Role of intestinal epithelial cells in immune effects mediated by gram-positive probiotic bacteria: Involvement of toll-like receptors

Clinical and Diagnostic Laboratory Immunology

Volumn 12, Issue 9, 2005, Pages 1075-1084

  Vinderola, Gabriel ^a,b   Matar, Chantal ^a   Perdigon, Gabriela ^b,c  

^a UNIVERSITÉ DE MONCTON   (Canada)

^b CENTRO DE REFERENCIA PARA LACTOBACILOS CERELA CONICET   (Argentina)

^c UNIVERSIDAD NACIONAL DE TUCUMÁN   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN A; PROBIOTIC AGENT; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CELL DIFFERENTIATION; CELL POPULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ESCHERICHIA COLI; FEMALE; GRAM POSITIVE BACTERIUM; IMMUNE RESPONSE; IMMUNOGLOBULIN PRODUCING CELL; INFLAMMATION; INTESTINE EPITHELIUM CELL; LACTIC ACID BACTERIUM; LACTOBACILLUS HELVETICUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; STRAIN IDENTIFICATION; T LYMPHOCYTE;

ANIMALS; EPITHELIAL CELLS; FEMALE; GRAM-POSITIVE BACTERIA; INTERLEUKIN-1; INTERLEUKIN-6; INTESTINAL MUCOSA; LACTOBACILLUS CASEI; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED BALB C; PROBIOTICS; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTORS;

EID: 24944493160     PISSN: 1071412X     EISSN: None     Source Type: Journal    
DOI: 10.1128/CDLI.12.9.1075-1084.2005     Document Type: Article

References (57)

