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Appl Environ Microbiol. 1994 December; 60(12): 4487–4494.
PMCID: PMC202009

Factors involved in adherence of lactobacilli to human Caco-2 cells.


A quantitative assay performed with bacterial cells labelled with [3H]thymidine was used to investigate factors involved in the adherence of human isolates Lactobacillus acidophilus BG2FO4 and NCFM/N2 and Lactobacillus gasseri ADH to human Caco-2 intestinal cells. For all three strains, adherence was concentration dependent, greater at acidic pH values, and significantly greater than adherence of a control dairy isolate, Lactobacillus delbrueckii subsp. bulgaricus 1489. Adherence of L. acidophilus BG2FO4 and NCFM/N2 was decreased by protease treatment of the bacterial cells, whereas adherence of L. gasseri ADH either was not affected or was enhanced by protease treatment. Putative surface layer proteins were identified on L. acidophilus BG2FO4 and NCFM/N2 cells but were not involved in adherence. Periodate oxidation of bacterial cell surface carbohydrates significantly reduced adherence of L. gasseri ADH, moderately reduced adherence of L. acidophilus BG2FO4, and had no effect on adherence of L. acidophilus NCFM/N2. These results indicate that Lactobacillus species adhere to human intestinal cells via mechanisms which involve different combinations of carbohydrate and protein factors on the bacterial cell surface. The involvement of a secreted bridging protein, which has been proposed as the primary mediator of adherence of L. acidophilus BG2FO4 in spent culture supernatant (M.-H. Coconnier, T. R. Klaenhammer, S. Kernéis, M.-F. Bernet, and A. L. Servin, Appl. Environ. Microbiol. 58:2034-2039, 1992), was not confirmed in this study. Rather, a pH effect on Caco-2 cells contributed significantly to the adherence of this strain in spent culture supernatant.(ABSTRACT TRUNCATED AT 250 WORDS)

