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PMID: 1319401 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Expression of receptors for enterotoxigenic Escherichia coli during enterocytic differentiation of human polarized intestinal epithelial cells in culture.

Infection and immunity ·Vol. 60 ·No. 7 ·1992-07-00 ·Pages 2572-80

Kernéis S, Chauvière G, Darfeuille-Michaud A, Aubel D, Coconnier MH, Joly B, Servin AL

Abstract

To study the expression of human intestinal receptors for enterotoxigenic Escherichia coli (ETEC), the human polarized intestinal epithelial cell line Caco-2 in culture and several subpopulations of HT-29 cells in culture--parental (mainly undifferentiated) HT-29 cells (HT-29 Std), an enterocytelike subpopulation obtained by selection through glucose deprivation (HT-29 Glc-), and an enterocytelike subpopulation obtained by selection through glucose deprivation which maintains its differentiation characteristics when switched back to standard glucose-containing medium (HT-29 Glc-/+)--were used. Since Caco-2 spontaneously differentiated in culture under standard culture conditions (in the presence of glucose) and HT-29 cells were undifferentiated when cultured under standard conditions (HT-29 Std) and differentiated when grown in a glucose-free medium (HT-29 Glc-), we studied the expression of the receptors for colonization factor antigens (CFA) I, II, and III and the 2230 antigen of ETEC in relation to enterocytic differentiation. We provide evidence that expression of ETEC CFA receptors develops in parallel with other differentiation functions of the cultured cells. The expression of ETEC-specific brush border receptors was studied by indirect immunofluorescence using antibodies raised against purified ETEC CFA. No ETEC receptors were detected in HT-29 Std or short-term-cultured Caco-2 cells. However, among the population of HT-29 Std cells, 2 to 4% of the cells were found to bind ETEC, and these cells expressed positive carcinoembryonic antigen immunoreactivity. This indicated that among the population of undifferentiated HT-29 cells, clusters of differentiated cells were present. ETEC CFA receptors were expressed in the apical and basolateral domains of differentiated HT-29 cells, whereas in differentiated Caco-2 cells only apical expression was observed. Both in HT-29 cells (HT-29 Glc-/+) and in Caco-2 cells cultured under standard conditions, ETEC CFA receptors develop as a function of day in culture. This indicated that the expression of the ETEC CFA receptors was a growth-related event. Indeed, ETEC CFA receptors developed in step with the apical expression of differentiation-associated proteins.

