Have a personal or library account? Click to login
A Mini-Review of Enteroaggregative Escherichia coli with a Specific Target on the Virulence Factors Controlled by the AggR Master Regulator Cover

A Mini-Review of Enteroaggregative Escherichia coli with a Specific Target on the Virulence Factors Controlled by the AggR Master Regulator

Open Access
|Dec 2023

References

  1. Al Safadi R, Abu-Ali GS, Sloup RE, Rudrik JT, Waters CM, Eaton KA, Manning SD. Correlation between in vivo biofilm formation and virulence gene expression in Escherichia coli O104:H4. PLoS One. 2012;7(7):e41628.https://doi.org/10.1371/journal.pone.0041628
  2. Avelino F, Saldaña Z, Islam S, Monteiro-Neto V, Dall’Agnol M, Eslava CA, Girón JA. The majority of enteroaggregative Escherichia coli strains produce the E. coli common pilus when adhering to cultured epithelial cells. Int J Med Microbiol. 2010 Nov;300(7):440-448. https://doi.org/10.1016/j.ijmm.2010.02.002
  3. Belmont-Monroy L, Saitz-Rojas W, Soria-Bustos J, Mickey AS, Sherman NE, Orsburn BC, Ruiz-Perez F, Santiago AE. Characterization of a novel AraC/XylS-regulated family of N-acyltransferases in pathogens of the order Enterobacterales. PLoS Pathog. 2020 Aug; 16(8):e1008776. https://doi.org/10.1371/journal.ppat.1008776
  4. Bernier C, Gounon P, Le Bouguénec C. Identification of an aggregative adhesion fimbria (AAF) type III-encoding operon in ente-roaggregative Escherichia coli as a sensitive probe for detecting the AAF-encoding operon family. Infect Immun. 2002 Aug;70(8): 4302-4311. https://doi.org/10.1128/IAI.70.8.4302-4311.2002
  5. Billane K, Harrison E, Cameron D, Brockhurst MA. Why do plasmids manipulate the expression of bacterial phenotypes? Philos Trans R Soc Lond B Biol Sci. 2022 Jan;377(1842):20200461.https://doi.org/10.1098/rstb.2020.0461
  6. Blanton LV, Wang LT, Hofmann J, DuBow J, Lafrance A, Kwak S, Bowers L, Levine MA, Hale CO, Meneely PM, et al. Aggregative adherence and intestinal colonization by enteroaggregative Escherichia coli are produced by interactions among multiple surface factors. mSphere. 2018 Mar;3(2):e00078-18.https://doi.org/10.1128/mSphere.00078-18
  7. Boisen N, Melton-Celsa AR, Hansen AM, Zangari T, Smith MA, Russo LM, Scheutz F, O’Brien AD, Nataro JP. The role of the AggR regulon in the virulence of the shiga toxin-producing enteroaggrega-tive Escherichia coli epidemic O104:H4 strain in mice. Front Microbiol. 2019 Aug;10:1824. https://doi.org/10.3389/fmicb.2019.01824
  8. Boisen N, Struve C, Scheutz F, Krogfelt KA, Nataro JP. New adhesin of enteroaggregative Escherichia coli related to the Afa/Dr/ AAF family. Infect Immun. 2008 Jul;76(7):3281-3292.https://doi.org/10.1128/IAI.01646-07
  9. Braga RLL, Pereira ACM, Ferreira AF, Rosa ACP, Pereira-Manfro WF. Intracellular persistence of enteroaggregative Escherichia coli induces a proinflammatory cytokines secretion in intestinal epithelial T84 cells. Arq Gastroenterol. 2018 Apr-Jun;55(2):133-137. https://doi.org/10.1590/S0004-2803.201800000-23
  10. Coyne MJ, Comstock LE. Type VI secretion systems and the gut microbiota. Microbiol Spectr. 2019 Mar;7(2):10.1128/microbiolspec. PSIB-0009-2018.https://doi.org/10.1128/microbiolspec.PSIB-0009-2018
  11. Coyne MJ, Roelofs KG, Comstock LE. Type VI secretion systems of human gut Bacteroidales segregate into three genetic architectures, two of which are contained on mobile genetic elements. BMC Genomics. 2016 Jan;17:58.https://doi.org/10.1186/s12864-016-2377-z
