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. 1991 Nov;59(11):4013–4018. doi: 10.1128/iai.59.11.4013-4018.1991

Use of purified F1845 fimbrial adhesin to study localization and expression of receptors for diffusely adhering Escherichia coli during enterocytic differentiation of human colon carcinoma cell lines HT-29 and Caco-2 in culture.

S Kerneis 1, S S Bilge 1, V Fourel 1, G Chauviere 1, M H Coconnier 1, A L Servin 1
PMCID: PMC258990  PMID: 1682255

Abstract

Whole diffusely adhering Escherichia coli (DAEC) C1845 cells bearing the F1845 adhesive factor bind diffusely to differentiated human colon carcinoma cell lines HT-29 and Caco-2. By using antibodies directed against the purified fimbrial adhesin F1845 factor, the expression of the DAEC F1845-specific brush border receptors in the polarized human intestinal HT-29 and Caco-2 epithelial cells was studied by indirect immunofluorescence. A low level of DAEC F1845 receptors in undifferentiated intestinal cells was detected; they were localized in a cluster of cells. DAEC F1845 receptors were expressed at a high level in differentiated HT-29 and Caco-2 cells. DAEC F1845 receptors were expressed at a strikingly high level in the apical domains of the cells and developed during enterocytic differentiation in culture, in parallel with the apical expression of the intestinal brush border hydrolase, sucrase-isomaltase.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Andrade J. R., Da Veiga V. F., De Santa Rosa M. R., Suassuna I. An endocytic process in HEp-2 cells induced by enteropathogenic Escherichia coli. J Med Microbiol. 1989 Jan;28(1):49–57. doi: 10.1099/00222615-28-1-49. [DOI] [PubMed] [Google Scholar]
  2. Benz I., Schmidt M. A. Cloning and expression of an adhesin (AIDA-I) involved in diffuse adherence of enteropathogenic Escherichia coli. Infect Immun. 1989 May;57(5):1506–1511. doi: 10.1128/iai.57.5.1506-1511.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bilge S. S., Clausen C. R., Lau W., Moseley S. L. Molecular characterization of a fimbrial adhesin, F1845, mediating diffuse adherence of diarrhea-associated Escherichia coli to HEp-2 cells. J Bacteriol. 1989 Aug;171(8):4281–4289. doi: 10.1128/jb.171.8.4281-4289.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cheney C. P., Boedeker E. C. Adherence of an enterotoxigenic Escherichia coli strain, serotype O78:H11, to purified human intestinal brush borders. Infect Immun. 1983 Mar;39(3):1280–1284. doi: 10.1128/iai.39.3.1280-1284.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Darfeuille-Michaud A., Aubel D., Chauviere G., Rich C., Bourges M., Servin A., Joly B. Adhesion of enterotoxigenic Escherichia coli to the human colon carcinoma cell line Caco-2 in culture. Infect Immun. 1990 Apr;58(4):893–902. doi: 10.1128/iai.58.4.893-902.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Darfeuille-Michaud A., Forestier C., Joly B., Cluzel R. Identification of a nonfimbrial adhesive factor of an enterotoxigenic Escherichia coli strain. Infect Immun. 1986 May;52(2):468–475. doi: 10.1128/iai.52.2.468-475.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Darfeuille A., Lafeuille B., Joly B., Cluzel R. A new colonization factor antigen (CFA/III) produced by enteropathogenic Escherichia coli O128:B12. Ann Microbiol (Paris) 1983 Jan-Feb;134A(1):53–64. doi: 10.1016/0769-2609(83)90103-5. [DOI] [PubMed] [Google Scholar]
  8. De Graaf F. K., Mooi F. R. The fimbrial adhesins of Escherichia coli. Adv Microb Physiol. 1986;28:65–143. doi: 10.1016/s0065-2911(08)60237-4. [DOI] [PubMed] [Google Scholar]
  9. Donnenberg M. S., Donohue-Rolfe A., Keusch G. T. Epithelial cell invasion: an overlooked property of enteropathogenic Escherichia coli (EPEC) associated with the EPEC adherence factor. J Infect Dis. 1989 Sep;160(3):452–459. doi: 10.1093/infdis/160.3.452. [DOI] [PubMed] [Google Scholar]
