Intimate Adherence by Enteropathogenic Escherichia coli Modulates TLR5 Localization and Proinflammatory Host Response in Intestinal Epithelial Cells

Scandinavian Journal of Immunology

Volumn 73, Issue 4, 2011, Pages 268-283

  Salazar Gonzalez, H ^a   Navarro Garcia, F ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

FLAGELLIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 8; INTIMIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; TOLL LIKE RECEPTOR 5; TUMOR NECROSIS FACTOR ALPHA; VIRULENCE FACTOR;

ARTICLE; BACTERIUM ADHERENCE; CELLULAR DISTRIBUTION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENTEROPATHOGENIC ESCHERICHIA COLI; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; INFLAMMATION; INTESTINE EPITHELIUM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ADHESINS, BACTERIAL; BACTERIAL ADHESION; BACTERIAL SECRETION SYSTEMS; CELL MEMBRANE; ENTEROPATHOGENIC ESCHERICHIA COLI; EPITHELIAL CELLS; ESCHERICHIA COLI PROTEINS; FLAGELLIN; GENE EXPRESSION; GENE KNOCKOUT TECHNIQUES; HT29 CELLS; HUMANS; I-KAPPA B PROTEINS; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-8; INTESTINES; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NF-KAPPA B; PHOSPHORYLATION; PROTEIN TRANSPORT; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTOR 5; TUMOR NECROSIS FACTOR-ALPHA; VIRULENCE FACTORS;

EID: 79952049457     PISSN: 03009475     EISSN: 13653083     Source Type: Journal    
DOI: 10.1111/j.1365-3083.2011.02507.x     Document Type: Article

References (56)

1. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol 2004;2:123-40.
2. Staley TE, Jones EW, Corley LD. Attachment and penetration of Escherichia coli into intestinal epithelium of the ileum in newborn pigs. Am J Pathol 1969;56:371-92.
3. Donnenberg MS, Kaper JB. Enteropathogenic Escherichia coli. Infect Immun 1992;60:3953-61.
4. Nougayrede JP, Fernandes PJ, Donnenberg MS. Adhesion of enteropathogenic Escherichia coli to host cells. Cell Microbiol 2003;5:359-72.
5. Cornelis GR. The type III secretion injectisome. Nat Rev Microbiol 2006;4:811-25.
6. Garmendia J, Frankel G, Crepin VF. Enteropathogenic and enterohemorrhagic Escherichia coli infections: translocation, translocation, translocation. Infect Immun 2005;73:2573-85.
7. 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;71:3310-9.
8. 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;17:2166-76.
9. 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;91:511-20.
10. Kenny B, Finlay BB. Intimin-dependent binding of enteropathogenic Escherichia coli to host cells triggers novel signaling events, including tyrosine phosphorylation of phospholipase C-gamma1. Infect Immun 1997;65:2528-36.
11. Hecht G. Microbes and microbial toxins: paradigms for microbial-mucosal interactions. VII. Enteropathogenic Escherichia coli: physiological alterations from an extracellular position. Am J Physiol Gastrointest Liver Physiol 2001;281:G1-7.
12. Kagnoff MF. Microbial-epithelial cell crosstalk during inflammation: the host response. Ann N Y Acad Sci 2006;1072:313-20.
13. Moon HW, Whipp SC, Argenzio RA, Levine MM, Giannella RA. Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines. Infect Immun 1983;41:1340-51.
14. Polotsky YE, Dragunskaya EM, Seliverstova VG et al. Pathogenic effect of enterotoxigenic Escherichia coli and Escherichia coli causing infantile diarrhoea. Acta Microbiol Acad Sci Hung 1977;24:221-36.
15. Tzipori S, Gibson R, Montanaro J. Nature and distribution of mucosal lesions associated with enteropathogenic and enterohemorrhagic Escherichia coli in piglets and the role of plasmid-mediated factors. Infect Immun 1989;57:1142-50.
16. Tzipori S, Montanaro J, Robins-Browne RM, Vial P, Gibson R, Levine MM. Studies with enteroaggregative Escherichia coli in the gnotobiotic piglet gastroenteritis model. Infect Immun 1992;60:5302-6.
17. Nataro JP, Kaper JB. Diarrheagenic Escherichia coli. Clin Microbiol Rev 1998;11:142-201.
18. Giannella RA. Importance of the intestinal inflammatory reaction in Salmonella-mediated intestinal secretion. Infect Immun 1979;23:140-5.
19. Perdomo OJ, Cavaillon JM, Huerre M, Ohayon H, Gounon P, Sansonetti PJ. Acute inflammation causes epithelial invasion and mucosal destruction in experimental shigellosis. J Exp Med 1994;180:1307-19.
20. Philpott DJ, Edgeworth JD, Sansonetti PJ. The pathogenesis of Shigella flexneri infection: lessons from in vitro and in vivo studies. Philos Trans R Soc Lond B Biol Sci 2000;355:575-86.
21. Wassef JS, Keren DF, Mailloux JL. Role of M cells in initial antigen uptake and in ulcer formation in the rabbit intestinal loop model of shigellosis. Infect Immun 1989;57:858-63.
22. Griffin PM, Olmstead LC, Petras RE. Escherichia coli O157:H7-associated colitis. A clinical and histological study of 11 cases. Gastroenterology 1990;99:142-9.
23. Mullin JM, Agostino N, Rendon-Huerta E, Thornton JJ. Keynote review: epithelial and endothelial barriers in human disease. Drug Discov Today 2005;10:395-408.
24. Zhou X, Giron JA, Torres AG et al. Flagellin of enteropathogenic Escherichia coli stimulates interleukin-8 production in T84 cells. Infect Immun 2003;71:2120-9.
25. Khan MA, Bouzari S, Ma C et al. Flagellin-dependent and -independent inflammatory responses following infection by enteropathogenic Escherichia coli and Citrobacter rodentium. Infect Immun 2008;76:1410-22.
26. Hayashi F, Smith KD, Ozinsky A et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 2001;410:1099-103.
27. Savkovic SD, Koutsouris A, Hecht G. Activation of NF-kappaB in intestinal epithelial cells by enteropathogenic Escherichia coli. Am J Physiol 1997;273:C1160-7.
28. Savkovic SD, Ramaswamy A, Koutsouris A, Hecht G. EPEC-activated ERK1/2 participate in inflammatory response but not tight junction barrier disruption. Am J Physiol Gastrointest Liver Physiol 2001;281:G890-8.
29. Czerucka D, Dahan S, Mograbi B, Rossi B, Rampal P. Implication of mitogen-activated protein kinases in T84 cell responses to enteropathogenic Escherichia coli infection. Infect Immun 2001;69:1298-305.
