Abstract
Thirteen human bifidobacterial strains were tested for their abilities to adhere to human enterocyte-like Caco-2 cells in culture. The adhering strains were also tested for binding to the mucus produced by the human mucus-secreting HT29-MTX cell line in culture. A high level of calcium-independent adherence was observed for Bifidobacterium breve 4, for Bifidobacterium infantis 1, and for three fresh human isolates from adults. As observed by scanning electron microscopy, adhesion occurs to the apical brush border of the enterocytic Caco-2 cells and to the mucus secreted by the HT29-MTX mucus-secreting cells. The bacteria interacted with the well-defined apical microvilli of Caco-2 cells without cell damage. The adhesion to Caco-2 cells of bifidobacteria did not require calcium and was mediated by a proteinaceous adhesion-promoting factor which was present both in the bacterial whole cells and in the spent supernatant of bifidobacterium culture. This adhesion-promoting factor appeared species specific, as are the adhesion-promoting factors of lactobacilli. We investigated the inhibitory effect of adhering human bifidobacterial strains against intestinal cell monolayer colonization by a variety of diarrheagenic bacteria. B. breve 4, B. infantis 1, and fresh human isolates were shown to inhibit cell association of enterotoxigenic, enteropathogenic, diffusely adhering Escherichia coli and Salmonella typhimurium strains to enterocytic Caco-2 cells in a concentration-dependent manner. Moreover, B. breve 4 and B. infantis 1 strains inhibited, dose dependently, Caco-2 cell invasion by enteropathogenic E. coli, Yersinia pseudotuberculosis, and S. typhimurium strains.
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- 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]
- Blomberg L., Henriksson A., Conway P. L. Inhibition of adhesion of Escherichia coli K88 to piglet ileal mucus by Lactobacillus spp. Appl Environ Microbiol. 1993 Jan;59(1):34–39. doi: 10.1128/aem.59.1.34-39.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bouhnik Y., Pochart P., Marteau P., Arlet G., Goderel I., Rambaud J. C. Fecal recovery in humans of viable Bifidobacterium sp ingested in fermented milk. Gastroenterology. 1992 Mar;102(3):875–878. doi: 10.1016/0016-5085(92)90172-u. [DOI] [PubMed] [Google Scholar]
- Chan R. C., Bruce A. W., Reid G. Adherence of cervical, vaginal and distal urethral normal microbial flora to human uroepithelial cells and the inhibition of adherence of gram-negative uropathogens by competitive exclusion. J Urol. 1984 Mar;131(3):596–601. doi: 10.1016/s0022-5347(17)50512-1. [DOI] [PubMed] [Google Scholar]
- Chan R. C., Reid G., Irvin R. T., Bruce A. W., Costerton J. W. Competitive exclusion of uropathogens from human uroepithelial cells by Lactobacillus whole cells and cell wall fragments. Infect Immun. 1985 Jan;47(1):84–89. doi: 10.1128/iai.47.1.84-89.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chauvière G., Coconnier M. H., Kerneis S., Darfeuille-Michaud A., Joly B., Servin A. L. Competitive exclusion of diarrheagenic Escherichia coli (ETEC) from human enterocyte-like Caco-2 cells by heat-killed Lactobacillus. FEMS Microbiol Lett. 1992 Mar 15;70(3):213–217. doi: 10.1016/0378-1097(92)90700-x. [DOI] [PubMed] [Google Scholar]
- Chauvière G., Coconnier M. H., Kernéis S., Fourniat J., Servin A. L. Adhesion of human Lactobacillus acidophilus strain LB to human enterocyte-like Caco-2 cells. J Gen Microbiol. 1992 Aug;138(Pt 8):1689–1696. doi: 10.1099/00221287-138-8-1689. [DOI] [PubMed] [Google Scholar]
- Coconnier M. H., Klaenhammer T. R., Kernéis S., Bernet M. F., Servin A. L. Protein-mediated adhesion of Lactobacillus acidophilus BG2FO4 on human enterocyte and mucus-secreting cell lines in culture. Appl Environ Microbiol. 1992 Jun;58(6):2034–2039. doi: 10.1128/aem.58.6.2034-2039.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Conway P. L., Gorbach S. L., Goldin B. R. Survival of lactic acid bacteria in the human stomach and adhesion to intestinal cells. J Dairy Sci. 1987 Jan;70(1):1–12. doi: 10.3168/jds.S0022-0302(87)79974-3. [DOI] [PubMed] [Google Scholar]
- 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]
- Darfeuille-Michaud A., Jallat C., Aubel D., Sirot D., Rich C., Sirot J., Joly B. R-plasmid-encoded adhesive factor in Klebsiella pneumoniae strains responsible for human nosocomial infections. Infect Immun. 1992 Jan;60(1):44–55. doi: 10.1128/iai.60.1.44-55.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Evans D. G., Evans D. J., Jr, Clegg S., Pauley J. A. Purification and characterization of the CFA/I antigen of enterotoxigenic Escherichia coli. Infect Immun. 1979 Aug;25(2):738–748. doi: 10.1128/iai.25.2.738-748.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Finlay B. B., Falkow S. Common themes in microbial pathogenicity. Microbiol Rev. 1989 Jun;53(2):210–230. doi: 10.1128/mr.53.2.210-230.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Francis C. L., Jerse A. E., Kaper J. B., Falkow S. Characterization of interactions of enteropathogenic Escherichia coli O127:H6 with mammalian cells in vitro. J Infect Dis. 1991 Oct;164(4):693–703. doi: 10.1093/infdis/164.4.693. [DOI] [PubMed] [Google Scholar]
