Lessons from probiotic-host interaction studies in murine models of experimental colitis

Molecular Nutrition and Food Research

Volumn 55, Issue 10, 2011, Pages 1441-1453

  Claes, Ingmar J J ^a   De Keersmaecker, Sigrid C J ^a   Vanderleyden, Jos ^a   Lebeer, Sarah ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Experimental colitis; Inflammatory bowel disease; Lipoteichoic acid; Mouse model; Probiotic

Indexed keywords

DEXTRAN SULFATE; INTERLEUKIN 10; PROBIOTIC AGENT; TRINITROBENZENESULFONIC ACID;

ANIMAL; CHEMICALLY INDUCED DISORDER; COLITIS; DISEASE MODEL; ENTERITIS; GENETICS; HUMAN; MICROBIOLOGY; MOUSE; MOUSE MUTANT; MOUSE STRAIN; REVIEW; ULCERATIVE COLITIS;

ANIMALS; COLITIS; COLITIS, ULCERATIVE; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; HUMANS; INFLAMMATORY BOWEL DISEASES; INTERLEUKIN-10; MICE; MICE, INBRED STRAINS; MICE, MUTANT STRAINS; PROBIOTICS; TRINITROBENZENESULFONIC ACID;

ANIMALIA; MURINAE;

EID: 80053918916     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201100139     Document Type: Review

References (112)