1. Abreu, M. T., L. S. Thomas, E. T. Arnold, K. Lukasek, K. S. Michelsen, and M. Arditi. 2003. TLR signaling at the intestinal epithelial interface. J. Endotoxin Res. 9:322-330.
2. Abreu, M. T., and M. Arditi. 2004. Innate immunity and toll-like receptors: clinical implication of basic science research. J. Pediatr. 144:421-429.
3. Aldhous, M. C., A. N. Shmakov, J. Bode, and S. Ghosh. 2001. Characterization of conditions for the primary culture of human small intestinal epithelial cells. Clin. Exp. Immunol. 125:32-40.
4. Alvarez, S., N. Gobbato, E. Bru, A. P. de Ruiz Holgado, and G. Perdigón. 1998. Specific immunity induction at mucosal level by viable Lactobacillus casei. Perspective for oral vaccine development. Food Agric. Immunol. 10: 79-87.
5. Backhed, F., and M. Hornef. 2003. Toll-like receptor 4-mediated signaling by epithelial surfaces: necessity or threat? Microbes Infect. 5:951-959.
6. Bai, A.-P., Q. Ouyang, W. Zhang, C.-H. Wang, and S.-F. Li. 2004. Probiotics inhibit TNF-α-induced interleukin-8 secretion of HT29 cells. World J. Gastroenterol. 10:455-457.
7. Beagley, K. W., J. H. Eldridge, W. K. Aicher, J. Mestecky, S. Difabio, H. Kiyono, and J. R. McGhee. 1991. Payer's patch B cells with memory cell characteristics undergo terminal differentiation within 24 hours in response to interleukin-6. Cytokine 3:107-116.
8. Carlo, E., and D. K. Podolsky. 2000. Differential alteration in intestinal epithelial cell expression of toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect. Immun. 68:7010-7017.
9. Cross, M. L. 2002. Microbes versus microbes: immune signals generated by probiotic lactobacilli and their role in protection against microbial pathogens. FEMS Immunol. Med. Microbiol. 34:245-253.
10. Delcour, J., T. Ferain, M. Deghorain, E. Palumbo, and P. Hols. 1999. The biosynthesis and functionality of the cell-wall of lactic acid bacteria. Antonie Leeuwenhoek 76:159-184.
11. Dougan, G., A. Haque, D. Pickard, G. Frankel, P. O'Goara, and J. Wain. 2001. The Escherichia coli gene pool. Curr. Opin. Microbiol. 4:90-94.
12. Dozois, C. M., and R. Curtis. 1999. Pathogenicity diversity of Escherichia coli and the emergence of 'exotic' islands in the gene stream. Vet. Res. 30:157-179.
13. Dunne, C., L. Murphy, S. Flynn, L. O'Mahony, S. O'Halloran, M. Feeney, D. Morrissey, G. Thornton, G. Fitzgerald, C. Daly, B. Kiely, E. M. M. Quigley, G. C. O'Sullivan, F. Shanahan, and J. K. Collins. 1999. Probiotics: from myth to reality. Demonstration of functionality in animal model of disease and in human clinical trials. Antonie Leeuwenhoek 76:279-292.
14. Erickson, K. L., and N. E. Hubbard. 2000. Probiotic immunomodulation in health and disease. J. Nutr. 130(Suppl. 25):403S-409S.
15. Faure, E., L. Thomas, H. Xu, A. E. Medvedev, O. Equils, and M. Arditi. 2001. Bacterial lipopolysaccharide and IFN-γ induce toll-like receptor 2 and toll-like receptor 4 expression in human endothelial cells: role of NF-κB activation. J. Immunol. 166:2018-2024.
16. Gleeson, M., and A. W. Cripps. 2004. Development of mucosal immunity in the first year of life and relationship to sudden infant death syndrome. FEMS Immunol. Med. Microbiol. 42:21-23.
17. Goodrich, M. E., and D. W. McGee. 1998. Regulation of mucosal B cell immunoglobulin secretion by intestinal epithelial cell-derived cytokines. Cytokine 10:948-955.
18. Goodrich, M. E., and D. W. McGee. 1999. Effect of intestinal epithelial cell cytokines on mucosal B-cell IgA secretion: enhancing effect of epithelial-derived IL-6 but not TGF-β on IgA+ B cells. Immunol. Lett. 67:11-14.
19. Haller, D., C. Bode, W. P. Hammes, A. M. A. Pfeifer, E. J. Schiffrin, and S. Blum. 2000. Non-pathogenic bacteria elicit a differential cytokine response by intestinal epithelial cell/leucocyte co-cultures. Gut 47:79-87.
20. Haller, D., H. Colbus, M. G. Ganzle, P. Scherenbacher, C. Bode, and W. P. Hammes. 2001. Metabolic and functional properties of lactic acid bacteria in the gastro-intestinal ecosystem: a comparative in vitro study between bacteria of intestinal and fermented food origin. Syst. Appl. Microbiol. 24:218-226.
