3,513
Views
9
CrossRef citations to date
0
Altmetric
Research Paper

Antimicrobial resistance and gene regulation in Enteroaggregative Escherichia coli from Egyptian children with diarrhoea: Similarities and differences

, , , , , , , , , , & ORCID Icon show all
Pages 57-74 | Received 28 Aug 2020, Accepted 01 Dec 2020, Published online: 29 Dec 2020

References

  • Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol. 2004;2(2):123–140.
  • Nataro JP, Mai V, Johnson J, et al. Diarrheagenic Escherichia coli infection in Baltimore, Maryland, and New Haven, Connecticut. Clin Infect Dis. 2006;43:402–407.
  • Wilson A, Evans J, Chart H, et al. Characterisation of strains of enteroaggregative Escherichia coli isolated during the infectious intestinal disease study in England. Eur J Epidemiol. 2001;17(12):1125–1130.
  • Okeke IN, Lamikanra A, Czeczulin J, et al. Heterogeneous virulence of Enteroaggregative Escherichia coli strains isolated from children in Southwest Nigeria. J Infect Dis. 2000;181(1):252–260.
  • Franca FL, Wells TJ, Browning DF, et al. Genotypic and phenotypic characterisation of enteroaggregative Escherichia coli from children in Rio de Janeiro, Brazil. PLoS One. 2013;8:e69971.
  • Adachi JA, Jiang ZD, Mathewson JJ, et al. Enteroaggregative Escherichia coli as a major Etiologic agent in Traveler’s Diarrhea in 3 regions of the world. Clin Infect Dis. 2001;32(12):1706–1709. .
  • Durrer P, Zbinden R, Fleisch F, et al. Intestinal infection due to Enteroaggregative Escherichia coli among human immunodeficiency virus–infected persons. J Infect Dis. 2000;182(5):1540–1544. .
  • Olesen B, Scheutz F, Andersen RL, et al. Enteroaggregative Escherichia coli O78:H10, the cause of an outbreak of urinary tract infection. J Clin Microbiol. 2012;50(11):3703–3711. .
  • Herzog K, Engeler Dusel J, Hugentobler M, et al. Diarrheagenic enteroaggregative Escherichia coli causing urinary tract infection and bacteremia leading to sepsis. Infection. 2014;42(2):441–444. .
  • Harrington SM, Dudley EG, Nataro JP. Pathogenesis of enteroaggregative Escherichia coli infection. FEMS Microbiol Lett. 2006;254(1):12–18.
  • Steiner TS, Lima AA, Nataro JP, et al. Enteroaggregative Escherichia coli produce intestinal inflammation and growth impairment and cause interleukin-8 release from intestinal epithelial cells. J Infect Dis. 1998;177(1):88–96.
  • Itoh Y, Nagano I, Kunishima M, et al. Laboratory investigation of enteroaggregative Escherichia coli O untypeable:H10 associated with a massive outbreak of gastrointestinal illness. J Clin Microbiol. 1997;35(10):2546–2550.
  • Harada T, Hiroi M, Kawamori F, et al. A food poisoning diarrhea outbreak caused by enteroaggregative Escherichia coli serogroup O126: h27in Shizuoka, Japan. Jpn J Infect Dis. 2007;60:154–155.
  • Frank C, Werber D, Cramer JP, et al. Epidemic profile of Shiga-toxin–producing Escherichia coli O104:H4 outbreak in Germany. N Engl J Med. 2011;365(19):1771–1780. .
  • Boisen N, Melton-Celsa AR, Scheutz F, et al. Shiga toxin 2a and Enteroaggregative Escherichia coli – a deadly combination. Gut Microbes. 2015;6(4):272–278.
  • Estrada-Garcia T, Navarro-Garcia F. Enteroaggregative Escherichia coli pathotype: a genetically heterogeneous emerging foodborne enteropathogen. FEMS Immunol Med Microbiol. 2012;66(3):281–298.