1. FAO/WHO, Food and Agriculture Organization of the United Nations and World Health Organization Expert Consultation Report. FAO/WHO, Rome, Italy 2001.
2. Podolsky, D. K., Inflammatory bowel disease. N. Engl. J. Med. 2002, 347, 417-429.
3. Sartor, R. B., Mechanisms of disease: pathogenesis of Crohn's disease and ulcerative colitis. Nat. Clin. Pract. 2006, 3, 390-407.
4. Sheil, B., Shanahan, F., O'Mahony, L., Probiotic effects on inflammatory bowel disease. J. Nutr. 2007, 137, 819S-824S.
5. Sartor, R. B., Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology 2004, 126, 1620-1633.
6. Lebeer, S., Vanderleyden, J., De Keersmaecker, S. C., Genes and molecules of lactobacilli supporting probiotic action. Microbiol. Mol. Biol. Rev. 2008, 72, 728-764.
7. Isaacs, K., Herfarth, H., Role of probiotic therapy in IBD. Inflamm. Bowel Dis. 2008, 14, 1597-1605.
8. Jurjus, A. R., Khoury, N. N., Reimund, J. M., Animal models of inflammatory bowel disease. J. Pharmacol. Toxicol. Methods 2004, 50, 81-92.
9. Kawada, M., Arihiro, A., Mizoguchi, E., Insights from advances in research of chemically induced experimental models of human inflammatory bowel disease. World J. Gastroenterol. 2007, 13, 5581-5593.
10. Elson, C. O., Cong, Y., McCracken, V. J., Dimmitt, R. A. et al., Experimental models of inflammatory bowel disease reveal innate, adaptive, and regulatory mechanisms of host dialogue with the microbiota. Immunol. Rev. 2005, 206, 260-276.
11. Arseneau, K. O., Pizarro, T. T., Cominelli, F., Discovering the cause of inflammatory bowel disease: lessons from animal models. Curr. Opin. Gastroenterol. 2000, 16, 310-317.
12. Okayasu, I., Hatakeyama, S., Yamada, M., Ohkusa, T. et al., A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 1990, 98, 694-702.
13. Melgar, S., Karlsson, A., Michaelsson, E., Acute colitis induced by dextran sulfate sodium progresses to chronicity in C57BL/6 but not in BALB/c mice: correlation between symptoms and inflammation. Am. J. Physiol. Gastrointest. Liver Physiol. 2005, 288, G1328-G1338.
14. Dieleman, L. A., Ridwan, B. U., Tennyson, G. S., Beagley, K. W. et al., Dextran sulfate sodium-induced colitis occurs in severe combined immunodeficient mice. Gastroenterology 1994, 107, 1643-1652.
15. Cooper, H. S., Murthy, S. N., Shah, R. S., Sedergran, D. J., Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab. Invest. 1993, 69, 238-249.
16. Kruis, W., Fric, P., Pokrotnieks, J., Lukas, M. et al., Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 2004, 53, 1617-1623.
17. Rembacken, B. J., Snelling, A. M., Hawkey, P. M., Chalmers, D. M., Axon, A. T., Non-pathogenic Escherichia coli versus mesalazine for the treatment of ulcerative colitis: a randomised trial. Lancet 1999, 354, 635-639.
18. Schultz, M., Strauch, U. G., Linde, H. J., Watzl, S. et al., Preventive effects of Escherichia coli strain Nissle 1917 on acute and chronic intestinal inflammation in two different murine models of colitis. Clin. Diagn. Lab. Immunol. 2004, 11, 372-378.
19. Kamada, N., Inoue, N., Hisamatsu, T., Okamoto, S. et al., Nonpathogenic Escherichia coli strain Nissle1917 prevents murine acute and chronic colitis. Inflamm. Bowel Dis. 2005, 11, 455-463.
20. Grabig, A., Paclik, D., Guzy, C., Dankof, A. et al., Escherichia coli strain Nissle 1917 ameliorates experimental colitis via toll-like receptor 2- and toll-like receptor 4-dependent pathways. Infect. Immun. 2006, 74, 4075-4082.
21. Kokesova, A., Frolova, L., Kverka, M., Sokol, D. et al., Oral administration of probiotic bacteria (E. coli Nissle, E. coli O83, Lactobacillus casei) influences the severity of dextran sodium sulfate-induced colitis in BALB/c mice. Folia Microbiol. 2006, 51, 478-484.
22. Ukena, S. N., Singh, A., Dringenberg, U., Engelhardt, R. et al., Probiotic Escherichia coli Nissle 1917 inhibits leaky gut by enhancing mucosal integrity. PLoS One 2007, 2, e1308.
23. Chapman, T. M., Plosker, G. L., Figgitt, D. P., VSL{music sharp sign}3 probiotic mixture: a review of its use in chronic inflammatory bowel diseases. Drugs 2006, 66, 1371-1387.
24. Rachmilewitz, D., Katakura, K., Karmeli, F., Hayashi, T. et al., Toll-like receptor 9 signaling mediates the anti-inflammatory effects of probiotics in murine experimental colitis. Gastroenterology 2004, 126, 520-528.
25. Reid, G., Guarner, F., Gibson, G., Tompkins, T. et al., Discussion on toll-like receptor 9 signaling mediates the anti-inflammatory effects of probiotics in murine experimental colitis. Gastroenterology 2004, 127, 366-367; author reply 367.
26. Mennigen, R., Nolte, K., Rijcken, E., Utech, M. et al., Probiotic mixture VSL{music sharp sign}3 protects the epithelial barrier by maintaining tight junction protein expression and preventing apoptosis in a murine model of colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2009, 296, G1140-G1149.
27. Gaudier, E., Michel, C., Segain, J. P., Cherbut, C., Hoebler, C., The VSL{music sharp sign}3 probiotic mixture modifies microflora but does not heal chronic dextran-sodium sulfate-induced colitis or reinforce the mucus barrier in mice. J. Nutr. 2005, 135, 2753-2761.
28. Nanda Kumar, N. S., Balamurugan, R., Jayakanthan, K., Pulimood, A. et al., Probiotic administration alters the gut flora and attenuates colitis in mice administered dextran sodium sulfate. J. Gastroenterol. Hepatol. 2008, 23, 1834-1839.