21. low monocytes inhibit lymphocyte-dependent activation of intestinal epithelial cells by commensal bacteria. Microbiol. Immunol. 46:195-205.
22. Hedger, S., M. Svensson, and C. Svanborg. 1992. Interleukin-6 response of epithelial cell lines to bacterial stimulation in vitro. Infect. Immun. 60:1295-1301.
23. Heumann, D., C. Barras, A. Severin, M. P. Glauser, and A. Tomasz. 1994. Gram-positive cell walls stimulate synthesis of tumor necrosis factor alpha and interleukin-6 by human monocytes. Infect. Immun. 62:2715-2721.
24. Hosoi, T., R. Hirose, S. Saegusa, A. Ametani, K. Kiuchi, and S. Kaminogawa. 2003. Cytokine responses of human intestinal epithelial-like Caco-2 cells to the non-pathogenic bacterium Bacillus subtilis (natto). Int. J. Food Microbiol. 82:255-264.
25. Isolauri, E., S. Salminen, and A. C. Ouwehand. 2004. Microbial-gut interactions in health and disease. Probiotics. Best Pract. Res. Clin. Gastroenterol. 18:299-313.
26. Jacobsen, C. N., V. R. Nielsen, A. E. Hayford, P. L. Møller, K. F. Michaelsen, A. Paerregaard, B. Sandström, M. Tvede, and M. Jakobsen. 1999. Screening of probiotic activities of forty-seven strains of Lactobacillus spp. by in vitro techniques and evaluation of the colonization ability of five selected strains in humans. Appl. Environ. Microbiol. 65:4949-4956.
27. Kagnoff, M. F., and L. Eckmann. 1997. Epithelial cells as sensors for microbial infection. J. Clin. Investig. 100:6-10.
28. Kedinger, M., K. Haffen, and P. Simon-Assmann. 1987. Intestinal tissue and cell cultures. Differentiation 36:71-85.
29. Ma, D., P. Forsythe, and J. Bienenstock. 2004. Live Lactobacillus reuteri is essential for the inhibitory effect on tumor necrosis factor alpha-induced interleukin-8 expression. Infect. Immun. 72:5308-5314.
30. Macartney, K. K., D. C. Baumgart, S. R. Carding, J. O. Brubaker, and P. A. Offit. 2000. Primary murine small intestinal epithelial cells, maintained in long-term culture, are susceptible to rotavirus infection. J. Virol. 74:5597-5603.
31. Maldonado Galdeano, C., and G. Perdigon. 2004. Role of viability of probiotic strains in their persistence in the gut and in mucosal immune stimulation. J. Appl. Microbiol. 97:673-681.
32. Mandel, L., A. P. Moran, A. Cocchiarella, J. M. Houghton, N. Taylor, J. G. Fox, T. C. Wang, and E. A. Kurt-Jones. 2004. Intact gram-negative Helicobacter pylori, Helicobacter felis, and Helicobacter hepaticus bacteria activate innate immunity via Toll-like receptor 2 but not Toll-like receptor 4. Infect. Immun. 72:6446-6454.
33. Matsuguchi, T., A. Takagi, T. Matsuzaki, M. Nagaoka, K. Ishikawa, T. Yokohura, and Y. Yoshikai. 2003. Lipoteichoic acids from Lactobacillus strains elicit strong tumor necrosis factor alpha-inducing activities in macrophages through Toll-like receptor 2. Clin. Diagn. Lab. Immunol. 10:259-266.
34. Matar, C., J. C. Valdez, M. Medina, M. Rachid, and G. Perdigón. 2001. Immunomodulating effect of milks fermented by Lactobacillus helveticus and its non-proteolytic variant. J. Dairy Res. 68:601-609.
35. Melmed, G., L. S. Thomas, N. Lee, S. Y. Tesfay, K. Lukasek, K. S. Michelsen, Y. Zhou, B. Hu, M. Arditi, and M. T. Abreu. 2003. Human intestinal epithelial cells are broadly unresponsive to Toll-like receptor 2-dependent bacterial ligands: implication for host-microbial interaction in the gut. J. Immunol. 170:1406-1415.
36. Miller, T. L., and D. W. McGee. 2002. Epithelial cells respond to proteolytic and non-proteolytic detachment by enhancing interleukin-6 responses. Immunology 105:101-110.
37. Morita, H., F. He, T. Fuse, A. C. Ouwehand, H. Hashimoto, M. Hosoda, K Mizumachi, and J.-I. Kurisaki. 2002. Adhesion of lactic acid bacteria to Caco-2 cells and their effect on cytokine secretion. Microbiol. Immunol. 46:293-297.