  10. Evans D. G., Evans D. J., Jr New surface-associated heat-labile colonization factor antigen (CFA/II) produced by enterotoxigenic Escherichia coli of serogroups O6 and O8. Infect Immun. 1978 Aug;21(2):638–647. doi: 10.1128/iai.21.2.638-647.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Evans D. G., Silver R. P., Evans D. J., Jr, Chase D. G., Gorbach S. L. Plasmid-controlled colonization factor associated with virulence in Esherichia coli enterotoxigenic for humans. Infect Immun. 1975 Sep;12(3):656–667. doi: 10.1128/iai.12.3.656-667.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Finlay B. B., Falkow S. Salmonella interactions with polarized human intestinal Caco-2 epithelial cells. J Infect Dis. 1990 Nov;162(5):1096–1106. doi: 10.1093/infdis/162.5.1096. [DOI] [PubMed] [Google Scholar]
  13. Fogh J., Fogh J. M., Orfeo T. One hundred and twenty-seven cultured human tumor cell lines producing tumors in nude mice. J Natl Cancer Inst. 1977 Jul;59(1):221–226. doi: 10.1093/jnci/59.1.221. [DOI] [PubMed] [Google Scholar]
  14. Gahring L. C., Heffron F., Finlay B. B., Falkow S. Invasion and replication of Salmonella typhimurium in animal cells. Infect Immun. 1990 Feb;58(2):443–448. doi: 10.1128/iai.58.2.443-448.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gaillard J. L., Berche P., Mounier J., Richard S., Sansonetti P. In vitro model of penetration and intracellular growth of Listeria monocytogenes in the human enterocyte-like cell line Caco-2. Infect Immun. 1987 Nov;55(11):2822–2829. doi: 10.1128/iai.55.11.2822-2829.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Girón J. A., Jones T., Millán-Velasco F., Castro-Muñoz E., Zárate L., Fry J., Frankel G., Moseley S. L., Baudry B., Kaper J. B. Diffuse-adhering Escherichia coli (DAEC) as a putative cause of diarrhea in Mayan children in Mexico. J Infect Dis. 1991 Mar;163(3):507–513. doi: 10.1093/infdis/163.3.507. [DOI] [PubMed] [Google Scholar]
  17. Hauri H. P., Sterchi E. E., Bienz D., Fransen J. A., Marxer A. Expression and intracellular transport of microvillus membrane hydrolases in human intestinal epithelial cells. J Cell Biol. 1985 Sep;101(3):838–851. doi: 10.1083/jcb.101.3.838. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Isberg R. R., Leong J. M. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells. Cell. 1990 Mar 9;60(5):861–871. doi: 10.1016/0092-8674(90)90099-z. [DOI] [PubMed] [Google Scholar]
  19. Jerse A. E., Yu J., Tall B. D., Kaper J. B. A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. Proc Natl Acad Sci U S A. 1990 Oct;87(20):7839–7843. doi: 10.1073/pnas.87.20.7839. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Knutton S., Baldwin T., Williams P. H., McNeish A. S. 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 Apr;57(4):1290–1298. doi: 10.1128/iai.57.4.1290-1298.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Knutton S., Lloyd D. R., Candy D. C., McNeish A. S. Ultrastructural study of adhesion of enterotoxigenic Escherichia coli to erythrocytes and human intestinal epithelial cells. Infect Immun. 1984 May;44(2):519–527. doi: 10.1128/iai.44.2.519-527.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Knutton S., Lloyd D. R., McNeish A. S. Adhesion of enteropathogenic Escherichia coli to human intestinal enterocytes and cultured human intestinal mucosa. Infect Immun. 1987 Jan;55(1):69–77. doi: 10.1128/iai.55.1.69-77.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Knutton S., McConnell M. M., Rowe B., McNeish A. S. Adhesion and ultrastructural properties of human enterotoxigenic Escherichia coli producing colonization factor antigens III and IV. Infect Immun. 1989 Nov;57(11):3364–3371. doi: 10.1128/iai.57.11.3364-3371.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mathewson J. J., Cravioto A. HEp-2 cell adherence as an assay for virulence among diarrheagenic Escherichia coli. J Infect Dis. 1989 Jun;159(6):1057–1060. doi: 10.1093/infdis/159.6.1057. [DOI] [PubMed] [Google Scholar]