MeSH Terms
Antigens, Bacterial/biosynthesis Bacterial Adhesion/immunology Cell Differentiation/immunology Cell Line Epithelium/physiology Fimbriae Proteins Fluorescent Antibody Technique Guanylate Cyclase Humans Intestines/physiology Microscopy, Phase-Contrast Receptors, Cell Surface/biosynthesis Receptors, Enterotoxin Receptors, Guanylate Cyclase-Coupled Receptors, Peptide
Chemicals
Antigens, Bacterial Receptors, Cell Surface Receptors, Peptide colonization factor antigens Fimbriae Proteins Guanylate Cyclase Receptors, Enterotoxin Receptors, Guanylate Cyclase-Coupled
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Kernéis S
Département de Microbiologie et Immunologie, UFR Sciences Pharmaceutiques Paris XI, France.
Chauvière G
Darfeuille-Michaud A
Aubel D
Coconnier M H
Joly B
Servin A L
References (70)
70 references, click to expand
  1. Penetration of human intestinal epithelial cells by Salmonella: molecular cloning and expression of Salmonella typhi invasion determinants in Escherichia coli.
    Proc Natl Acad Sci U S A. 1989 Jul;86(13):5173-7 PMID: 2662196
  2. ZO-1 mRNA and protein expression during tight junction assembly in Caco-2 cells.
    J Cell Biol. 1989 Sep;109(3):1047-56 PMID: 2670954
  3. 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):3727-34 PMID: 2680979
  4. Vectorial targeting of apical and basolateral plasma membrane proteins in a human adenocarcinoma epithelial cell line.
    Proc Natl Acad Sci U S A. 1989 Dec;86(23):9313-7 PMID: 2687880
  5. Effect of glutamine deprivation and glutamate or ammonium chloride addition on growth rate, metabolism and differentiation of human colon cancer cell-line HT29.
    Int J Biochem. 1986;18(3):263-9 PMID: 2869987
  6. The fimbrial adhesins of Escherichia coli.
    Adv Microb Physiol. 1986;28:65-143 PMID: 2880484
  7. Dissection of the asynchronous transport of intestinal microvillar hydrolases to the cell surface.
    J Cell Biol. 1988 Jun;106(6):1853-61 PMID: 2898478
  8. 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
  9. Enterocytic differentiation and glucose utilization in the human colon tumor cell line Caco-2: modulation by forskolin.
    J Cell Physiol. 1985 Jun;123(3):377-85 PMID: 2985631
  10. Biogenesis and intracellular transport of intestinal brush border membrane hydrolases. Use of antibody probes and tissue culture.
    Subcell Biochem. 1988;12:155-219 PMID: 3043766
  11. Genetic determinants of Shigella pathogenicity.
    Annu Rev Microbiol. 1988;42:127-50 PMID: 3059992
  12. 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
  13. Cingulin, a new peripheral component of tight junctions.
    Nature. 1988 May 19;333(6170):272-6 PMID: 3285223
  14. Penetration of Salmonella through a polarized Madin-Darby canine kidney epithelial cell monolayer.
    J Cell Biol. 1988 Jul;107(1):221-30 PMID: 3292541
  15. Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells.
    Cell. 1987 Aug 28;50(5):769-78 PMID: 3304658
  16. 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
  17. Identification of a nonfimbrial adhesive factor of an enterotoxigenic Escherichia coli strain.
    Infect Immun. 1986 May;52(2):468-75 PMID: 3516874
  18. 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 PMID: 3548768
  19. 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. 1987 Jul;105(1):345-57 PMID: 3611191
  20. 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
  21. Expression and intracellular transport of microvillus membrane hydrolases in human intestinal epithelial cells.
    J Cell Biol. 1985 Sep;101(3):838-51 PMID: 3897250
  22. Cell surface polarity in epithelia.
    Annu Rev Cell Biol. 1985;1:243-88 PMID: 3939606
  23. 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
  24. Adherence of an enterotoxigenic Escherichia coli strain, serotype O78:H11, to purified human intestinal brush borders.
    Infect Immun. 1983 Mar;39(3):1280-4 PMID: 6132875
  25. A new colonization factor antigen (CFA/III) produced by enteropathogenic Escherichia coli O128:B12.
    Ann Microbiol (Paris). 1983 Jan-Feb;134A(1):53-64 PMID: 6342499
  26. Bacterial toxins: cellular mechanisms of action.
    Microbiol Rev. 1984 Sep;48(3):199-221 PMID: 6436655
  27. Emergence of permanently differentiated cell clones in a human colonic cancer cell line in culture after treatment with sodium butyrate.
    Cancer Res. 1984 Sep;44(9):3961-9 PMID: 6744312
  28. ["In vitro" study of attachment to human enterocytes in "Escherichia coli" strains isolated from infants with diarrheal disease (author's transl)].
    Ann Microbiol (Paris). 1981 Jul-Aug;132B(1):57-67 PMID: 7030173
  29. 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
  30. One hundred and twenty-seven cultured human tumor cell lines producing tumors in nude mice.
    J Natl Cancer Inst. 1977 Jul;59(1):221-6 PMID: 327080
  31. Plasmid-controlled colonization factor associated with virulence in Esherichia coli enterotoxigenic for humans.
    Infect Immun. 1975 Sep;12(3):656-67 PMID: 1100526
  32. Movement along actin filaments of the perijunctional area and de novo polymerization of cellular actin are required for Shigella flexneri colonization of epithelial Caco-2 cell monolayers.
    Infect Immun. 1992 Mar;60(3):1031-40 PMID: 1541518
  33. Symmetric infection of rotavirus on polarized human intestinal epithelial (Caco-2) cells.
    J Virol. 1991 Aug;65(8):4190-7 PMID: 1649325
  34. Microtubular organization and its involvement in the biogenetic pathways of plasma membrane proteins in Caco-2 intestinal epithelial cells.
    J Cell Biol. 1991 Apr;113(2):275-88 PMID: 1672691
  35. Discrimination between intracellular uptake and surface adhesion of bacterial pathogens.
    Science. 1991 May 17;252(5008):934-8 PMID: 1674624
  36. Binding of Escherichia coli and Salmonella strains to members of the carcinoembryonic antigen family: differential binding inhibition by aromatic alpha-glycosides of mannose.
