medigraphic.com
Instituto Nacional de Salud Pública

2007, Number 5

<< Back

salud publica mex 2007; 49 (5)

Molecular pathogenesis, epidemiology and diagnosis of enteropathogenic Escherichia coli.

Vidal JE, Canizález-Román A, Gutiérrez-Jiménez J, Navarro-García F

Language: Spanish
References: 100
Page: 376-386
PDF size: 274.37 Kb.


ABSTRACT

Enteropathogenic Escherichia coli (EPEC) is a leading cause of diarrhea in infants less than two years of age in developing countries. To induce diarrhea EPEC uses several virulence factors acting on a still unknown and mysterious mechanism. The hallmark of EPEC infection is a histological intestinal alteration known as the attaching and effacing (A/E) lesion. The bacterium attaches intimately to the enterocyte and induces assembly of cytoskeleton intracellular actin on the cellular surface. Rearrangements of the actin cytoskeleton form a pedestal-like structure where bacterium tightly cups the cells, leading to degeneration of brush border microvilli. Although the mechanism of EPEC-induced pedestal formation has been dissected in detail, the overall mechanism of diarrhea is still obscure. It is believed that EPEC-mediated secretory diarrhea is related to a) intestinal microvilli effacement, b) massive loss of intracellular ions into the intestinal milieu and c) secretion of an EPEC enterotoxin. Epidemiological studies conducted in developing countries have shown that EPEC is one of the main bacteria frequently isolated from children with diarrhea, causing high morbidity and mortality rates. The microbiological diagnosis of EPEC-induced disease is performed with analytic methodologies different from those used by the standard microbiology laboratory, the most relevant being: a) serotypification, b) the adherence assay, c) FAS test, and d) the specific detection of virulence-involved genes (bfpA and eae genes) using molecular biology techniques. The purpose of this review is to update the most recent findings regarding the molecular pathogenesis of EPEC, its epidemiology in Mexico as well as other developing countries, and also the developed methodology for the diagnosis of EPEC infection.


REFERENCES

  1. Winfield MD, Groisman EA. Role of nonhost environments in the lifestyles of Salmonella and Escherichia coli. Appl Environ Microbiol 2003;69(7):3687-3694.

  2. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol 2004;2(2):123-140.

  3. Cravioto A, Vasquez V. Escherichia coli: pathogenic mechanisms and enterohemorrhagic strains. Bol Med Hosp Infant Mex 1988;45(3):196-197.

  4. Clarke SC, Haigh RD, Freestone PP, Williams PH. Virulence of enteropathogenic Escherichia coli, a global pathogen. Clin Microbiol Rev 2003;16(3):365-378.

  5. Nataro JP, Kaper JB. Diarrheagenic Escherichia coli. Clin Microbiol Rev 1998;11(1):142-201.

  6. Senerwa D, Olsvik O, Mutanda LN, Gathuma JM, Wachsmuth K. Colonization of neonates in a nursery ward with enteropathogenic Escherichia coli and correlation to the clinical histories of the children. J Clin Microbiol 1989;27(11):2539-2543.

  7. Senerwa D, Olsvik O, Mutanda LN, et al. Enteropathogenic Escherichia coli serotype O111:HNT isolated from preterm neonates in Nairobi, Kenya. J Clin Microbiol 1989;27(6):1307-1311.

  8. Levine MM, Bergquist EJ, Nalin DR, et al. Escherichia coli strains that cause diarrhoea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet 1978;1(8074):1119-1122.

  9. Donnenberg MS, Kaper JB, Finlay BB. Interactions between enteropathogenic Escherichia coli and host epithelial cells. Trends Microbiol 1997;5(3):109-114.

  10. Celli J, Deng W, Finlay BB. Enteropathogenic Escherichia coli (EPEC) attachment to epithelial cells: exploiting the host cell cytoskeleton from the outside. Cell Microbiol 2000;2(1):1-9.

  11. Finlay BB, Rosenshine I, Donnenberg MS, Kaper JB. Cytoskeletal composition of attaching and effacing lesions associated with enteropathogenic Escherichia coli adherence to HeLa cells. Infect Immun 1992;60(6):2541-2543.

