Aggregative adherence fimbriae contribute to the inflammatory response of epithelial cells infected with enteroaggregative Escherichia coli

Cellular Microbiology

Volumn 7, Issue 11, 2005, Pages 1565-1578

  Harrington, Susan M ^a   Strauman, Maura C ^a   Abe, Cecilia M ^b,d   Nataro, James P ^a,c  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^c University of Maryland School of Medicine Center for Vaccine Development   (United States)

^d UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; COMPLEMENTARY DNA; FLAGELLIN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; INTERLEUKIN 8; STROMAL CELL DERIVED FACTOR 1; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIUM MUTANT; CELL CULTURE; CELL STRAIN HT29; CONTROLLED STUDY; CYTOKINE PRODUCTION; DNA MICROARRAY; EPITHELIUM CELL; ESCHERICHIA COLI; FIMBRIA; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INFLAMMATION; INTESTINE EPITHELIUM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; VERNER MORRISON SYNDROME;

ADHESINS, ESCHERICHIA COLI; BACTERIAL ADHESION; CELL POLARITY; CYTOKINES; EPITHELIAL CELLS; ESCHERICHIA COLI; FIMBRIAE, BACTERIAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; INTESTINES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 27244433581     PISSN: 14625814     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2005.00588.x     Document Type: Article

References (59)