    Infect Immun. 1991 Jun;59(6):2051-7 PMID: 1674739
  37. Characterization of interactions of enteropathogenic Escherichia coli O127:H6 with mammalian cells in vitro.
    J Infect Dis. 1991 Oct;164(4):693-703 PMID: 1680136
  38. Bacterial adhesion: genetics, biogenesis, and role in pathogenesis of fimbrial adhesins of Escherichia coli.
    Rev Infect Dis. 1991 Jul-Aug;13(4):721-35 PMID: 1681580
  39. 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.
    Infect Immun. 1991 Nov;59(11):4013-8 PMID: 1682255
  40. A sialoglycoprotein complex linked to the microvillus cytoskeleton acts as a receptor for pilus (AF/R1) mediated adhesion of enteropathogenic Escherichia coli (RDEC-1) in rabbit small intestine.
    J Cell Biol. 1991 Nov;115(4):1021-9 PMID: 1683351
  41. Inability of toxin inhibitors to neutralize enhanced toxicity caused by bacteria adherent to tissue culture cells.
    Infect Immun. 1990 Nov;58(11):3737-42 PMID: 1699898
  42. Shigella flexneri enters human colonic Caco-2 epithelial cells through the basolateral pole.
    Infect Immun. 1992 Jan;60(1):237-48 PMID: 1729185
  43. The invasin protein of Yersinia enterocolitica: internalization of invasin-bearing bacteria by eukaryotic cells is associated with reorganization of the cytoskeleton.
    J Cell Biol. 1992 Jan;116(1):197-207 PMID: 1730744
  44. Reovirus 1 and 3 bind and internalise at the apical surface of intestinal epithelial cells.
    Virology. 1991 Sep;184(1):162-9 PMID: 1871963
  45. Bacterial entry into eukaryotic cells.
    Cell. 1991 Jun 28;65(7):1099-102 PMID: 1905978
  46. Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci.
    Cell. 1991 Jun 28;65(7):1127-41 PMID: 1905979
  47. Plasmid and chromosomal elements involved in the pathogenesis of attaching and effacing Escherichia coli.
    Infect Immun. 1991 Nov;59(11):3869-75 PMID: 1937746
  48. A new in vitro model of Entamoeba histolytica adhesion, using the human colon carcinoma cell line Caco-2: scanning electron microscopic study.
    Infect Immun. 1991 Nov;59(11):4142-6 PMID: 1937772
  49. Sexual stage development of cryptosporidia in the Caco-2 cell line.
    Infect Immun. 1991 Dec;59(12):4610-3 PMID: 1937821
  50. Increased growth adaptability to 5-fluorouracil and methotrexate of HT-29 sub-populations selected for their commitment to differentiation.
    Int J Cancer. 1991 Nov 11;49(5):731-7 PMID: 1937959
  51. The binding of colonization factor antigens of enterotoxigenic Escherichia coli to intestinal cell membrane proteins.
    FEMS Microbiol Lett. 1990 Jan 1;54(1-3):107-12 PMID: 1969827
  52. Asexual development of Cryptosporidium parvum within a differentiated human enterocyte cell line.
    Infect Immun. 1991 Jan;59(1):234-9 PMID: 1987037
  53. New adhesive factor (antigen 8786) on a human enterotoxigenic Escherichia coli O117:H4 strain isolated in Africa.
    Infect Immun. 1991 Apr;59(4):1290-9 PMID: 2004811
  54. 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):1048-58 PMID: 2108086
  55. Growth and characterisation of human faecal astrovirus in a continuous cell line.
    Arch Virol. 1990;113(1-2):73-81 PMID: 2117433
  56. A nonvirulent mutant of Listeria monocytogenes does not move intracellularly but still induces polymerization of actin.
    Infect Immun. 1990 Nov;58(11):3477-86 PMID: 2172164
  57. 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):7839-43 PMID: 2172966
  58. Adhesion of enterotoxigenic Escherichia coli to the human colon carcinoma cell line Caco-2 in culture.
    Infect Immun. 1990 Apr;58(4):893-902 PMID: 2180823
  59. Growth adaptation to methotrexate of HT-29 human colon carcinoma cells is associated with their ability to differentiate into columnar absorptive and mucus-secreting cells.
    Cancer Res. 1990 Oct 1;50(19):6334-43 PMID: 2205381
  60. Development of an in vitro model for study of non-O1 Vibrio cholerae virulence using Caco-2 cells.
    Infect Immun. 1990 Oct;58(10):3415-24 PMID: 2205582
  61. Microtubule perturbation retards both the direct and the indirect apical pathway but does not affect sorting of plasma membrane proteins in intestinal epithelial cells (Caco-2).
    EMBO J. 1990 Oct;9(10):3163-70 PMID: 2209541
  62. Salmonella interactions with polarized human intestinal Caco-2 epithelial cells.
    J Infect Dis. 1990 Nov;162(5):1096-106 PMID: 2230236
  63. Sorting of endogenous plasma membrane proteins occurs from two sites in cultured human intestinal epithelial cells (Caco-2).
    Cell. 1990 Feb 9;60(3):429-37 PMID: 2302734
  64. Multiple beta 1 chain integrins are receptors for invasin, a protein that promotes bacterial penetration into mammalian cells.
    Cell. 1990 Mar 9;60(5):861-71 PMID: 2311122
  65. 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):1375-82 PMID: 2364431
  66. Invasion and replication of Salmonella typhimurium in animal cells.
    Infect Immun. 1990 Feb;58(2):443-8 PMID: 2404872
  67. Common themes in microbial pathogenicity.
    Microbiol Rev. 1989 Jun;53(2):210-30 PMID: 2569162
  68. Reversible forskolin-induced impairment of sucrase-isomaltase mRNA levels, biosynthesis, and transport to the brush border membrane in Caco-2 cells.
    J Cell Physiol. 1989 Dec;141(3):627-35 PMID: 2592430
  69. 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
  70. HEp-2 cell adherence as an assay for virulence among diarrheagenic Escherichia coli.
    J Infect Dis. 1989 Jun;159(6):1057-60 PMID: 2656874
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
DOI
10.1128/iai.60.7.2572-2580.1992
Published
1992-07-00
Pages
2572-80
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC257205
Subset
IM
External Links
PubMed source DOI: 10.1128/iai.60.7.2572-2580.1992 PMC Full Text View journal details
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