  12. Goosney DL, Gruenheid S, Finlay BB. Gut feelings: enteropathogenic E. coli (EPEC) interactions with the host. Annu Rev Cell Dev Biol 2000;16:173-189.

  13. Giron JA, Ho AS, Schoolnik GK. An inducible bundle-forming pilus of enteropathogenic Escherichia coli. Science 1991;254(5032):710-713.

  14. Nougayrede JP, Fernandes PJ, Donnenberg MS. Adhesion of enteropathogenic Escherichia coli to host cells. Cell Microbiol 2003;5(6):359-372.

  15. Tórres AG, Zhou X, Kaper JB. Adherence of diarrheagenic Escherichia coli strains to epithelial cells. Infect Immun 2005;73(1):18-29.

  16. Ibarra JA, Villalba MI, Puente JL. Identification of the DNA binding sites of PerA, the transcriptional activator of the bfp and per operons in enteropathogenic Escherichia coli. J Bacteriol 2003;185(9):2835-2847.

  17. Donnenberg MS, Giron JA, Nataro JP, Kaper JB. A plasmid-encoded type IV fimbrial gene of enteropathogenic Escherichia coli associated with localized adherence. Mol Microbiol 1992;6(22):3427-3437.

  18. Puente JL, Bieber D, Ramer SW, Murray W, Schoolnik GK. The bundleforming pili of enteropathogenic Escherichia coli: transcriptional regulation by environmental signals. Mol Microbiol 1996;20(1):87-100.

  19. Bieber D, Ramer SW, Wu CY, et al. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli. Science 1998;280(5372):2114-2118.

  20. Giron JA, Torres AG, Freer E, Kaper JB. The flagella of enteropathogenic Escherichia coli mediate adherence to epithelial cells. Mol Microbiol 2002;44(2):361-379.

  21. Garmendia J, Frankel G, Crepin VF. Enteropathogenic and enterohemorrhagic Escherichia coli infections: translocation, translocation, translocation. Infect Immun 2005;73(5):2573-2585.

  22. Jarvis KG, Giron JA, Jerse AE, McDaniel TK, Donnenberg MS, Kaper JB. Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc Natl Acad Sci USA 1995;92(17):7996-8000.

  23. Kenny B, Finlay BB. Protein secretion by enteropathogenic Escherichia coli is essential for transducing signals to epithelial cells. Proc Natl Acad Sci USA 1995;92(17):7991-7995.

  24. DeVinney R, Knoechel DG, Finlay BB. Enteropathogenic Escherichia coli: cellular harassment. Curr Opin Microbiol 1999;2(1):83-88.

  25. Elliott SJ, Wainwright LA, McDaniel TK, et al. The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69. Mol Microbiol 1998;28(1):1-4.

  26. Hueck CJ. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 1998;62(2):379-433.

  27. Gruenheid S, Sekirov I, Thomas NA, et al. Identification and characterization of NleA, a non-LEE-encoded type III translocated virulence factor of enterohaemorrhagic Escherichia coli O157:H7. Mol Microbiol 2004;51(5):1233-1249.

  28. Crepin VF, Prasannan S, Shaw RK, et al. Structural and functional studies of the enteropathogenic Escherichia coli type III needle complex protein EscJ. Mol Microbiol 2005;55(6):1658-1670.

  29. Yip CK, Kimbrough TG, Felise HB, et al. Structural characterization of the molecular platform for type III secretion system assembly. Nature 2005;435(7042):702-707.

  30. Gauthier A, Puente JL, Finlay BB. Secretin of the enteropathogenic Escherichia coli type III secretion system requires components of the type III apparatus for assembly and localization. Infect Immun 2003;71(6):3310-3319.

  31. Hartland EL, Daniell SJ, Delahay RM, et al. The type III protein translocation system of enteropathogenic Escherichia coli involves EspAEspB protein interactions. Mol Microbiol 2000;35(6):1483-1492.