1. Bambou, J., Giraud, A., Menard, S., Begue, B., Rakotobe, S., Heyman, M., et al. (2004) In vitro and ex vivo activation of the TLR5 signaling pathway in intestinal epithelial cells by a commensal Escherichia coli strain. J Biol Chem 279: 42984-42992.
2. Berin, M.C., Darfeuille-Michaud, A., Egan, L.J., Miyamoto, Y., and Kagnoff, M.F. (2002) Role of EHEC O157: H7 virulence factors in the activation of intestinal epithelial cell NF-κB and MAP kinase pathways and the up-regulated expression of interleukin-8. Cell Microbiol 4: 635-647.
3. Bernier, C., and Le Bouguenec, C.C. (2002) The AggB and Agg3B proteins produced by enteroaggregative Escherichia coli are two distinct invasins of the AfaD family. In ASM 102nd General Meeting. American Society for Microbiology, Salt Lake City, UT, Abstract B-189, p. 64.
4. Bernier, C., Gounon, P., and Le Bouguenec, C. (2002) Identification of an aggregative adhesion fimbriae (AAF) type III-encoding operon in enteroaggregataive Escherichia coli as a sensitive probe for detecting the AAF-encoding operon family. Infect Immun 70: 4302-4311.
5. Betis, F., Brest, P., Hofman, V., Guignot, J., Bernet-Camard, M., Rossi, B., et al. (2003) The Afa/Dr adhesins of diffusely adhering Escherichia coli stimulate interleukin-8 secretion, activate mitogen-activated protein kinases, and promote polymorphonuclear transepithelial migration in T84 polarized epithelial cells. Infect Immun 71: 1068-1074.
6. Bhan, M.K., Raj, P., Levine, M.M., Kaper, J.B., Bhandari, N., Srivastava, R., et al. (1989) Enteroaggregative Escherichia coli associated with persistent diarrhea in a cohort of rural children in India. J Infect Dis 159: 1061-1064.
7. Bouckenooghe, A.R., Dupont, H.L., Jiang, Z.D., Adachi, J., Mathewson, J.J., Verenkar, M.P., et al. (2000) Markers of enteric inflammation in enteroaggregative Escherichia coli diarrhea in travelers. Am J Trop Med Hyg 62: 711-713.
8. Cario, E., Rosenberg, I.M., Brandwein, S.L., Beck, P.L., Reinecker, H., and Podolsky, D.K. (2000) Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing toll-like receptors. J Immunol 164: 966-972.
9. Cobeljic, M., Miljkovic-Selimovic, B., Paunovic-Todosijevic, D., Velickovic, Z., Lepsanovic, Z., Zec, N., et al. (1996) Enteroaggregative Escherichia coli associated with an outbreak of diarrhoea in a neonatal nursery ward. Epidemiol Infect 117: 11-16.
10. Cota, E., Chen, H.A., Anderson, K.L., Simpson, P., Du Merle, L., Bernier-Febreau, C., et al. (2004) Complete resonance assignments of the 'donor-strand complemented' AfaD: the afimbrial invasin from Diffusely Adherent E. coli. J Biomol NMR 29: 411-412.
11. Czeczulin, J.R., Balepur, S., Hicks, S., Phillips, A., Hall, R., Kothary, M.H., et al. (1997) Aggregative adherence fimbria II, a second fimbrial antigen mediating aggregative adherence in enteroaggregative Escherichia coli. Infect Immun 65: 4135-4145.
12. Donnelly, M.A., and Steiner, T.S. (2002) Two nonadjacent regions in enteroaggregative Escherichia coli flagellin are required for activation of Toll-like receptor 5. J Biol Chem 43: 40456-40461.
13. Eaves-Pyles, T., Murthy, K., Liaudet, L., Virag, L., Ross, G., Soriano, F.G., et al. (2001) Flagellin, a novel mediator of Salmonella-induced epithelial activation and systemic inflammation: IKBα degradation, induction of nitric oxide synthase, induction of proinflammatory mediators, and cardiovascular dysfunction. J Immunol 166: 1248-1260.
14. Eitel, J., Heise, T., Thiesen, U., and Dersch, P. (2005) Cell invasion and IL-8 production pathways initiated by YadA of Yersinia pseudotuberculosis require common signalling molecules (FAK, c-Src, Ras) and distinct cell factors. Cell Microbiol 7: 63-77.
15. Elias, W.P., JrCzeczulin, J.R. Henderson, I.R. Trabulsi, L.R., and Nataro, J.P. (1999) Organization of biogenesis genes for aggregative adherence fimbria II defines a virulence gene cluster in enteroaggregative Escherichia coli. J Bacteriol 181: 1779-1785.
16. Frendeus, B. Wachtler, C. Hedlund, M. Fischer, H. Samuelsson, P. Svensson, M., and Svanborg, C. (2001) Escherichia coli P fimbriae utilize the Toll-like receptor 4 pathway for cell activation. Mol Microbiol 40: 37-51.
17. Gascon, J. Vargas, M. Quinto, L. Corachan, M. Jimenez de Anta, M.T., and Vila, J. (1998) Enteroaggregative Escherichia coli strains as a cause of traveler's diarrhea: a case-control study. J Infect Dis 177: 1409-1412.
18. Germani, Y. Minsssart, P. Vohito, M. Yassibanda, S. Glaziou, P. Hocquet, D., et al. (1998) Etiologies of acute, persistent, and dysenteric diarrheas in adults in Bangui, Central African Republic, in relation to human immunodeficiency virus serostatus. Am J Trop Med Hyg 59: 1008-1014.