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  • Barefoot SF, Klaenhammer TR. Detection and activity of lactacin B, a bacteriocin produced by Lactobacillus acidophilus. Appl Environ Microbiol. 1983 Jun;45(6):1808–1815. [PMC free article] [PubMed]
  • Bernet MF, Brassart D, Neeser JR, Servin AL. Adhesion of human bifidobacterial strains to cultured human intestinal epithelial cells and inhibition of enteropathogen-cell interactions. Appl Environ Microbiol. 1993 Dec;59(12):4121–4128. [PMC free article] [PubMed]
  • Boot HJ, Kolen CP, van Noort JM, Pouwels PH. S-layer protein of Lactobacillus acidophilus ATCC 4356: purification, expression in Escherichia coli, and nucleotide sequence of the corresponding gene. J Bacteriol. 1993 Oct;175(19):6089–6096. [PMC free article] [PubMed]
  • Brooker BE, Fuller R. Adhesion of Lactobacilli to the chicken crop epithelium. J Ultrastruct Res. 1975 Jul;52(1):21–31. [PubMed]
  • Chan RC, Reid G, Irvin RT, Bruce AW, Costerton JW. Competitive exclusion of uropathogens from human uroepithelial cells by Lactobacillus whole cells and cell wall fragments. Infect Immun. 1985 Jan;47(1):84–89. [PMC free article] [PubMed]
  • Chauvière G, Coconnier MH, Kerneis S, Darfeuille-Michaud A, Joly B, Servin AL. 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. [PubMed]
  • Chauvière G, Coconnier MH, Kernéis S, Fourniat J, Servin AL. Adhesion of human Lactobacillus acidophilus strain LB to human enterocyte-like Caco-2 cells. J Gen Microbiol. 1992 Aug;138(Pt 8):1689–1696. [PubMed]
  • Coconnier MH, Klaenhammer TR, Kernéis S, Bernet MF, Servin AL. 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. [PMC free article] [PubMed]
  • Conway PL, Kjelleberg S. Protein-mediated adhesion of Lactobacillus fermentum strain 737 to mouse stomach squamous epithelium. J Gen Microbiol. 1989 May;135(5):1175–1186. [PubMed]
  • Conway PL, Gorbach SL, Goldin BR. Survival of lactic acid bacteria in the human stomach and adhesion to intestinal cells. J Dairy Sci. 1987 Jan;70(1):1–12. [PubMed]
  • 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. [PMC free article] [PubMed]
  • Finlay BB, Falkow S. Common themes in microbial pathogenicity. Microbiol Rev. 1989 Jun;53(2):210–230. [PMC free article] [PubMed]
  • Finlay BB, Falkow S. Salmonella interactions with polarized human intestinal Caco-2 epithelial cells. J Infect Dis. 1990 Nov;162(5):1096–1106. [PubMed]
  • Fogh J, Fogh JM, 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. [PubMed]
  • Gahring LC, Heffron F, Finlay BB, Falkow S. Invasion and replication of Salmonella typhimurium in animal cells. Infect Immun. 1990 Feb;58(2):443–448. [PMC free article] [PubMed]
  • Gaillard JL, 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. [PMC free article] [PubMed]
  • Hastings JW, Sailer M, Johnson K, Roy KL, Vederas JC, Stiles ME. Characterization of leucocin A-UAL 187 and cloning of the bacteriocin gene from Leuconostoc gelidum. J Bacteriol. 1991 Dec;173(23):7491–7500. [PMC free article] [PubMed]
  • Henriksson A, Conway PL. Adhesion to porcine squamous epithelium of saccharide and protein moieties of Lactobacillus fermentum strain 104-S. J Gen Microbiol. 1992 Dec;138(12):2657–2661. [PubMed]
  • Henriksson A, Szewzyk R, Conway PL. Characteristics of the adhesive determinants of Lactobacillus fermentum 104. Appl Environ Microbiol. 1991 Feb;57(2):499–502. [PMC free article] [PubMed]
  • Huet C, Sahuquillo-Merino C, Coudrier E, Louvard D. 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):345–357. [PMC free article] [PubMed]
  • Kleeman EG, Klaenhammer TR. Adherence of Lactobacillus species to human fetal intestinal cells. J Dairy Sci. 1982 Nov;65(11):2063–2069. [PubMed]
  • Knutton S, Baldwin T, Williams PH, McNeish AS. 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. [PMC free article] [PubMed]
  • Kotarski SF, Savage DC. Models for study of the specificity by which indigenous lactobacilli adhere to murine gastric epithelia. Infect Immun. 1979 Dec;26(3):966–975. [PMC free article] [PubMed]
  • Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. [PubMed]
  • McCarthy DM, Lin JH, Rinckel LA, Savage DC. Genetic transformation in Lactobacillus sp. strain 100-33 of the capacity to colonize the nonsecreting gastric epithelium in mice. Appl Environ Microbiol. 1988 Feb;54(2):416–422. [PMC free article] [PubMed]
  • Molin G, Jeppsson B, Johansson ML, Ahrné S, Nobaek S, Ståhl M, Bengmark S. Numerical taxonomy of Lactobacillus spp. associated with healthy and diseased mucosa of the human intestines. J Appl Bacteriol. 1993 Mar;74(3):314–323. [PubMed]
  • Morrissey JH. Silver stain for proteins in polyacrylamide gels: a modified procedure with enhanced uniform sensitivity. Anal Biochem. 1981 Nov 1;117(2):307–310. [PubMed]
  • Mounier J, Ryter A, Coquis-Rondon M, Sansonetti PJ. 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. [PMC free article] [PubMed]
  • Panigrahi P, Tall BD, Russell RG, Detolla LJ, Morris JG., 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. [PMC free article] [PubMed]
  • Raya RR, Fremaux C, De Antoni GL, Klaenhammer TR. Site-specific integration of the temperate bacteriophage phi adh into the Lactobacillus gasseri chromosome and molecular characterization of the phage (attP) and bacterial (attB) attachment sites. J Bacteriol. 1992 Sep;174(17):5584–5592. [PMC free article] [PubMed]
  • Raya RR, Kleeman EG, Luchansky JB, Klaenhammer TR. Characterization of the temperate bacteriophage phi adh and plasmid transduction in Lactobacillus acidophilus ADH. Appl Environ Microbiol. 1989 Sep;55(9):2206–2213. [PMC free article] [PubMed]
  • Reid G, Servin AL, Bruce AW, Busscher HJ. Adhesion of three Lactobacillus strains to human urinary and intestinal epithelial cells. Microbios. 1993;75(302):57–65. [PubMed]
  • Sanders ME. Effect of consumption of lactic cultures on human health. Adv Food Nutr Res. 1993;37:67–130. [PubMed]
  • Savage DC. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol. 1977;31:107–133. [PubMed]
  • Schneitz C, Nuotio L, Lounatma K. Adhesion of Lactobacillus acidophilus to avian intestinal epithelial cells mediated by the crystalline bacterial cell surface layer (S-layer). J Appl Bacteriol. 1993 Mar;74(3):290–294. [PubMed]
  • Sleytr UB, Messner P. Crystalline surface layers on bacteria. Annu Rev Microbiol. 1983;37:311–339. [PubMed]
  • Tannock GW. The normal microflora: new concepts in health promotion. Microbiol Sci. 1988 Jan;5(1):4–8. [PubMed]
  • Vidgrén G, Palva I, Pakkanen R, Lounatmaa K, Palva A. S-layer protein gene of Lactobacillus brevis: cloning by polymerase chain reaction and determination of the nucleotide sequence. J Bacteriol. 1992 Nov;174(22):7419–7427. [PMC free article] [PubMed]
  • Wadström T, Andersson K, Sydow M, Axelsson L, Lindgren S, Gullmar B. Surface properties of lactobacilli isolated from the small intestine of pigs. J Appl Bacteriol. 1987 Jun;62(6):513–520. [PubMed]

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