  32. Sekiya K, Ohishi M, Ogino T, Tamano K, Sasakawa C, Abe A. Supermolecular structure of the enteropathogenic Escherichia coli type III secretion system and its direct interaction with the EspA-sheath-like structure. Proc Natl Acad Sci USA 2001;98(20):11638-11643.

  33. Taylor KA, O’Connell CB, Luther PW, Donnenberg MS. The EspB protein of enteropathogenic Escherichia coli is targeted to the cytoplasm of infected HeLa cells. Infect Immun 1998;66(11):5501-5507.

  34. Wolff C, Nisan I, Hanski E, Frankel G, Rosenshine I. Protein translocation into host epithelial cells by infecting enteropathogenic Escherichia coli. Mol Microbiol 1998;28(1):143-155.

  35. Wachter C, Beinke C, Mattes M, Schmidt MA. Insertion of EspD into epithelial target cell membranes by infecting enteropathogenic Escherichia coli. Mol Microbiol 1999;31(6):1695-1707.

  36. Crepin VF, Shaw R, Abe CM, Knutton S, Frankel G. Polarity of enteropathogenic Escherichia coli EspA filament assembly and protein secretion. J Bacteriol 2005;187(8):2881-2889.

  37. Elliott SJ, Krejany EO, Mellies JL, Robins-Browne RM, Sasakawa C, Kaper JB. EspG, a novel type III system-secreted protein from enteropathogenic Escherichia coli with similarities to VirA of Shigella flexneri. Infect Immun 2001;69(6):4027-4033.

  38. Tu X, Nisan I, Yona C, Hanski E, Rosenshine I. EspH, a new cytoskeleton-modulating effector of enterohaemorrhagic and enteropathogenic Escherichia coli. Mol Microbiol 2003;47(3):595-606.

  39. Kanack KJ, Crawford JA, Tatsuno I, Karmali MA, Kaper JB. SepZ/EspZ is secreted and translocated into HeLa cells by the enteropathogenic Escherichia coli type III secretion system. Infect Immun 2005;73(7):4327- 4337.

  40. McNamara BP, Koutsouris A, O’Connell CB, Nougayrede JP, Donnenberg MS, Hecht G. Translocated EspF protein from enteropathogenic Escherichia coli disrupts host intestinal barrier function. J Clin Invest 2001;107(5):621-629.

  41. Kenny B, Jepson M. Targeting of an enteropathogenic Escherichia coli (EPEC) effector protein to host mitochondria. Cell Microbiol 2000;2(6):579-590.

  42. Tomson FL, Viswanathan VK, Kanack KJ, et al. Enteropathogenic Escherichia coli EspG disrupts microtubules and in conjunction with Orf3 enhances perturbation of the tight junction barrier. Mol Microbiol 2005;56(2):447-464.

  43. Beutin L, Marches O, Bettelheim KA, et al. HEp-2 cell adherence, actin aggregation, and intimin types of attaching and effacing Escherichia coli strains isolated from healthy infants in Germany and Australia. Infect Immun 2003;71(7):3995-4002.

  44. Marches O, Wiles S, Dziva F, et al. Characterization of two non-locus of enterocyte effacement-encoded type III-translocated effectors, NleC and NleD, in attaching and effacing pathogens. Infect Immun 2005;73(12):8411- 8417.

  45. Viswanathan VK, Lukic S, Koutsouris A, Miao R, Muza MM, Hecht G. Cytokeratin 18 interacts with the enteropathogenic Escherichia coli secreted protein F (EspF) and is redistributed after infection. Cell Microbiol 2004;6(10):987-997.

  46. Matsuzawa T, Kuwae A, Abe A. Enteropathogenic Escherichia coli type III effectors EspG and EspG2 alter epithelial paracellular permeability. Infect Immun 2005;73(10):6283-6289.

  47. Kenny B, Ellis S, Leard AD, Warawa J, Mellor H, Jepson MA. Co-ordinate regulation of distinct host cell signalling pathways by multifunctional enteropathogenic Escherichia coli effector molecules. Mol Microbiol 2002;44(4):1095-1107.

  48. Kenny B, DeVinney R, Stein M, Reinscheid DJ, Frey EA, Finlay BB. Enteropathogenic E. coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 1997;91(4):511-520.