  12. Czeczulin JR, Balepur S, Hicks S, Phillips A, Hall R, Kothary MH, Navarro-Garcia F, Nataro JP. Aggregative adherence fimbria II, a second fimbrial antigen mediating aggregative adherence in entero-aggregative Escherichia coli. Infect Immun. 1997 Oct;65(10):4135-4145. https://doi.org/10.1128/iai.65.10.4135-4145.1997
  13. Dudley EG, Thomson NR, Parkhill J, Morin NP, Nataro JP. Pro-teomic and microarray characterization of the AggR regulon identifies a pheU pathogenicity island in enteroaggregative Escherichia coli. Mol Microbiol. 2006 Sep;61(5):1267-1282.https://doi.org/10.1111/j.1365-2958.2006.05281.x
  14. Elias WP Jr, Czeczulin JR, Henderson IR, Trabulsi LR, Nataro JP. Organization of biogenesis genes for aggregative adherence fimbria II defines a virulence gene cluster in enteroaggregative Escherichia coli. J Bacteriol. 1999 Mar;181(6):1779-1785.https://doi.org/10.1128/JB.181.6.1779-1785.1999
  15. Eslava C, Navarro-García F, Czeczulin JR, Henderson IR, Cravioto A, Nataro JP. Pet, an autotransporter enterotoxin from enteroaggregative Escherichia coli. Infect Immun. 1998 Jul;66(7): 3155-3163. https://doi.org/10.1128/IAI.66.7.3155-3163.1998
  16. Farfan MJ, Inman KG, Nataro JP. The major pilin subunit of the AAF/II fimbriae from enteroaggregative Escherichia coli mediates binding to extracellular matrix proteins. Infect Immun. 2008 Oct; 76(10):4378-4384. https://doi.org/10.1128/IAI.00439-08
  17. Flores J, Okhuysen PC. Enteroaggregative Escherichia coli infection. Curr Opin Gastroenterol. 2009 Jan;25(1):8-11.https://doi.org/10.1097/MOG.0b013e32831dac5e
  18. Flores-Sanchez F, Chavez-Dueñas L, Sanchez-Villamil J, Navarro-Garcia F. Pic protein from enteroaggregative E. coli induces different mechanisms for its dual activity as a mucus secretagogue and a mucinase. Front Immunol. 2020 Nov;11:564953.https://doi.org/10.3389/fimmu.2020.564953
  19. Gomes TA, Elias WP, Scaletsky IC, Guth BE, Rodrigues JF, Piazza RM, Ferreira LC, Martinez MB. Diarrheagenic Escherichia coli Braz J Microbiol. 2016 Dec;47(Suppl 1):3-30.https://doi.org/10.1016/j.bjm.2016.10.015
  20. Greenberg DE, Jiang ZD, Steffen R, Verenker MP, DuPont HL. Markers of inflammation in bacterial diarrhea among travelers, with a focus on enteroaggregative Escherichia coli pathogenicity. J Infect Dis. 2002 Apr;185(7):944-949. https://doi.org/10.1086/339617
  21. Harrington SM, Strauman MC, Abe CM, Nataro JP. Aggregative adherence fimbriae contribute to the inflammatory response of epithelial cells infected with enteroaggregative Escherichia coli. Cell Microbiol. 2005 Nov;7(11):1565-1578.https://doi.org/10.1111/j.1462-5822.2005.00588.x
  22. Henderson IR, Czeczulin J, Eslava C, Noriega F, Nataro JP. Characterization of pic, a secreted protease of Shigella flexneri and enteroaggregative Escherichia coli. Infect Immun. 1999 Nov;67(11): 5587-5596. https://doi.org/10.1128/IAI.67.11.5587-5596.1999
  23. Huang DB, Brown EL, DuPont HL, Cerf J, Carlin L, Flores J, et al. Seroprevalence of the enteroaggregative Escherichia coli virulence factor dispersin among USA travellers to Cuernavaca, Mexico: A pilot study. J Med Microbiol 2008;57(Pt 4):476-479.https://doi.org/10.1099/jmm.0.47495-0
  24. Hüttener M, Prieto A, Espelt J, Bernabeu M, Juárez A. Stringent response and AggR-dependent virulence regulation in the enteroag-gregative Escherichia coli strain 042. Front Microbiol. 2018 Apr;9:717. https://doi.org/10.3389/fmicb.2018.00717