- Fuller R. Probiotics in human medicine. Gut. 1991 Apr;32(4):439–442. doi: 10.1136/gut.32.4.439. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Goldin B. R., Gorbach S. L., Saxelin M., Barakat S., Gualtieri L., Salminen S. Survival of Lactobacillus species (strain GG) in human gastrointestinal tract. Dig Dis Sci. 1992 Jan;37(1):121–128. doi: 10.1007/BF01308354. [DOI] [PubMed] [Google Scholar]
- Henriksson A., Szewzyk R., Conway P. L. Characteristics of the adhesive determinants of Lactobacillus fermentum 104. Appl Environ Microbiol. 1991 Feb;57(2):499–502. doi: 10.1128/aem.57.2.499-502.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hitchins A. D., McDonough F. E. Prophylactic and therapeutic aspects of fermented milk. Am J Clin Nutr. 1989 Apr;49(4):675–684. doi: 10.1093/ajcn/49.4.675. [DOI] [PubMed] [Google Scholar]
- Isberg R. R., Voorhis D. L., Falkow S. Identification of invasin: a protein that allows enteric bacteria to penetrate cultured mammalian cells. Cell. 1987 Aug 28;50(5):769–778. doi: 10.1016/0092-8674(87)90335-7. [DOI] [PubMed] [Google Scholar]
- Isolauri E., Juntunen M., Rautanen T., Sillanaukee P., Koivula T. A human Lactobacillus strain (Lactobacillus casei sp strain GG) promotes recovery from acute diarrhea in children. Pediatrics. 1991 Jul;88(1):90–97. [PubMed] [Google Scholar]
- Itoh K., Freter R. Control of Escherichia coli populations by a combination of indigenous clostridia and lactobacilli in gnotobiotic mice and continuous-flow cultures. Infect Immun. 1989 Feb;57(2):559–565. doi: 10.1128/iai.57.2.559-565.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kerneis S., Bilge S. S., Fourel V., Chauviere G., Coconnier M. H., Servin A. L. 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):4013–4018. doi: 10.1128/iai.59.11.4013-4018.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kernéis S., Chauvière G., Darfeuille-Michaud A., Aubel D., Coconnier M. H., Joly B., Servin A. L. Expression of receptors for enterotoxigenic Escherichia coli during enterocytic differentiation of human polarized intestinal epithelial cells in culture. Infect Immun. 1992 Jul;60(7):2572–2580. doi: 10.1128/iai.60.7.2572-2580.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kleeman E. G., Klaenhammer T. R. Adherence of Lactobacillus species to human fetal intestinal cells. J Dairy Sci. 1982 Nov;65(11):2063–2069. doi: 10.3168/jds.S0022-0302(82)82462-4. [DOI] [PubMed] [Google Scholar]
- Konkel M. E., Mead D. J., Hayes S. F., Cieplak W., Jr Translocation of Campylobacter jejuni across human polarized epithelial cell monolayer cultures. J Infect Dis. 1992 Aug;166(2):308–315. doi: 10.1093/infdis/166.2.308. [DOI] [PubMed] [Google Scholar]
- Lesuffleur T., Barbat A., Dussaulx E., Zweibaum A. 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):6334–6343. [PubMed] [Google Scholar]
- Levine M. M. Escherichia coli that cause diarrhea: enterotoxigenic, enteropathogenic, enteroinvasive, enterohemorrhagic, and enteroadherent. J Infect Dis. 1987 Mar;155(3):377–389. doi: 10.1093/infdis/155.3.377. [DOI] [PubMed] [Google Scholar]
- Mounier J., Vasselon T., Hellio R., Lesourd M., Sansonetti P. J. Shigella flexneri enters human colonic Caco-2 epithelial cells through the basolateral pole. Infect Immun. 1992 Jan;60(1):237–248. doi: 10.1128/iai.60.1.237-248.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- 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]
- Reid G., Bruce A. W., McGroarty J. A., Cheng K. J., Costerton J. W. Is there a role for lactobacilli in prevention of urogenital and intestinal infections? Clin Microbiol Rev. 1990 Oct;3(4):335–344. doi: 10.1128/cmr.3.4.335. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reid G., Cook R. L., Bruce A. W. Examination of strains of lactobacilli for properties that may influence bacterial interference in the urinary tract. J Urol. 1987 Aug;138(2):330–335. doi: 10.1016/s0022-5347(17)43137-5. [DOI] [PubMed] [Google Scholar]
- Simon G. L., Gorbach S. L. The human intestinal microflora. Dig Dis Sci. 1986 Sep;31(9 Suppl):147S–162S. doi: 10.1007/BF01295996. [DOI] [PubMed] [Google Scholar]
- Svensson L., Finlay B. B., Bass D., von Bonsdorff C. H., Greenberg H. B. Symmetric infection of rotavirus on polarized human intestinal epithelial (Caco-2) cells. J Virol. 1991 Aug;65(8):4190–4197. doi: 10.1128/jvi.65.8.4190-4197.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]