  49. Elliott SJ, Hutcheson SW, Dubois MS, et al. Identification of CesT, a chaperone for the type III secretion of Tir in enteropathogenic Escherichia coli. Mol Microbiol 1999;33(6):1176-1189.

  50. Kenny B. Phosphorylation of tyrosine 474 of the enteropathogenic Escherichia coli (EPEC) Tir receptor molecule is essential for actin nucleating activity and is preceded by additional host modifications. Mol Microbiol 1999;31(4):1229-1241.

  51. Phillips N, Hayward RD, Koronakis V. Phosphorylation of the enteropathogenic E. coli receptor by the Src-family kinase c-Fyn triggers actin pedestal formation. Nat Cell Biol 2004;6(7):618-625.

  52. Lommel S, Benesch S, Rohde M, Wehland J, Rottner K. Enterohaemorrhagic and enteropathogenic Escherichia coli use different mechanisms for actin pedestal formation that converge on N-WASP. Cell Microbiol 2004;6(3):243-254.

  53. Goosney DL, DeVinney R, Pfuetzner RA, Frey EA, Strynadka NC, Finlay BB. Enteropathogenic E. coli translocated intimin receptor, Tir, interacts directly with alpha-actinin. Curr Biol 2000;10(12):735-738.

  54. Canil C, Rosenshine I, Ruschkowski S, Donnenberg MS, Kaper JB, Finlay BB. Enteropathogenic Escherichia coli decreases the transepithelial electrical resistance of polarized epithelial monolayers. Infect Immun 1993;61(7):2755-2762.

  55. Knutton S, Rosenshine I, Pallen MJ, et al. A novel EspA-associated surface organelle of enteropathogenic Escherichia coli involved in protein translocation into epithelial cells. Embo J 1998;17(8):2166-2176.

  56. Stein M, Kenny B, Stein MA, Finlay BB. Characterization of EspC, a 110- kilodalton protein secreted by enteropathogenic Escherichia coli which is homologous to members of the immunoglobulin A protease-like family of secreted proteins. J Bacteriol 1996;178(22):6546-6554.

  57. Collington GK, Booth IW, Donnenberg MS, Kaper JB, Knutton S. Enteropathogenic Escherichia coli virulence genes encoding secreted signalling proteins are essential for modulation of Caco-2 cell electrolyte transport. Infect Immun 1998;66(12):6049-6053.

  58. Collington GK, Booth IW, Knutton S. Rapid modulation of electrolyte transport in Caco-2 cell monolayers by enteropathogenic Escherichia coli (EPEC) infection. Gut 1998;42(2):200-207.

  59. Mellies JL, Navarro-García F, Okeke I, Frederickson J, Nataro JP, Kaper JB. espC pathogenicity island of enteropathogenic Escherichia coli encodes an enterotoxin. Infect Immun 2001;69(1):315-324.

  60. Navarro-García F, Canizález-Román A, Sui BQ, Nataro JP, Azamar Y. The serine protease motif of EspC from enteropathogenic Escherichia coli produces epithelial damage by a mechanism different from that of Pet toxin from enteroaggregative E. coli. Infect Immun 2004;72(6):3609-3621.

  61. Navarro-García F, Sears C, Eslava C, Cravioto A, Nataro JP. Cytoskeletal effects induced by pet, the serine protease enterotoxin of enteroaggregative Escherichia coli. Infect Immun 1999;67(5):2184-2192.

  62. Canizalez-Roman A, Navarro-García F. Fodrin CaM-binding domain cleavage by Pet from enteroaggregative Escherichia coli leads to actin cytoskeletal disruption. Mol Microbiol 2003;48(4):947-958.

  63. Henderson IR, Navarro-García F, Desvaux M, Fernández RC, Ala’Aldeen D. Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev 2004;68(4):692-744.

  64. Dutta PR, Cappello R, Navarro-García F, Nataro JP. Functional comparison of serine protease autotransporters of enterobacteriaceae. Infect Immun 2002;70(12):7105-7113.