  • Henderson IR, Hicks S, Navarro-Garcia F, et al. Involvement of the EnteroaggregativeEscherichia coli plasmid-encoded toxin in causing human intestinal damage. Infect Immun. 1999;67(10):5338–5344.
  • Savarino SJ, Fasano A, Robertson DC, et al. Enteroaggregative Escherichia coli elaborate a heat-stable enterotoxin demonstrable in an in vitro rabbit intestinal model. J Clin Invest. 1991;87(4):1450–1455.
  • Nataro JP, Yikang D, Yingkang D, et al. AggR, a transcriptional activator of aggregative adherence fimbria I expression in enteroaggregative Escherichia coli. J Bacteriol. 1994;176(15):4691–4699.
  • Sarantuya J, Nishi J, Wakimoto N, et al. Typical enteroaggregative Escherichia coli is the most prevalent pathotype among E. coli strains causing diarrhea in Mongolian children. J Clin Microbiol. 2004;42(1):133–139. .
  • Elias WP Jr., Czeczulin JR, Henderson IR, et al. Organization of biogenesis genes for aggregative adherence fimbria II defines a virulence gene cluster in enteroaggregative Escherichia coli. J Bacteriol. 1999;181(6):1779–1785.
  • Sheikh J, Czeczulin JR, Harrington S, et al. A novel dispersin protein in enteroaggregative Escherichia coli. J Clin Invest. 2002;110(9):1329–1337. .
  • Nishi J, Sheikh J, Mizuguchi K, et al. The export of coat protein from Enteroaggregative Escherichia coli by a specific ATP-binding cassette transporter system. J Biol Chem. 2003;278(46):45680–45689. .
  • Morin N, Santiago AE, Ernst RK, et al. Characterization of the AggR regulon in Enteroaggregative Escherichia coli. Infect Immun. 2013;81(1):122–132.
  • Morin N, Tirling C, Ivison SM, et al. Autoactivation of the AggR regulator of enteroaggregative Escherichia coli in vitro and in vivo. FEMS Immunol Med Microbiol. 2010;58(3):344–355.
  • Santiago AE, Ruiz-Perez F, Jo NY, et al. A large family of antivirulence regulators modulates the effects of transcriptional activators in gram-negative pathogenic bacteria. PLoS Pathog. 2014;10:e1004153.
  • Yasir M, Icke C, Abdelwahab R, et al. Organization and architecture of AggR-dependent promoters from enteroaggregative Escherichia coli. Mol Microbiol. 2019;111(2):534–551. .
  • Mickey AS, Nataro JP. Dual function of Aar, a member of the new AraC negative regulator family, in Escherichia coli gene expression. Infect Immun. 2020;88(6). DOI:10.1128/IAI.00100-20
  • Nataro JP, Deng Y, Cookson S, et al. Heterogeneity of enteroaggregative Escherichia coli virulence demonstrated in volunteers. J Infect Dis. 1995;171(2):465–468. .
  • Veilleux S, Holt N, Schultz BD, et al. Escherichia coli EAST1 toxin toxicity of variants 17-2 and O 42. Comp Immunol Microbiol Infect Dis. 2008;31:567–578.
  • Zhang R, Gu DX, Huang YL, et al. Comparative genetic characterization of Enteroaggregative Escherichia coli strains recovered from clinical and non-clinical settings. Sci Rep. 2016;6(1):24321.
  • Guiral E, Mendez-Arancibia E, Soto SM, et al. CTX-M-15–producing Enteroaggregative Escherichia coli as cause of travelers’ Diarrhea. Emerg Infect Dis. 2011;17(10):1950–1953. .
  • Chattaway MA, Jenkins C, Ciesielczuk H, et al. Evidence of evolving Extraintestinal Enteroaggregative Escherichia coli ST38 Clone. Emerg Infect Dis. 2014;20(11):1935–1937. .