  25. Miliotis M. D., Koornhof H. J., Phillips J. I. Invasive potential of noncytotoxic enteropathogenic Escherichia coli in an in vitro Henle 407 cell model. Infect Immun. 1989 Jul;57(7):1928–1935. doi: 10.1128/iai.57.7.1928-1935.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mounier J., Ryter A., Coquis-Rondon M., Sansonetti P. J. Intracellular and cell-to-cell spread of Listeria monocytogenes involves interaction with F-actin in the enterocytelike cell line Caco-2. Infect Immun. 1990 Apr;58(4):1048–1058. doi: 10.1128/iai.58.4.1048-1058.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Neeser J. R., Chambaz A., Golliard M., Link-Amster H., Fryder V., Kolodziejczyk E. Adhesion of colonization factor antigen II-positive enterotoxigenic Escherichia coli strains to human enterocytelike differentiated HT-29 cells: a basis for host-pathogen interactions in the gut. Infect Immun. 1989 Dec;57(12):3727–3734. doi: 10.1128/iai.57.12.3727-3734.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Nowicki B., Hull R., Moulds J. Use of the Dr hemagglutinin of uropathogenic Escherichia coli to differentiate normal from abnormal red cells in paroxysmal nocturnal hemoglobinuria. N Engl J Med. 1988 Nov 10;319(19):1289–1290. doi: 10.1056/NEJM198811103191916. [DOI] [PubMed] [Google Scholar]
  29. Nowicki B., Labigne A., Moseley S., Hull R., Hull S., Moulds J. The Dr hemagglutinin, afimbrial adhesins AFA-I and AFA-III, and F1845 fimbriae of uropathogenic and diarrhea-associated Escherichia coli belong to a family of hemagglutinins with Dr receptor recognition. Infect Immun. 1990 Jan;58(1):279–281. doi: 10.1128/iai.58.1.279-281.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nowicki B., Truong L., Moulds J., Hull R. Presence of the Dr receptor in normal human tissues and its possible role in the pathogenesis of ascending urinary tract infection. Am J Pathol. 1988 Oct;133(1):1–4. [PMC free article] [PubMed] [Google Scholar]
  31. Panigrahi P., Tall B. D., Russell R. G., Detolla L. J., Morris J. G., Jr Development of an in vitro model for study of non-O1 Vibrio cholerae virulence using Caco-2 cells. Infect Immun. 1990 Oct;58(10):3415–3424. doi: 10.1128/iai.58.10.3415-3424.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Relman D., Tuomanen E., Falkow S., Golenbock D. T., Saukkonen K., Wright S. D. Recognition of a bacterial adhesion by an integrin: macrophage CR3 (alpha M beta 2, CD11b/CD18) binds filamentous hemagglutinin of Bordetella pertussis. Cell. 1990 Jun 29;61(7):1375–1382. doi: 10.1016/0092-8674(90)90701-f. [DOI] [PubMed] [Google Scholar]
  33. Scaletsky I. C., Milani S. R., Trabulsi L. R., Travassos L. R. Isolation and characterization of the localized adherence factor of enteropathogenic Escherichia coli. Infect Immun. 1988 Nov;56(11):2979–2983. doi: 10.1128/iai.56.11.2979-2983.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Scaletsky I. C., Silva M. L., Trabulsi L. R. Distinctive patterns of adherence of enteropathogenic Escherichia coli to HeLa cells. Infect Immun. 1984 Aug;45(2):534–536. doi: 10.1128/iai.45.2.534-536.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Scotland S. M., Willshaw G. A., Smith H. R., Rowe B. Properties of strains of Escherichia coli O26:H11 in relation to their enteropathogenic or enterohemorrhagic classification. J Infect Dis. 1990 Nov;162(5):1069–1074. doi: 10.1093/infdis/162.5.1069. [DOI] [PubMed] [Google Scholar]
  36. Semenza G. Anchoring and biosynthesis of stalked brush border membrane proteins: glycosidases and peptidases of enterocytes and renal tubuli. Annu Rev Cell Biol. 1986;2:255–313. doi: 10.1146/annurev.cb.02.110186.001351. [DOI] [PubMed] [Google Scholar]
  37. Simons K., Fuller S. D. Cell surface polarity in epithelia. Annu Rev Cell Biol. 1985;1:243–288. doi: 10.1146/annurev.cb.01.110185.001331. [DOI] [PubMed] [Google Scholar]
  38. Toth I., Cohen M. L., Rumschlag H. S., Riley L. W., White E. H., Carr J. H., Bond W. W., Wachsmuth I. K. Influence of the 60-megadalton plasmid on adherence of Escherichia coli O157:H7 and genetic derivatives. Infect Immun. 1990 May;58(5):1223–1231. doi: 10.1128/iai.58.5.1223-1231.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Vial P. A., Robins-Browne R., Lior H., Prado V., Kaper J. B., Nataro J. P., Maneval D., Elsayed A., Levine M. M. Characterization of enteroadherent-aggregative Escherichia coli, a putative agent of diarrheal disease. J Infect Dis. 1988 Jul;158(1):70–79. doi: 10.1093/infdis/158.1.70. [DOI] [PubMed] [Google Scholar]
  40. Wennerås C., Holmgren J., Svennerholm A. M. The binding of colonization factor antigens of enterotoxigenic Escherichia coli to intestinal cell membrane proteins. FEMS Microbiol Lett. 1990 Jan 1;54(1-3):107–112. doi: 10.1016/0378-1097(90)90266-s. [DOI] [PubMed] [Google Scholar]

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