  65. Vidal JE, Navarro-García F. Efficient translocation of EspC into epithelial cells depends on enteropathogenic Escherichia coli and host cell contact. Infect Immun 2006;74(4):2293-2303.

  66. McDaniel TK, Jarvis KG, Donnenberg MS, Kaper JB. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci USA 1995;92(5):1664-1668.

  67. Trabulsi LR, Keller R, Tardelli Gomes TA. Typical and atypical enteropathogenic Escherichia coli. Emerg Infect Dis 2002;8(5):508-513.

  68. Giono-Cerezo S, Rodríguez-Ángeles MG, Rodríguez-Cadena MJ, Valdespino-Gómez JL. Identification of enterotoxins and cytotoxins of Escherichia coli by Vero cell culture and solid-phase hybridization (colony blot). Rev Latinoam Microbiol 1994;36(4):231-241.

  69. Rodríguez-Ángeles G. Principal characteristics and diagnosis of the pathogenic groups of Escherichia coli. Salud Publica Mex 2002;44(5):464-475.

  70. Olarte J, Varela G. A complete somatic antigen common to Salmonella adelaide, Escherichia coli-gomez, and Escherichia coli 0111:B4. J Lab Clin Med 1952;40(2):252-254.

  71. Olarte J, Aldama A, Varela G. Epidemiology of infantile diarrhea and enteritis in the mexican republic and in the federal district. Prensa Med Mex 1952;17:168-176.

  72. Olarte J. New method of obtaining samples for coproculture. Bol Med Hosp Infant Mex 1952;9:537-540.

  73. De los Corvera MA, Olarte J, Ruiz Castañeda M. A new medium for the isolation of Brucella and Salmonella by blood culture. Bull World Health Organ 1956;14:797.

  74. Varela G, Aguirre A, Carrillo J. Escherichia coli-gomez nueva especie aislada de un caso mortal de diarrea. Bol Med Hosp Infant Mex 1946;3:3.

  75. Giammanco A, Maggio M, Giammanco G, et al. Characteristics of Escherichia coli strains belonging to enteropathogenic E. coli serogroups isolated in Italy from children with diarrhea. J Clin Microbiol 1996;34(3):689-94.

  76. Campos LC, Franzolin MR, Trabulsi LR. Diarrheagenic Escherichia coli categories among the traditional enteropathogenic E. coli O serogroups-a review. Mem Inst Oswaldo Cruz 2004;99(6):545-552.

  77. Cravioto A, Tello A, Navarro A, et al. Association of Escherichia coli HEp-2 adherence patterns with type and duration of diarrhoea. Lancet 1991;337(8736):262-264.

  78. Cravioto A, Gross RJ, Scotland SM, Rowe B. An adhesive factor found in Escherichia coli belonging to the traditional infantile enteropathogenic serogroups. Microbiology 1979;6:3427-3437.

  79. Scaletsky IC, Silva ML, Trabulsi LR. Distinctive patterns of adherence of enteropathogenic Escherichia coli to HeLa cells. Infect Immun 1984;45(2):534-536.

  80. Scaletsky IC, Milani SR, Trabulsi LR, Travassos LR. Isolation and characterization of the localized adherence factor of enteropathogenic Escherichia coli. Infect Immun 1988;56(11):2979-2983.

  81. Zepeda-Lopez HM, Gonzalez-Lugo GM. Escherichia coli adherence to HEp-2 cells with prefixed cells. J Clin Microbiol 1995;33(5):1414-1417.

  82. Knutton S, Baldwin T, Williams PH, McNeish AS. Actin accumulation at sites of bacterial adhesion to tissue culture cells: basis of a new diagnostic test for enteropathogenic and enterohemorrhagic Escherichia coli. Infect Immun 1989;57(4):1290-1298.

  83. Knutton S, Lloyd DR, McNeish AS. Adhesion of enteropathogenic Escherichia coli to human intestinal enterocytes and cultured human intestinal mucosa. Infect Immun 1987;55(1):69-77.

  84. López-Saucedo C, Cerna JF, Villegas-Sepúlveda N, et al. Single multiplex polymerase chain reaction to detect diverse loci associated with diarrheagenic Escherichia coli. Emerg Infect Dis 2003;9(1):127-131.