19. Gewirtz, A.T., Navas, T.A., Lyons, S., Godowski, P.J., and Madara, J.L. (2001a) Cutting Edge: Bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 167: 1882-1885.
20. Gewirtz, A.T., Simon, P.O., Schmitt, C.K., Taylor, L.J., Hagedorn, C.H., O'Brien, A.D., et al. (2001b) Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J Clin Invest 107: 99-109.
21. Greenberg, D.E., Jiang, Z., Steffen, R., Verenker, M.P., and DuPont, H.L. (2002) Markers of inflammation in bacterial diarrhea among travelers, with a focus on enteroaggregative Escherichia coli pathogenicity. J Infect Dis 185: 944-949.
22. Hayashi, F., Smith, K.D., Ozinsky, A., Hawn, T.R., Yi, E.C., Goodlett, D.R., et al. (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410: 1099-1103.
23. Hedlund, M., Frendeus, B., Wachtler, C., Hang, L., Fischer, H., and Svanborg, C. (2001) Type 1 fimbriae deliver an LPS- and TLR4-dependent activation signal to CD14-negative cells. Mol Microbiol 39: 542-552.
24. Henderson, I.R., Hicks, S., Navarro-Garcia, F., Elias, W.P., Philips, A.D., and Nataro, J.P. (1999) Involvement of the enteroaggregative Escherichia coli plasmid-encoded toxin in causing human intestinal damage. Infect Immun 67: 5338-5344.
25. Hobert, M.E., Sands, K.A., Mrsny, R.J., and Madara, J.L. (2002) Cdc42 and Rac1 regulate late events in Salmonella typhimurium-induced interleukin-8 secretion from polarized epithelial cells. J Biol Chem 277: 51025-51032.
26. Huang, D.B., and Dupont, H.L. (2004) Enteroaggregative Escherichia coli: an emerging pathogen in children. Semin Pediatr Infect Dis 15: 266-271.
27. Huang, D.B., DuPont, H.L., Jiang, Z., Carlin, L., and Okhuysen, P.C. (2004) Interleukin-8 response in an intestinal HCT-8 cell line infected with enteroaggregative and enterotoxigenic Escherichia coli. Clin Diagn Lab Immunol 11: 548-551.
28. Huet, C., Sahuquillo-Merino, C., Coudrier, E., and Louvard, D. (1987) Absorptive and mucus-secreting subclones isolated from a multipotent intestinal cell line (HT-29) provide new models for cell polarity and terminal differentiation. J Cell Biol 105: 345-357.
29. Huppertz, H., Rutkowski, S., Aleksic, S., and Karch, H. (1997) Acute and chronic diarrhoea and abdominal colic associated with enteroaggregative Escherichia coli in young children living in western Europe. Lancet 349: 1660-1662.
30. Jiang, Z., Greenberg, D., Nataro, J.P., Steffen, R., and DuPont, H.L. (2002) Rate of occurrence and pathogenic effect of enteroaggregative Escherichia coli virulence factors in international travelers. J Clin Microbiol 40: 4185-4190.
31. Jung, H.C., Eckmann, L., Yang, S., Panja, A., Fierer, J., Morzycka-Wroblewska, E., and Kagnoff, M.F. (1995) A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J Clin Invest 95: 55-65.
32. Khan, M.A.S., Kang, J., and Steiner, T.S. (2004) Enteroaggregative Escherichia coli flagellin-induced interleukin-8 secretion requires Toll-like receptor 5-dependent p38 MAP kinase activation. Immunology 112: 651-660.
33. Lencer, W.I., Strohmeier, G., Moe, S., and Carlson, S.L. (1995) Signal transduction by cholera toxin subunits across model human intestinal epithelia. Am J Physiol 269: G542-G557.
34. Levine, M.M., Bergquist, E.J., Nalin, D.R., Waterman, D.H., Hornick, R.B., Young, C.R., et al. (1978) Escherichia coli strains that cause diarrhea but do not produce heat-labile or heat-stable enterotoxins and are non-invasive. Lancet 1: 1119-1122.
35. Levine, S.J., Larivee, P., Logun, C., Angus, C.W., Ognibee, F.P., and Shelhamer, J.H. (1995) Tumor necrosis factor-alpha induces mucin hypersecretion and MUC-2 gene expression by human airway epithelial cells. Am J Respir Cell Mol Biol 12: 196-204.
36. Lyons, S., Wang, L., Casanova, J., Sitaraman, S., Merlin, D., and Gewirtz, A. (2004) Salmonella typhimurium transcytoses flagellin via an SPI2-mediated vesicular transport pathway. J Cell Sci 117: 5771-5780.
37. McCormick, B.A. (2003) The use of transepithelial models to examine host-pathogen interactions. Curr Opin Microbiol 6: 77-81.
38. Muza-Moons, M.M., Koutsouris, A., and Hecht, G. (2003) Disruption of cell polarity by enteropathogenic Escherichia coli enables basolateral membrane proteins to migrate apically and to potentiate physiological consequences. Infect Immun 71: 7069-7078.
39. Nataro, J.P., Deng, Y., Maneval, D.R., German, A.L., Martin, W.C., and Levine, M.M. (1992) Aggregative adherence fimbriae I of enteroaggregative Escherichia coli mediate adherence to HEp-2 cells and hemagglutination of human erythrocytes. Infect Immun 60: 2297-2304.