  • Ali MM, Ahmed SF, Klena JD, et al. Enteroaggregative Escherichia coli in diarrheic children in Egypt: molecular characterization and antimicrobial susceptibility. J Infect Dev Ctries. 2014;8(05):589–596.
  • Sanders JW, Putnam SD, Gould P, et al. Diarrheal illness among deployed U.S. military personnel during Operation Bright Star 2001–Egypt. Diagn Microbiol Infect Dis. 2005;52(2):85–90. .
  • Riddle MS, Halvorson HA, Shiau D, et al. Acute gastrointestinal infection, respiratory illness, and noncombat injury among US military personnel during Operation Bright Star 2005, in Northern Egypt. J Travel Med. 2007;14(6):392–401. .
  • Meheissen M, Header D, Abdelaty K. Phylogenetic and pathotype analysis of Escherichia coli stool isolates from Egyptian patients with inflammatory bowel disease. Germs. 2019;9(4):172–181.
  • Ahmed SF, Shaheen HI, Abdel-Messih IA, et al. The epidemiological and clinical characteristics of diarrhea associated with enteropathogenic, enteroaggregative and diffuse-adherent Escherichia coli in Egyptian children. J Trop Pediatr. 2014;60(5):397–400. .
  • Sambrook J, Russell DW. Molecular cloning: a laboratory manual. 3rd ed. Cold Spring Harbor, N.Y: Cold Spring Harbor Laboratory Press; 2001.
  • Lodge J, Fear J, Busby S, et al. Broad host range plasmids carrying the Escherichia coli lactose and galactose operons. FEMS Microbiol Lett. 1992;74(2–3):271–276.
  • Islam MS, Bingle LE, Pallen MJ, et al. Organization of the LEE1 operon regulatory region of enterohaemorrhagic Escherichia coli O157: H7 O157:H7 and activation by GrlA. Mol Microbiol. 2011;79(2):468–483.
  • Bauer AW, Kirby WM, Sherris JC, et al. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol. 1966;45:493–496.
  • Clinical_and_Laboratory_Standards_Institute_(CLSI). Performance standards for antimicrobial susceptibility testing; Twenty-Fourth informational supplement, CLSI Document M100-S24, Wayne. 2014;34(1)
  • Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30(15):2114–2120.
  • Wick RR, Judd LM, Gorrie CL, et al. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol. 2017;13(6):e1005595.
  • Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30(14):2068–2069.
  • Rutherford K, Parkhill J, Crook J, et al. Artemis: sequence visualization and annotation. Bioinformatics. 2000;16(10):944–945. .
  • Grant JR, Stothard P. The CGView Server: a comparative genomics tool for circular genomes. Nucleic Acids Res. 2008;36(Web Server):W181–4.
  • Carver TJ, Rutherford KM, Berriman M, et al. ACT: the Artemis Comparison Tool. Bioinformatics. 2005;21(16):3422–3423.
  • Carver T, Thomson N, Bleasby A, et al. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics. 2009;25(1):119–120.
  • Larsen MV, Cosentino S, Rasmussen S, et al. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol. 2012;50(4):1355–1361. .
  • Joensen KG, Tetzschner AM, Iguchi A, et al. Rapid and easy in Silico serotyping of Escherichia coli isolates by use of whole-genome sequencing data. J Clin Microbiol. 2015;53(8):2410–2426.
  • Carattoli A, Zankari E, Garcia-Fernandez A, et al. In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother. 2014;58:3895–3903.
  • Zankari E, Hasman H, Cosentino S, et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012;67:2640–2644.
  • Joensen KG, Scheutz F, Lund O, et al. Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J Clin Microbiol. 2014;52(5):1501–1510. .
  • Zhang Z, Schwartz S, Wagner L, et al. A greedy algorithm for aligning DNA sequences. J Comput Biol. 2000;7(1–2):203–214.