  85. Gunzburg ST, Tornieporth NG, Riley LW. Identification of enteropathogenic Escherichia coli by PCR-based detection of the bundleforming pilus gene. J Clin Microbiol 1995;33(5):1375-1377.

  86. Vidal R, Vidal M, Lagos R, Levine M, Prado V. Multiplex PCR for diagnosis of enteric infections associated with diarrheagenic Escherichia coli. J Clin Microbiol 2004;42(4):1787-1789.

  87. Li Y, Liu D, Cao B, et al. Development of a serotype-specific DNA microarray for identification of some Shigella and pathogenic Escherichia coli strains. J Clin Microbiol 2006;44(12):4376-4383.

  88. Ballmer K, Korczak BM, Kuhnert P, Slickers P, Ehricht R, Hachler H. Fast DNA serotyping of Escherichia coli by use of an oligonucleotide microarray. J Clin Microbiol 2007;45(2):370-379.

  89. Levine MM, Ferreccio C, Prado V, et al. Epidemiologic studies of Escherichia coli diarrheal infections in a low socioeconomic level periurban community in Santiago, Chile. Am J Epidemiol 1993;138(10):849-869.

  90. Cravioto A, Reyes RE, Ortega R, Fernández G, Hernández R, López D. Prospective study of diarrhoeal disease in a cohort of rural Mexican children: incidence and isolated pathogens during the first two years of life. Epidemiol Infect 1988;101(1):123-134.

  91. Estrada-García T, Cerna JF, Paheco-Gil L, et al. Drug-resistant diarrheogenic Escherichia coli, Mexico. Emerg Infect Dis 2005;11(8):1306-1308.

  92. Franzolin MR, Alves RC, Keller R, et al. Prevalence of diarrheagenic Escherichia coli in children with diarrhea in Salvador, Bahia, Brazil. Mem Inst Oswaldo Cruz 2005;100(4):359-363.

  93. Flisser A, Velasco-Villa A, Martínez-Campos C, et al. Infectious diseases in Mexico. A survey from 1995-2000. Arch Med Res 2002;33(4):343-350.

  94. Mathewson JJ, Oberhelman RA, Dupont HL, Javier de la Cabada F, Garibay EV. Enteroadherent Escherichia coli as a cause of diarrhea among children in Mexico. J Clin Microbiol 1987;25(10):1917-1919.

  95. Gutiérrez-Jiménez J, Vidal JE, Mejía-Albarrán ME, Resçendiz-Sánchez J, Pérez-Miravete A, Navarro-García F. Prevalencia de patotipos de Escherichia coli diarreogénica en niños del Hospital Infantil de Mexico. Memorias del 34o. Congreso Nacional de Microbiologia, Asociación Mexicana de Microbiología. 2004.

  96. Gomes TA, Blake PA, Trabulsi LR. Prevalence of Escherichia coli strains with localized, diffuse, and aggregative adherence to HeLa cells in infants with diarrhea and matched controls. J Clin Microbiol 1989;27(2):266-269.

  97. Kain KC, Barteluk RL, Kelly MT, et al. Etiology of childhood diarrhea in Beijing, China. J Clin Microbiol 1991;29(1):90-95.

  98. Tornieporth NG, John J, Salgado K, et al. Differentiation of pathogenic Escherichia coli strains in Brazilian children by PCR. J Clin Microbiol 1995;33(5):1371-1374.

  99. Aranda KR, Fabbricotti SH, Fagundes-Neto U, Scaletsky IC. Single multiplex assay to identify simultaneously enteropathogenic, enteroaggregative, enterotoxigenic, enteroinvasive and Shiga toxinproducing Escherichia coli strains in Brazilian children. FEMS Microbiol Lett 2007;267(2):145-150.

  100. Okeke IN, Lamikanra A, Steinruck H, Kaper JB. Characterization of Escherichia coli strains from cases of childhood diarrhea in provincial southwestern Nigeria. J Clin Microbiol 2000;38(1):7-12.




2020     |     www.medigraphic.com