40. Nataro, J.P., Yikang, D., Yingkang, D., and Walker, K. (1994) AggR, a transcriptional activator of aggregative adherence fimbria I expression in enteroaggregative Escherichia coli. J Bacteriol 176: 4691-4699.
41. Nataro, J.P., Yikang, D., Cookson, S., Cravioto, A., Savarino, S.J., Guers, L.D., et al. (1995) Heterogeneity of enteroaggregative Escherichia coli virulence demonstrated in volunteers. J Infect Dis 171: 465-468.
42. Nataro, J.P., Hicks, S., Phillips, A.D., Vial, P.A., and Sears, C.L. (1996) T84 cells in culture as a model for enteroaggregative Escherichia coli pathogenesis. Infect Immun 64: 4761-4768.
43. Nishi, J., Sheikh, J., Mizuguchi, K., Luisi, B., Burland, V., Boutin, A., et al. (2003) The export of coat protein from enteroaggregative Escherichia coli by a specific ATP-binding cassette transporter system. J Biol Chem 278: 45680-45689.
44. Pabst, W.L., Altwegg, M., Kind, C., Mirjanic, S., Hardegger, D., and Nadal, D. (2003) Prevalence of enteroaggregative Escherichia coli among children with and without diarrhea in Switzerland. J Clin Microbiol 41: 2289-2293.
45. Plancon, L., du Merle, L., Le Friec, S., Gounon, P., Jouve, M., Guignot, J., et al. (2003) Recognition of the cellular β1-chain integrin by the bacterial AfaD invasin is implicated in the internalization of afa-expressing pathogenic Escherichia coli strains. Cell Microbiol 5: 681-693.
46. Rakeman, J.L., Bonifield, H.R., and Miller, S.I. (1999) A HilA-independent pathway to Salmonella typhimurium invasion gene transcription. J Bacteriol 181: 3096-3104.
47. Savarino, S.J., Fasano, A., Robertson, D.C., and Levine, M.M. (1991) Enteroaggregative Escherichia coli elaborate a heat-stable enterotoxin demonstrable in an in vitro rabbit intestinal model. J Clin Invest 87: 1450-1455.
48. Shazberg, G., Wolk, M., Schmidt, H., Sechter, I., Gottesman, G., and Miron, D. (2003) Enteroaggregative Escherichia coli serotype O126: H27, Israel. Emerg Infect Dis 9: 1170-1173.
49. Sheikh, J., Hicks, S., Dall'Agnol, M., Phillips, A.D., and Nataro, J.P. (2001) Roles for Fis and YafK in biofilm formation by enteroaggregative Escherichia coli. Mol Microbiol 41: 1-16.
50. Sheikh, J., Czeczulin, J.R., Harrington, S., Hicks, S., Henderson, I.R., Le Bouguenec, C., et al. (2002) A novel dispersin protein in enteroaggregative Escherichia coli. J Clin Invest 110: 1329-1337.
51. Sierro, F., Dubois, B., Coste, A., Kaiserlian, D., Kraehenbuhl, J., and Sirard, J. (2001) Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells. Proc Natl Acad Sci USA 98: 13722-13727.
52. Smith, K.D., Andersen-Nissen, E., Hayashi, F., Strobe, K., Bergman, M.A., Rassoulian Barrett, S.L., et al. (2003) Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat Immunol 4: 1247-1253.
53. Sokolova, O., Heppel, N., Jagerhuber, R., Kim, K.S., Frosch, M., Eigenthaler, M., and Schubert-Unkmeir, A. (2004) Interaction of Neisseria meningitidis with human brain microvascular endothelial cells: role of MAP- and tyrosine kinases in invasion and inflammatory cytokine release. Cell Microbiol 6: 1153-1166.
54. Steiner, T.S., Lima, A.A.M., Nataro, J.P., and Guerrant, R.L. (1998) Enteroaggregative Escherichia coli produce intestinal inflammation and growth impairment and cause interleukin-8 release from intestinal epithelial cells. J Infect Dis 177: 88-96.
55. Steiner, T.S., Nataro, J.P., Poteet-Smith, C.E., Smith, J.A., and Guerrant, R.L. (2000) Enteroaggregative Escherichia coli expresses a novel flagellin that causes IL-8 release from intestinal epithelial cells. J Clin invest 105: 1769-1777.
56. Vargas, M., Gascon, J., Gallardo, F., Jimenez deAnta, M.T., and Vila, J. (1998) Prevalence of diarrheagenic Escherichia coli strains detected by PCR in patients with travelers' diarrhea. Clin Microbiol Infect 4: 682-688.
57. Wanke, C.A., Schorling, J.B., Barrett, L.J., Desouza, M.A., and Guerrant, R.L. (1991) Potential role of adherence traits of Escherichia coli in persistent diarrhea in an urban Brazilian slum. Pediatr Infect Dis J 10: 746-751.
58. Zeng, H., Carlson, A.Q., Guo, Y., Yu, Y., Collier-Hyams, J.L., Madara, J.L., et al. (2003) Flagellin is the major proinflammatory determinant of enteropathogenic Salmonella. J Immunol 171: 3668-3674.
59. Zhou, X., Giron, J.A., Torres, A.G., Crawford, J.A., Negrete, E., Vogel, S.N., and Kaper, J.B. (2003) Flagellin of enteropathogenic Escherichia coli stimulates interleukin-8 production in T84 cells. Infect Immun 71: 2120-2129.