  25. Iwashita M, Nishi J, Wakimoto N, Fujiyama R, Yamamoto K, Tokuda K, Manago K, Kawano Y. Role of the carboxy-terminal region of the outer membrane protein AatA in the export of disper-sin from enteroaggregative Escherichia coli. FEMS Microbiol Lett. 2006 Mar;256(2):266-272.https://doi.org/10.1111/j.1574-6968.2006.00123.x
  26. Jenkins C. Enteroaggregative Escherichia coli. Curr Top Microbiol Immunol. 2018;416:27-50. https://doi.org/10.1007/82_2018_105
  27. Johnson TJ, Nolan LK. Pathogenomics of the virulence plasmids of Escherichia coli. Microbiol Mol Biol Rev. 2009 Dec;73(4):750-774. https://doi.org/10.1128/MMBR.00015-09
  28. Jønsson R, Struve C, Boisen N, Mateiu RV, Santiago AE, Jenssen H, Nataro JP, Krogfelt KA. Novel aggregative adherence fimbria variant of enteroaggregative Escherichia coli. Infect Immun. 2015 Apr; 83(4):1396-1405. https://doi.org/10.1128/IAI.02820-14
  29. Jønsson R, Struve C, Boll EJ, Boisen N, Joensen KG, Sørensen CA, Jensen BH, Scheutz F, Jenssen H, Krogfelt KA. A novel pAA virulence plasmid encoding toxins and two distinct variants of the fimbriae of enteroaggregative Escherichia coli. Front Microbiol 2017; 8:263. https://doi.org/10.3389/fmicb.2017.00263
  30. Journet L, Cascales E. The type VI secretion system in Escherichia coli and related species. EcoSal Plus. 2016 May;7(1):10.1128/ecosalplus. ESP-0009-2015. https://doi.org/10.1128/ecosalplus.ESP-0009-2015
  31. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol. 2004 Feb;2(2):123-140.https://doi.org/10.1038/nrmicro818
  32. Kaur P, Chakraborti A, Asea A. Enteroaggregative Escherichia coli: an emerging enteric food borne pathogen. Interdiscip Perspect Infect Dis. 2010;2010:254159. https://doi.org/10.1155/2010/254159
  33. Kislichkina AA, Kartsev NN, Skryabin YP, Sizova AA, Kanashenko ME, Teymurazov MG, Kuzina ES, Bogun AG, Fursova NK, Svetoch EA, et al. Genomic analysis of a hybrid entero-aggregative hemorrhagic Escherichia coli O181:H4 strain causing colitis with hemolytic-uremic syndrome. Antibiotics. 2022 Oct; 11(10):1416. https://doi.org/10.3390/antibiotics11101416
  34. Lima AAM, Medeiros PHQS, Havt A. Enteroaggregative Escherichia coli subclinical and clinical infections. Curr Opin Infect Dis. 2018 Oct; 31(5):433-439. https://doi.org/10.1097/QCO.0000000000000477
  35. Mayer HB, Wanke CA. Enteroaggregative Escherichia coli as a possible cause of diarrhea in an HIV-infected patient. N Engl J Med. 1995 Jan;332(4):273-274.https://doi.org/10.1056/NEJM199501263320417
  36. 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):e00100-20.https://doi.org/10.1128/IAI.00100-20
  37. Modgil V, Mahindroo J, Narayan C, Kalia M, Yousuf M, Shahi V, Koundal M, Chaudhary P, Jain R, Sandha KS, et al. Comparative analysis of virulence determinants, phylogroups, and antibiotic susceptibility patterns of typical versus atypical enteroaggregative E. coli in India. PLoS Negl Trop Dis. 2020 Nov 18;14(11):e0008769. https://doi.org/10.1371/journal.pntd.0008769
  38. Mohamed JA, Huang DB, Jiang ZD, DuPont HL, Nataro JP, Belkind-Gerson J, Okhuysen PC. Association of putative enteroag-gregative Escherichia coli virulence genes and biofilm production in isolates from travelers to developing countries. J Clin Microbiol. 2007 Jan;45(1):121-126. https://doi.org/10.1128/JCM.01128-06