38. Naik, S., E. J. Kelly, L. Meyer, S. Pettersson, and I. R. Sanderson. 2001. Absence of toll-like receptor 4 explains endotoxin hyporesponsiveness in human intestinal epithelium. J. Pediatr. Gastroenterol. Nutr. 32:449-453.
39. Ng, E. K., N. Panesar, W. E. Longo, M. J. Shapiro, D. L. Kaminski, K. C. Tolman, and J. E. Mazuski. 2003. Human intestinal epithelial and smooth muscle cells are potent producers of IL-6. Mediators Inflamm. 12:3-8.
40. Ohashi, K., V. Burkart, S. Flohe, and H. Kolb. 2000. Cutting edge: heat shock protein 60 is putative endogenous ligand of the toll-like receptor-4 complex. J. Biol. Chem. 164:558-561.
41. Otte, J. M., E. Cario, and D. K. Podolsky. 2004. Mechanisms of cross hyporesponsiveness to toll-like receptor bacterial ligands in intestinal epithelial cells. Gastroenterology 126:1054-1070.
42. Perdigón, G., R. Fuller, and R. Raya. 2001. Lactic acid bacteria and their effect on the immune system. Curr. Issues Intest. Microbiol. 2:27.
43. Perdigón G., S. Alvarez, and A. Pesce de Ruiz Holgado. 1991. Immunoadjuvant activity of oral Lactobacillus casei: influence of dose on the secretory immune response and protective capacity in intestinal infections. J. Dairy Res. 58:485.
44. Perdigón, G., C. Maldonado Galdeano, J. C. Valdez, and M. Medici. 2002. Interaction of lactic acid bacteria with the gut immune system. Eur. J. Clin. Nutr. 56:S21-S26.
45. Rhee, K. J., P. Sethupathi, A. Driks, D. K. Lanning, and K. L. Knight. 2004. Role of commensal bacteria in development of gut-associated lymphoid tissues and preimmune antibody repertoire. J. Immunol. 172:1118-1124.
46. Sennikov, S. V., V. Temchura, V. A. Kozlov, and V. A. Trufakin. 2002. The influence of conditioned medium from mouse intestinal epithelial cells on the proliferative activity of crypt cells: role of granulocyte-macrophage colony-stimulating factor. J. Gastroenterol. 37:1048-1051.
47. Shuto, T., A. Imasato, H. Jono, A. Sakai, H. Xu, T. Watanabe, D. D. Rixter, H. Kai, A. Andalibi, F. Linthicum, et al. 2002. Glucocorticoids synergistically enhance nontypeable Haemophilus influenzae-induced toll-like receptor 2 expression via a negative cross-talk with p38 MPA kinase. J. Biol. Chem. 277:17263.
48. Slorach E. M., F. C. Campbell, and J. R. Dorin. 1999. A mouse model of intestinal stem cell function and regeneration. J. Cell Sci. 112:3029-3038.
49. Stadnyk, A., G. R. Sisson, and C. C. M. Waterhouse. 1995. IL-1α is constitutively expressed in the rat intestinal epithelial cell line IEC-6. Exp. Cell Res. 220:298-303.
50. Takeda, K., T. Kaisho, and S. Akira. 2003. Toll-like receptors. Annu. Rev. Immunol. 21:335-376.
51. Tötemeyer, S., N. Foster, P. Kaiser, D. J. Maskell, and C. E. Bryant. 2003. Toll-like receptor expression in C3H/HeN and C3H/HeJ mice during Salmonella enterica serovar Typhimurium infection. Infect. Immun. 71:6653-6657.
52. Triantafilou, K., M. Triantafilou, and R. L. Dedrick. 2001. A CD14-independent LPS receptor cluster. Nat. Immunol. 2:338-359.
53. Uehori, J., M. Matsumoto, S. Tsuji, T. Akazawa, O. Takeuchi, S. Akira, T. Kawata, I. Azuma, K. Tuyoshima, and T. Seya. 2003. Simultaneous blocking of human Toll-like receptors 2 and 4 suppresses myeloid dendritic cell activation induced by Mycobacterium bovis Calmette-Guerin peptidoglycan. Infect. Immun. 71:4238-4249.
54. Umesaki, Y., and H. Setoyama. 2000. Structure of the intestinal flora responsible for development of the gut immune system in a rodent model. Microbes Infect. 2:1343-1351.
55. Vinderola, C. G., and J. A. Reinheimer. 2003. Lactic acid starter and probiotic bacteria: a comparative in vitro study of probiotic characteristics and biological barrier resistance. Food Res. Intern. 36:895-904.
56. Vintiñi, E., S. Alvarez, M. Medina, M. Medici, M. V. de Budeguer, and G. Perdigón. 2000. Gut mucosal immunostimulation by lactic acid bacteria. Biocell 23:223.
57. Weinstein D. L., B. L. O'Neill, and E. S. Metcalf. 1997. Salmonella typhi stimulation of human intestinal epithelial cell induces secretion of epithelial cell-derived interleukin-6. Infect. Immun. 65:395-404.