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PMID: 2680979 Published · ppublish English Journal Article

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.

Infection and immunity ·Vol. 57 ·No. 12 ·1989-12-00 ·Pages 3727-34

Neeser JR, Chambaz A, Golliard M, Link-Amster H, Fryder V, Kolodziejczyk E

Abstract

Enterotoxigenic Escherichia coli are the most common cause of travelers' and infant diarrhea in less-developed countries. In the present work, among several metabolically labeled human diarrheagenic E. coli strains, enterotoxigenic strains expressing colonization factor antigen II were shown to bind to HT-29 intestinal cell monolayers when these cells were grown in conditions promoting their enterocytic differentiation. Indirect immunofluorescence with fimbrial antisera revealed that pathogen attachment was associated with the production of a specific bacterial adhesin, the E. coli surface antigen CS3. Scanning and transmission electron micrographs showed an apical pattern of colonization, characteristic of enterotoxigenic E. coli infections. The above data were consistent with all observations previously made with human enterocytes obtained from intestinal biopsies. The lectin-carbohydrate nature of this cell-cell recognition mechanism was also established. Bacterial binding to differentiated HT-29 cells was inhibited by a mixture of newborn meconium glycopeptides. By coating the cell layers with the plant agglutinin from Evonymus europaea, pathogen attachment was also prevented. Binding of 125I-labeled CS3 adhesin and E. europaea agglutinin to brush border membrane proteins separated by sodium dodecyl sulfate-polyacrylamide gel electrophoresis and transferred to nitrocellulose revealed three bands of about 30, 20, and 13 kilodaltons, which acted as receptors for both bacterial and plant lectins. These data suggest that the sugar units to which the bacterial colonization factor CS3 binds are synthesized as carbohydrate chains of three brush border membrane glycoproteins in HT-29 cells by a differentiation-specific pathway.