  39. Monteiro BT, Campos LC, Sircili MP, Franzolin MR, Bevilacqua LF, Nataro JP, Elias WP. The dispersin-encoding gene (aap) is not restricted to enteroaggregative Escherichia coli. Diagn Microbiol Infect Dis. 2009 Sep;65(1):81-84.https://doi.org/10.1016/j.diagmicrobio.2009.05.011
  40. Moraes CTP, Longo J, Silva LB, Pimenta DC, Carvalho E, Morone MSLC, da Rós N, Serrano SMT, Santos ACM, Piazza RMF, et al. Surface protein dispersin of enteroaggregative Escherichia coli binds plasminogen that is converted into active plasmin. Front Microbiol. 2020 Jun 18;11:1222. https://doi.org/10.3389/fmicb.2020.01222
  41. Moreira CG, Carneiro SM, Nataro JP, Trabulsi LR, Elias WP. Role of type I fimbriae in the aggregative adhesion pattern of enteroaggre-gative Escherichia coli. FEMS Microbiol Lett. 2003 Sep;226(1):79-85. https://doi.org/10.1016/S0378-1097(03)00561-5
  42. Morin N, Santiago AE, Ernst RK, Guillot SJ, Nataro JP. Characterization of the AggR regulon in enteroaggregative Escherichia coli. Infect Immun. 2013 Jan;81(1):122-32.https://doi.org/10.1128/IAI.00676-12
  43. Morin N, Tirling C, Ivison SM, Kaur AP, Nataro JP, Steiner TS. Autoactivation of the AggR regulator of enteroaggregative Escherichia coli in vitro and in vivo. FEMS Immunol Med Microbiol. 2010 Apr;58(3):344-355.https://doi.org/10.1111/j.1574-695X.2010.00645.x
  44. Mortensen NP, Fowlkes JD, Maggart M, Doktycz MJ, Nataro JP, Drusano G, Allison DP. Effects of sub-minimum inhibitory concentrations of ciprofloxacin on enteroaggregative Escherichia coli and the role of the surface protein dispersin. Int J Antimicrob Agents. 2011 Jul;38(1):27-34. https://doi.org/10.1016/j.ijantimicag.2011.03.011
  45. Nagy A, Xu Y, Bauchan GR, Shelton DR, Nou X. Aggregative adherence fimbriae I (AAF/I) mediate colonization of fresh produce and abiotic surface by Shiga toxigenic enteroaggregative Escherichia coli O104:H4. Int J Food Microbiol. 2016 Jul;229:44-51.https://doi.org/10.1016/j.ijfoodmicro.2016.04.007
  46. Nascimento JAS, Santos FF, Valiatti TB, Santos-Neto JF, M Santos AC, Cayô R, Gales AC, A T Gomes T. Frequency and diversity of hybrid Escherichia coli strains isolated from urinary tract infections. Microorganisms. 2021 Mar;9(4):693.https://doi.org/10.3390/microorganisms9040693
  47. Nataro JP, Deng Y, Cookson S, Cravioto A, Savarino SJ, Guers LD, Levine MM, Tacket CO. Heterogeneity of enteroaggregative Escherichia coli virulence demonstrated in volunteers. J Infect Dis. 1995 Feb; 171(2):465-468. https://doi.org/10.1093/infdis/171.2.465
  48. Nataro JP, Deng Y, Maneval DR, German AL, Martin WC, Levine MM. Aggregative adherence fimbriae I of enteroaggregative Escherichia coli mediate adherence to HEp-2 cells and hemagglutination of human erythrocytes. Infect Immun. 1992 Jun;60(6):2297-2304. https://doi.org/10.1128/iai.60.6.2297-2304.1992
  49. Nataro JP, Kaper JB, Robins-Browne R, Prado V, Vial P, Levine MM. Patterns of adherence of diarrheagenic Escherichia coli to HEp-2 cells. Pediatr Infect Dis J. 1987 Sep;6(9):829-831.https://doi.org/10.1097/00006454-198709000-00008
  50. Nataro JP, Kaper JB. Diarrheagenic Escherichia coli. Clin Microbiol Rev 1998;11(1):142-201.https://doi.org/10.1128/CMR.11.1.142
  51. Nataro JP, Yikang D, Yingkang D, Walker K. AggR, a transcriptional activator of aggregative adherence fimbria I expression in enteroag-gregative Escherichia coli. J Bacteriol. 1994 Aug;176(15):4691-4699. https://doi.org/10.1128/jb.176.15.4691-4699.1994