  • Dunne KA, Chaudhuri RR, Rossiter AE, et al. Sequencing a piece of history: complete genome sequence of the original Escherichia coli strain. Microb Genom. 2017;3:mgen000106.
  • Rasko DA, Webster DR, Sahl JW, et al. Origins of the E. coli strain causing an outbreak of Hemolytic–Uremic Syndrome in Germany. N Engl J Med. 2011;365(8):709–717. .
  • Page AJ, Cummins CA, Hunt M, et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics. 2015;31(22):3691–3693. .
  • Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312–1313.
  • Sarkar G, Sommer SS. The “megaprimer” method of site-directed mutagenesis. Biotechniques. 1990;8:404–407.
  • Guzman LM, Belin D, Carson MJ, et al. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol. 1995;177(14):4121–4130.
  • Browning DF, Lee DJ, Wolfe AJ, et al. The Escherichia coli K-12 NarL and NarP proteins insulate the nrf promoter from the effects of integration host factor. J Bacteriol. 2006;188(21):7449–7456.
  • Okeke IN, Wallace-Gadsden F, Simons HR, et al. Multi-locus sequence typing of enteroaggregative Escherichia coli isolates from Nigerian children uncovers multiple lineages. PLoS One. 2010;5(11):e14093. .
  • Nataro JP, Deng Y, Maneval DR, et al. Aggregative adherence fimbriae I of enteroaggregative Escherichia coli mediate adherence to HEp-2 cells and hemagglutination of human erythrocytes. Infect Immun. 1992;60(6):2297–2304.
  • Villa L, Garcia-Fernandez A, Fortini D, et al. Replicon sequence typing of IncF plasmids carrying virulence and resistance determinants. J Antimicrob Chemother. 2010;65(12):2518–2529.
  • Chaudhuri RR, Sebaihia M, Hobman JL, et al. Complete genome sequence and comparative metabolic profiling of the prototypical enteroaggregative Escherichia coli strain 042. PLoS One. 2010;5(1):e8801. .
  • Ho PL, Lo WU, Lai EL, et al. Clonal diversity of CTX-M-producing, multidrug-resistant Escherichia coli from rodents. J Med Microbiol. 2015;64(2):185–190. .
  • Scholz P, Haring V, Wittmann-Liebold B, et al. Complete nucleotide sequence and gene organization of the broad-host-range plasmid RSF1010. Gene. 1989;75:271–288.
  • Timofte D, Maciuca IE, Evans NJ, et al. Detection and molecular characterization of Escherichia coli CTX-M-15 and Klebsiella pneumoniae SHV-12 beta-lactamases from bovine mastitis isolates in the United Kingdom. Antimicrob Agents Chemother. 2014;58(2):789–794. .
  • Zhang L, Lu X, Zong Z. The emergence of blaCTX-M-15-carrying Escherichia coli of ST131 and new sequence types in Western China. Ann Clin Microbiol Antimicrob. 2013;12(1):35.
  • Smet A, Van Nieuwerburgh F, Vandekerckhove TT, et al. Complete nucleotide sequence of CTX-M-15-plasmids from clinical Escherichia coli isolates: insertional events of transposons and insertion sequences. PLoS One. 2010;5(6):e11202. .
  • Santiago AE, Yan MB, Tran M, et al. A large family of anti-activators accompanying XylS/AraC family regulatory proteins. Mol Microbiol. 2016;101:314–332.
  • Jonsson R, Struve C, Boisen N, et al. Novel aggregative adherence fimbria variant of enteroaggregative Escherichia coli. Infect Immun. 2015;83(4):1396–1405. .
  • Boisen N, Struve C, Scheutz F, et al. New adhesin of enteroaggregative Escherichia coli related to the Afa/Dr/AAF family. Infect Immun. 2008;76(7):3281–3292.
  • Fujiyama R, Nishi J, Imuta N, et al. The shf gene of a Shigella flexneri homologue on the virulent plasmid pAA2 of enteroaggregative Escherichia coli 042 is required for firm biofilm formation. Curr Microbiol. 2008;56:474–480.