MeSH Terms
Antigens, Bacterial Bacterial Adhesion Colon/cytology,microbiology Diarrhea/microbiology Enterotoxins/biosynthesis Escherichia coli/cytology Fimbriae Proteins Fluorescent Antibody Technique Humans In Vitro Techniques Intestinal Mucosa/microbiology Meconium/metabolism,microbiology Membrane Glycoproteins/metabolism Microscopy, Electron Microvilli/microbiology Molecular Weight Receptors, Immunologic/metabolism Tumor Cells, Cultured
Chemicals
Antigens, Bacterial Enterotoxins Membrane Glycoproteins Receptors, Immunologic bacterial adhesin receptor colonization factor antigens Fimbriae Proteins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Neeser J R
Nestlé Research Centre, Nestec Limited, Lausanne, Switzerland.
Chambaz A
Golliard M
Link-Amster H
Fryder V
Kolodziejczyk E
References (38)
38 references, click to expand
  1. 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):638-47 PMID: 80383
  2. Role of Escherichia coli colonisation factor antigen in acute diarrhoea.
    Lancet. 1978 Jul 22;2(8082):181-4 PMID: 78384
  3. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  4. Dissociation and reassembly of Escherichia coli type 1 pili.
    J Bacteriol. 1981 Oct;148(1):308-14 PMID: 6116696
  5. Properties of pili from Escherichia coli SS142 that mediate mannose-resistant adhesion to mammalian cells.
    J Bacteriol. 1983 Feb;153(2):1038-44 PMID: 6130060
  6. Immunochemical studies on the combining sites of Forssman hapten reactive hemagglutinins from Dolichos biflorus, Helix pomatia, and Wistaria floribunda.
    Biochemistry. 1983 May 24;22(11):2741-50 PMID: 6603233
  7. 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):2822-9 PMID: 3117693
  8. The processing of asparagine-linked oligosaccharides in HT-29 cells is a function of their state of enterocytic differentiation. An accumulation of Man9,8-GlcNAc2-Asn species is indicative of an impaired N-glycan trimming in undifferentiated cells.
    J Biol Chem. 1988 May 5;263(13):6031-7 PMID: 3360773
  9. Attachment of Escherichia coli via mannose- or Gal alpha 1----4Gal beta-containing receptors to human colonic epithelial cells.
    Infect Immun. 1988 Oct;56(10):2531-7 PMID: 2901402
  10. 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):1290-8 PMID: 2647635
  11. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy.
    J Cell Biol. 1963 Apr;17:208-12 PMID: 13986422
  12. Novel fucolipids accumulating in human adenocarcinoma. I. Glycolipids with di- or trifucosylated type 2 chain.
    J Biol Chem. 1984 Apr 10;259(7):4672-80 PMID: 6707026
  13. Novel fucolipids accumulating in human adenocarcinoma. II. Selective isolation of hybridoma antibodies that differentially recognize mono-, di-, and trifucosylated type 2 chain.
    J Biol Chem. 1984 Apr 10;259(7):4681-5 PMID: 6200484
  14. Coli surface antigens 1 and 3 of colonization factor antigen II-positive enterotoxigenic Escherichia coli: morphology, purification, and immune responses in humans.
    Infect Immun. 1984 May;44(2):409-20 PMID: 6370866
  15. In vitro adhesion of enterotoxigenic Escherichia coli to human intestinal epithelial cells from mucosal biopsies.
    Infect Immun. 1984 May;44(2):514-8 PMID: 6370868
  16. Ultrastructural study of adhesion of enterotoxigenic Escherichia coli to erythrocytes and human intestinal epithelial cells.
    Infect Immun. 1984 May;44(2):519-27 PMID: 6143731
  17. The intracellular accumulation of UDP-N-acetylhexosamines is concomitant with the inability of human colon cancer cells to differentiate.
    J Biol Chem. 1985 Jan 10;260(1):139-46 PMID: 3965444
  18. Enterocytic differentiation of a subpopulation of the human colon tumor cell line HT-29 selected for growth in sugar-free medium and its inhibition by glucose.
    J Cell Physiol. 1985 Jan;122(1):21-9 PMID: 3880764
  19. A quantitative determination by capillary gas-liquid chromatography of neutral and amino sugars (as O-methyloxime acetates), and a study on hydrolytic conditions for glycoproteins and polysaccharides in order to increase sugar recoveries.
    Anal Biochem. 1984 Oct;142(1):58-67 PMID: 6517320
  20. Structural analysis of the O-glycosidically linked core-region oligosaccharides of human meconium glycoproteins which express oncofoetal antigens.
    Eur J Biochem. 1985 Apr 15;148(2):367-77 PMID: 2580706
  21. Adhesion of enterotoxigenic Escherichia coli to human small intestinal enterocytes.
    Infect Immun. 1985 Jun;48(3):824-31 PMID: 2860070
  22. Fimbrial adhesions of Escherichia coli.
    Rev Infect Dis. 1985 May-Jun;7(3):321-40 PMID: 2862689
  23. G.l.c. of O-methyloxime and alditol acetate derivatives of neutral sugars, hexosamines, and sialic acids: "one-pot" quantitative determination of the carbohydrate constituents of glycoproteins and a study of the selectivity of alkaline borohydride reductions.
    Carbohydr Res. 1985 May 15;138(2):189-98 PMID: 4028042
  24. Oligomannoside-type glycopeptides inhibiting adhesion of Escherichia coli strains mediated by type 1 pili: preparation of potent inhibitors from plant glycoproteins.
    Infect Immun. 1986 May;52(2):428-36 PMID: 2870987
  25. Immunochemical studies on the interaction between synthetic glycoconjugates and alpha-L-fucosyl binding lectins.
    Biochemistry. 1986 May 20;25(10):2829-38 PMID: 3718924
  26. Chronic diarrhea in travelers: diagnostic and therapeutic considerations.
    Rev Infect Dis. 1986 May-Jun;8 Suppl 2:S223-6 PMID: 3523719
  27. Novel fucolipids of human adenocarcinoma: characterization of the major Ley antigen of human adenocarcinoma as trifucosylnonaosyl Ley glycolipid (III3FucV3FucVI2FucnLc6).
    J Biol Chem. 1986 Aug 25;261(24):11247-53 PMID: 3733752
  28. Escherichia coli that cause diarrhea: enterotoxigenic, enteropathogenic, enteroinvasive, enterohemorrhagic, and enteroadherent.
    J Infect Dis. 1987 Mar;155(3):377-89 PMID: 3543152
  29. A and H blood group antigens as markers of sucrase-isomaltase from the enterocyte-like differentiated human colon carcinoma cell lines HT-29 and Caco-2.
    Cancer Res. 1987 Mar 1;47(5):1426-33 PMID: 2434217
  30. The posttranslational processing of sucrase-isomaltase in HT-29 cells is a function of their state of enterocytic differentiation.
    J Cell Biol. 1987 May;104(5):1199-205 PMID: 3553207
  31. A one-step ultramicro method for the assay of intestinal disaccharidases.
    Anal Biochem. 1966 Mar;14(3):376-92 PMID: 5944942
  32. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  33. The sialic acids. XI. A periodate-resorcinol method for the quantitative estimation of free sialic acids and their glycosides.
    J Biol Chem. 1971 Jan 25;246(2):430-5 PMID: 5542012
  34. Plasmid-controlled colonization factor associated with virulence in Esherichia coli enterotoxigenic for humans.
    Infect Immun. 1975 Sep;12(3):656-67 PMID: 1100526
  35. Detection of the K99 antigen by means of agglutination and immunoelectrophoresis in Escherichia coli isolates from calves and its correlation with entertoxigenicity.
    Infect Immun. 1976 May;13(5):1369-77 PMID: 773832
  36. Hemagglutination of human group A erythrocytes by enterotoxigenic Escherichia coli isolated from adults with diarrhea: correlation with colonization factor.
    Infect Immun. 1977 Nov;18(2):330-7 PMID: 336541
  37. How bacteria stick.
    Sci Am. 1978 Jan;238(1):86-95 PMID: 635520
  38. Purification and characterization of the CFA/I antigen of enterotoxigenic Escherichia coli.
    Infect Immun. 1979 Aug;25(2):738-48 PMID: 39896
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
1989-12-00
Pages
3727-34
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC259897
Subset
IM
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