  52. Nataro JP. Enteroaggregative Escherichia coli pathogenesis. Curr Opin Gastroenterol. 2005 Jan;21(1): 4-8.
  53. Nishi J, Sheikh J, Mizuguchi K, Luisi B, Burland V, Boutin A, Rose DJ, Blattner FR, Nataro JP. The export of coat protein from enteroaggregative Escherichia coli by a specific ATP-binding cassette transporter system. J Biol Chem. 2003 Nov;278(46):45680-45689. https://doi.org/10.1074/jbc.M306413200
  54. Okhuysen PC, Dupont HL. Enteroaggregative Escherichia coli (EAEC): A cause of acute and persistent diarrhea of worldwide importance. J Infect Dis. 2010 Aug;202(4):503-505.https://doi.org/10.1086/654895
  55. Pereira AL, Silva TN, Gomes AC, Araújo AC, Giugliano LG. Diarrhea-associated biofilm formed by enteroaggregative Escherichia coli and aggregative Citrobacter freundii: a consortium mediated by putative F pili. BMC Microbiol. 2010 Feb;10:57.https://doi.org/10.1186/1471-2180-10-57
  56. Petro CD, Duncan JK, Seldina YI, Allué-Guardia A, Eppinger M, Riddle MS, Tribble DR, Johnson RC, Dalgard CL, Sukumar G, et al. Genetic and virulence profiles of enteroaggregative Escherichia coli (EAEC) isolated from deployed military personnel (DMP) with travelers’ diarrhea. Front Cell Infect Microbiol. 2020 May;10:200. https://doi.org/10.3389/fcimb.2020.00200
  57. Rivas ZP, Talbot KM, Merselis LC, McCormack RM, Adkins B, Munson GP. CexE is a coat protein and virulence factor of diar-rheagenic pathogens. Front Microbiol. 2020 Jun;11:1374.https://doi.org/10.3389/fmicb.2020.01374
  58. Rogawski ET, Guerrant RL, Havt A, Lima IFN, Medeiros PHQS, Seidman JC, McCormick BJJ, Babji S, Hariraju D, Bodhidatta L, et al.; MAL-ED Network Investigators. Epidemiology of enteroag-gregative Escherichia coli infections and associated outcomes in the MAL-ED birth cohort. PLoS Negl Trop Dis. 2017 Jul;11(7):e0005798. https://doi.org/10.1371/journal.pntd.0005798
  59. Santiago AE, Ruiz-Perez F, Jo NY, Vijayakumar V, Gong MQ, Nataro JP. A large family of antivirulence regulators modulates the effects of transcriptional activators in Gram-negative pathogenic bacteria. PLoS Pathog. 2014 May;10(5):e1004153.https://doi.org/10.1371/journal.ppat.1004153
  60. Santiago AE, Yan MB, Hazen TH, Sauder B, Meza-Segura M, Rasko DA, Kendall MM, Ruiz-Perez F, Nataro JP. The AraC Negative Regulator family modulates the activity of histone-like proteins in pathogenic bacteria. PLoS Pathog. 2017 Aug;13(8):e1006545. https://doi.org/10.1371/journal.ppat.1006545
  61. Santiago AE, Yan MB, Tran M, Wright N, Luzader DH, Kendall MM, Ruiz-Perez F, Nataro JP. A large family of anti-activators accompanying XylS/AraC family regulatory proteins. Mol Microbiol. 2016 Jul;101(2):314-332. https://doi.org/10.1111/mmi.13392
  62. Savarino SJ, Fasano A, Watson J, Martin BM, Levine MM, Guandalini S, Guerry P. Enteroaggregative Escherichia coli heatstable enterotoxin 1 represents another subfamily of E. coli heat-stable toxin. Proc Natl Acad Sci USA. 1993 Apr 1;90(7):3093-3097.https://doi.org/10.1073/pnas.90.7.3093