  • Dudley EG, Thomson NR, Parkhill J, et al. Proteomic and microarray characterization of the AggR regulon identifies a pheU pathogenicity island in enteroaggregative Escherichia coli. Mol Microbiol. 2006;61:1267–1282.
  • Sheikh J, Dudley EG, Sui B, et al. EilA, a HilA-like regulator in enteroaggregative Escherichia coli. Mol Microbiol. 2006;61(2):338–350.
  • Lund P, Tramonti A, De Biase D. Coping with low pH: molecular strategies in neutralophilic bacteria. FEMS Microbiol Rev. 2014;38:1091–1125.
  • Johnson TJ, Wannemuehler YM, Nolan LK. Evolution of the iss gene in Escherichia coli. Appl Environ Microbiol. 2008;74:2360–2369.
  • Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of theEscherichia coli Phylogenetic Group. Appl Environ Microbiol. 2000;66(10):4555–4558.
  • Toma C, Higa N, Iyoda S, et al. The long polar fimbriae genes identified in Shiga toxin-producing Escherichia coli are present in other diarrheagenic E. coli and in the standard E. coli collection of reference (ECOR) strains. Res Microbiol. 2006;157(2):153–161.
  • Benjelloun-Touimi Z, Sansonetti PJ, Parsot C. SepA, the major extracellular protein of Shigella flexneri: autonomous secretion and involvement in tissue invasion. Mol Microbiol. 1995;17(1):123–135.
  • Browning DF, Godfrey RE, Richards KL, et al. Exploitation of the Escherichia coli lac operon promoter for controlled recombinant protein production. Biochem Soc Trans. 2019;47:755–763.
  • Sheikh J, Hicks S, Dall’Agnol M, et al. Roles for Fis and YafK in biofilm formation by enteroaggregative Escherichia coli. Mol Microbiol. 2001;41(5):983–997.
  • Boisen N, Hansen AM, Melton-Celsa AR, et al. The Presence of the pAA Plasmid in the German O104: h4Shiga O104:H4 Shiga Toxin Type 2a (Stx2a)-producing Stx2a)–Producing Enteroaggregative Escherichia coli strain promotes the translocation of Stx2a across an Epithelial cell Monolayer. J Infect Dis. 2014;210(12):1909–1919. .
  • Nataro JP, Kaper JB, Robins-Browne R, et al. Patterns of adherence of diarrheagenic Escherichia coli to HEp-2 cells. Pediatr Infect Dis J. 1987;6(9):829–831.
  • Boisen N, Østerlund MT, Joensen KG, et al. Redefining enteroaggregative Escherichia coli (EAEC): genomic characterization of epidemiological EAEC strains. PLoS Negl Trop Dis. 2020;14(9):e0008613. .
  • Oteo J, Perez-Vazquez M, Campos J. Extended-spectrum [beta]-lactamase β-lactamase producing Escherichia coli: changing epidemiology and clinical impact. Curr Opin Infect Dis. 2010;23(4):320–326.
  • Tooke CL, Hinchliffe P, Bragginton EC, et al. beta-Lactamases and beta-Lactamase Inhibitors in the 21st Century. J Mol Biol. 2019;431(18):3472–3500. .
  • Chetri S, Bhowmik D, Paul D, et al. AcrAB-TolC efflux pump system plays a role in carbapenem non-susceptibility in Escherichia coli. BMC Microbiol. 2019;19:210.
  • Guyer DM, Henderson IR, Nataro JP, et al. Identification of sat, an autotransporter toxin produced by uropathogenic Escherichia coli. Mol Microbiol. 2000;38:53–66.
  • Vial PA, Robins-Browne R, Lior H, et al. Characterization of enteroadherent-aggregative Escherichia coli, a putative agent of diarrheal disease. J Infect Dis. 1988;158(1):70–79.