Edited by P. E. Wright. J Mol Biol. 2000;295(3):605‒612. doi: 10.1006/jmbi.1999.3347
  • Kern R, Malki A, Abdallah J, et al. Escherichia coli HdeB is an acid stress chaperone. J Bacteriol. 2007;189(2):603‒610. doi: 10.1128/JB.01522-06
  • McClure PJ, Hall S. Survival of Escherichia coli in foods. Symp Ser Soc Appl Microbiol. 2000;88(S1):61S‒70S. doi: 10.1111/j.1365-2672.2000.tb05333.x
  • Dong T, Schellhorn HE. Global effect of RpoS on gene expression in pathogenic Escherichia coli O157: H7 strain EDL933. BMC Genomics. 2009;10(1):349. doi: 10.1186/1471-2164-10-349
  • Flockhart AF Analysis of O-island deletions in Escherichia coli O157:H7. Thesis presented for the degree of Doctor of Philosophy. 2012.
  • Dos Santos GF, de Sousa FG, Beier SL, et al. Escherichia coli O157: H7 strains in bovine carcasses and the impact on the animal production chain. Braz J Microbiol. 2023;54(3):2243‒2251. doi: 10.1007/s42770-023-01034-x
  • Hall G, Kurosawa S, Stearns-Kurosawa DJ. Shiga toxin therapeutics: beyond neutralization. Toxins (Basel). 2017;9(9):291. doi: 10.3390/toxins9090291
  • Shimizu T, Ohta Y, Tsutsuki H, et al. Construction of a novel bioluminescent reporter system for investigating shiga toxin expression of enterohemorrhagic Escherichia coli. Gene. 2011;478(1–2):1‒10. doi: 10.1016/j.gene.2011.01.006
  • Detzner J, Pohlentz G, Muthing J. Enterohemorrhagic Escherichia coli and a fresh view on shiga toxin-binding glycosphingolipids of primary human kidney and colon epithelial cells and their toxin susceptibility. Int J Mol Sci. 2022;23(13):6884. doi: 10.3390/ijms23136884
  • Minadakis G, Spyrou GM. A systems bioinformatics approach to interconnect biological pathways. Methods Mol Biol. 2021;2189:231‒249. doi: 10.1007/978-1-0716-0822-7_17
  • Low AS, Holden N, Rosser T, et al. Analysis of fimbrial gene clusters and their expression in enterohaemorrhagic Escherichia coli O157: H7. Environ Microbiol. 2006;8(6):1033‒1047. doi: 10.1111/j.1462-2920.2006.00995.x