  63. Schiebel J, Böhm A, Nitschke J, Burdukiewicz M, Weinreich J, Ali A, Roggenbuck D, Rödiger S, Schierack P. Genotypic and phenotypic characteristics associated with biofilm formation by human clinical Escherichia coli isolates of different pathotypes. Appl Environ Microbiol. 2017 Dec;83(24):e01660-17.https://doi.org/10.1128/AEM.01660-17
  64. Sheikh J, Czeczulin JR, Harrington S, Hicks S, Henderson IR, Le Bouguénec C, Gounon P, Phillips A, Nataro JP. A novel disper-sin protein in enteroaggregative Escherichia coli. J Clin Invest. 2002 Nov;110(9):1329-1337. https://doi.org/10.1172/JCI16172
  65. Sheikh J, Hicks S, Dall’Agnol M, Phillips AD, Nataro JP. Roles for Fis and YafK in biofilm formation by enteroaggregative Escherichia coli. Mol Microbiol. 2001 Sep;41(5):983-997.https://doi.org/10.1046/j.1365-2958.2001.02512.x
  66. Steiner TS, Lima AA, Nataro JP, Guerrant RL. Enteroaggregative Escherichia coli produce intestinal inflammation and growth impairment and cause interleukin-8 release from intestinal epithelial cells. J Infect Dis. 1998 Jan;177(1):88-96. https://doi.org/10.1086/513809
  67. Steiner TS, Nataro JP, Poteet-Smith CE, Smith JA, Guerrant RL. Enteroaggregative Escherichia coli expresses a novel flagellin that causes IL-8 release from intestinal epithelial cells. J Clin Invest. 2000 Jun; 105(12):1769-1777. https://doi.org/10.1172/JCI8892
  68. Velarde JJ, Varney KM, Inman KG, Farfan M, Dudley E, Fletcher J, Weber DJ, Nataro JP. Solution structure of the novel dispersin protein of enteroaggregative Escherichia coli. Mol Microbiol. 2007 Dec; 66(5):1123-1135.https://doi.org/10.1111/j.1365-2958.2007.05985.x
  69. Vial PA, Robins-Browne R, Lior H, Prado V, Kaper JB, Nataro JP, Maneval D, Elsayed A, Levine MM. Characterization of enteroadherent-aggregative Escherichia coli, a putative agent of diarrheal disease. J Infect Dis. 1988 Jul;158(1):70-79.https://doi.org/10.1093/infdis/158.1.70
  70. Weintraub A. Enteroaggregative Escherichia coli: epidemiology, virulence and detection. J Med Microbiol. 2007 Jan;56(1):4-8.https://doi.org/10.1099/jmm.0.46930-0
  71. Yáñez D, Izquierdo M, Ruiz-Perez F, Nataro JP, Girón JA, Vidal RM, Farfan MJ. The role of fibronectin in the adherence and inflammatory response induced by enteroaggregative Escherichia coli on epithelial cells. Front Cell Infect Microbiol. 2016 Dec;6:166.https://doi.org/10.3389/fcimb.2016.00166
  72. Yasir M, Icke C, Abdelwahab R, Haycocks JR, Godfrey RE, Sazinas P, Pallen MJ, Henderson IR, Busby SJW, Browning DF. Organization and architecture of AggR-dependent promoters from enteroaggrega-tive Escherichia coli. Mol Microbiol. 2019 Feb;111(2):534-551.https://doi.org/10.1111/mmi.14172
DOI: https://doi.org/10.33073/pjm-2023-037 | Journal eISSN: 2544-4646 | Journal ISSN: 1733-1331
Language: English
Page range: 347 - 354
Submitted on: Jun 23, 2023
Accepted on: Sep 8, 2023
Published on: Dec 16, 2023
Published by: Polish Society of Microbiologists
In partnership with: Paradigm Publishing Services
Publication frequency: 4 issues per year

© 2023 Jeannett Alejandra Izquierdo-Vega, Rubi Joseline Castillo-Juarez, Manuel Sánchez-Gutiérrez, Miguel A. Ares, Miguel A. De La Cruz, published by Polish Society of Microbiologists
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.