30. Dong C, Davis RJ, Flavell RA. MAP kinases in the immune response. Annu Rev Immunol 2002;20:55-72.
31. Bonizzi G, Karin M. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol 2004;25:280-8.
32. Savkovic SD, Koutsouris A, Hecht G. Attachment of a noninvasive enteric pathogen, enteropathogenic Escherichia coli, to cultured human intestinal epithelial monolayers induces transmigration of neutrophils. Infect Immun 1996;64:4480-7.
33. Ramirez K, Huerta R, Oswald E, Garcia-Tovar C, Hernandez JM, Navarro-Garcia F. Role of EspA and intimin in expression of proinflammatory cytokines from enterocytes and lymphocytes by rabbit enteropathogenic Escherichia coli-infected rabbits. Infect Immun 2005;73:103-13.
34. Oliver-Gonzalez R, Garcia-Tovar C, Juarez-Mosqueda L, Navarro-Garcia F. Infection of rabbit kidney cells (RK13) by enteropathogenic Escherichia coli as a model to study the dynamics of actin cytoskeleton. Can J Microbiol 2008;54:748-57.
35. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 2000;97:6640-5.
36. 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;105:1769-77.
37. Van Weemen BK, Schuurs AH. Immunoassay using antigen-enzyme conjugates. FEBS Lett 1971;15:232-6.
38. Abreu MT, Fukata M, Arditi M. TLR signaling in the gut in health and disease. J Immunol 2005;174:4453-60.
39. Sharma R, Tesfay S, Tomson FL, Kanteti RP, Viswanathan VK, Hecht G. Balance of bacterial pro- and anti-inflammatory mediators dictates net effect of enteropathogenic Escherichia coli on intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 2006;290:G685-94.
40. Milon A, Oswald E, De Rycke J. Rabbit EPEC: a model for the study of enteropathogenic Escherichia coli. Vet Res 1999;30:203-19.
41. Gewirtz AT, Navas TA, Lyons S, Godowski PJ, Madara JL. Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 2001;167:1882-5.
42. Schuller S, Lucas M, Kaper JB, Giron JA, Phillips AD. The ex vivo response of human intestinal mucosa to enteropathogenic Escherichia coli infection. Cell Microbiol 2009;11:521-30.
43. Takeda K, Akira S. Toll-like receptors in innate immunity. Int Immunol 2005;17:1-14.
44. Caron E, Crepin VF, Simpson N, Knutton S, Garmendia J, Frankel G. Subversion of actin dynamics by EPEC and EHEC. Curr Opin Microbiol 2006;9:40-5.
45. Peralta-Ramirez J, Hernandez JM, Manning-Cela R et al. EspF Interacts with nucleation-promoting factors to recruit junctional proteins into pedestals for pedestal maturation and disruption of paracellular permeability. Infect Immun 2008;76:3854-68.
46. Thanabalasuriar A, Koutsouris A, Weflen A, Mimee M, Hecht G, Gruenheid S. The bacterial virulence factor NleA is required for the disruption of intestinal tight junctions by enteropathogenic Escherichia coli. Cell Microbiol 2010;12:31-41.
47. Ferreiro DU, Komives EA. Molecular mechanisms of system control of NF-kappaB signaling by IkappaBalpha. Biochemistry 2010;49:1560-7.
48. Melo AR, Lasunskaia EB, de Almeida CM, Schriefer A, Kipnis TL, Dias da Silva W. Expression of the virulence factor, BfpA, by enteropathogenic Escherichia coli is essential for apoptosis signalling but not for NF-kappaB activation in host cells. Scand J Immunol 2005;61:511-9.
49. Ruchaud-Sparagano MH, Maresca M, Kenny B. Enteropathogenic Escherichia coli (EPEC) inactivate innate immune responses prior to compromising epithelial barrier function. Cell Microbiol 2007;9:1909-21.
50. Miao EA, Alpuche-Aranda CM, Dors M et al. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol 2006;7:569-75.
51. Badea L, Beatson SA, Kaparakis M, Ferrero RL, Hartland EL. Secretion of flagellin by the LEE-encoded type III secretion system of enteropathogenic Escherichia coli. BMC Microbiol 2009;9:30.
52. Boyer HW, Roulland-Dussoix D. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol 1969;41:459-72.
53. 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;1:1119-22.
54. Camguilhem R, Milon A. Biotypes and O serogroups of Escherichia coli involved in intestinal infections of weaned rabbits: clues to diagnosis of pathogenic strains. J Clin Microbiol 1989;27:743-7.
55. Nougayrede JP, Marches O, Boury M et al. The long-term cytoskeletal rearrangement induced by rabbit enteropathogenic Escherichia coli is Esp dependent but intimin independent. Mol Microbiol 1999;31:19-30.
56. Marches O, Ledger TN, Boury M et al. Enteropathogenic and enterohaemorrhagic Escherichia coli deliver a novel effector called Cif, which blocks cell cycle G2/M transition. Mol Microbiol 2003;50:1553-67.