29. Feighery, L. M., Smith, P., O'Mahony, L., Fallon, P. G., Brayden, D. J., Effects of Lactobacillus salivarius 433118 on intestinal inflammation, immunity status and in vitro colon function in two mouse models of inflammatory bowel disease. Dig. Dis. Sci. 2008, 53, 2495-2506.
30. Claes, I. J., Lebeer, S., Shen, C., Verhoeven, T. L. et al., Impact of lipoteichoic acid modification on the performance of the probiotic Lactobacillus rhamnosus GG in experimental colitis. Clin. Exp. Immunol. 2010, 162, 306-314.
31. Mileti, E., Matteoli, G., Iliev, I. D., Rescigno, M., Comparison of the immunomodulatory properties of three probiotic strains of lactobacilli using complex culture systems: prediction for in vivo efficacy. PLoS ONE 2009, 4, e7056.
32. Mohamadzadeh, M., Pfeiler, E. A., Brown, J. B., Zadeh, M. et al., Microbes and Health Sackler Colloquium: regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. Proc. Natl. Acad. Sci. USA 2011, 108, Suppl.1, 4623-4630.
33. Morris, G. P., Beck, P. L., Herridge, M. S., Depew, W. T. et al., Hapten-induced model of chronic inflammation and ulceration in the rat colon. Gastroenterology 1989, 96, 795-803.
34. Neurath, M. F., Fuss, I., Kelsall, B. L., Stuber, E., Strober, W., Antibodies to interleukin 12 abrogate established experimental colitis in mice. J. Exp. Med. 1995, 182, 1281-1290.
35. Di Giacinto, C., Marinaro, M., Sanchez, M., Strober, W., Boirivant, M., Probiotics ameliorate recurrent Th1-mediated murine colitis by inducing IL-10 and IL-10-dependent TGF-beta-bearing regulatory cells. J. Immunol. 2005, 174, 3237-3246.
36. Roselli, M., Finamore, A., Nuccitelli, S., Carnevali, P. et al., Prevention of TNBS-induced colitis by different Lactobacillus and Bifidobacterium strains is associated with an expansion of gammadeltaT and regulatory T cells of intestinal intraepithelial lymphocytes. Inflamm. Bowel Dis. 2009, 15, 1526-1536.
37. Drouault-Holowacz, S., Foligne, B., Dennin, V., Goudercourt, D. et al., Anti-inflammatory potential of the probiotic dietary supplement lactibiane tolerance: in vitro and in vivo considerations. Clin. Nutr. 2006, 25, 994-1003.
38. Daniel, C., Poiret, S., Goudercourt, D., Dennin, V. et al., Selecting lactic acid bacteria for their safety and functionality by use of a mouse colitis model. Appl. Environ. Microbiol. 2006, 72, 5799-5805.
39. Foligne, B., Nutten, S., Grangette, C., Dennin, V. et al., Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World J. Gastroenterol. 2007, 13, 236-243.
40. Zoumpopoulou, G., Foligne, B., Christodoulou, K., Grangette, C. et al., Lactobacillus fermentum ACA-DC 179 displays probiotic potential in vitro and protects against trinitrobenzene sulfonic acid (TNBS)-induced colitis and Salmonella infection in murine models. Int. J. Food Microbiol. 2008, 121, 18-26.
41. Grangette, C., Nutten, S., Palumbo, E., Morath, S. et al., Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. Proc. Natl. Acad. Sci. USA 2005, 102, 10321-10326.
42. Pavan, S., Desreumaux, P., Mercenier, A., Use of mouse models to evaluate the persistence, safety, and immune modulation capacities of lactic acid bacteria. Clin. Diagn. Lab. Immunol. 2003, 10, 696-701.
43. Im, E., Choi, Y. J., Pothoulakis, C., Rhee, S. H., Bacillus polyfermenticus ameliorates colonic inflammation by promoting cytoprotective effects in colitic mice. J. Nutr. 2009, 139, 1848-1854.
44. Lee, B., Lee, J. H., Lee, H. S., Bae, E. A. et al., Glycosaminoglycan degradation-inhibitory lactic acid bacteria ameliorate 2, 4, 6-trinitrobenzenesulfonic acid-induced colitis in mice. J. Microbiol. Biotechnol. 2009, 19, 616-621.
45. Preising, J., Philippe, D., Gleinser, M., Wei, H. et al., Selection of bifidobacteria based on adhesion and anti-inflammatory capacity in vitro for amelioration of murine colitis. Appl. Environ. Microbiol. 2010, 76, 3048-3051.
46. Mane, J., Loren, V., Pedrosa, E., Ojanguren, I. et al., Lactobacillus fermentum CECT 5716 prevents and reverts intestinal damage on TNBS-induced colitis in mice. Inflamm. Bowel Dis. 2009, 15, 1155-1163.
47. Sokol, H., Pigneur, B., Watterlot, L., Lakhdari, O. et al., Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. USA 2008, 105, 16731-16736.
48. Manichanh, C., Rigottier-Gois, L., Bonnaud, E., Gloux, K. et al., Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut 2006, 55, 205-211.
49. Sokol, H., Seksik, P., Rigottier-Gois, L., Lay, C. et al., Specificities of the fecal microbiota in inflammatory bowel disease. Inflamm. Bowel Dis. 2006, 12, 106-111.
50. Davidson, N. J., Leach, M. W., Fort, M. M., Thompson-Snipes, L. et al., T helper cell 1-type CD4+T cells, but not B cells, mediate colitis in interleukin 10-deficient mice. J. Exp. Med. 1996, 184, 241-251.
51. Berg, D. J., Davidson, N., Kuhn, R., Muller, W. et al., Enterocolitis and colon cancer in interleukin-10-deficient mice are associated with aberrant cytokine production and CD4(+) TH1-like responses. J. Clin. Invest. 1996, 98, 1010-1020.
52. Hormannsperger, G., Clavel, T., Hoffmann, M., Reiff, C. et al., Posttranslational inhibition of proinflammatory chemokine secretion in intestinal epithelial cells: implications for specific IBD indications. J. Clin. Gastroenterol. 2010, 44, S10-S15.
53. Reiff, C., Delday, M., Rucklidge, G., Reid, M. et al., Balancing inflammatory, lipid, and xenobiotic signaling pathways by VSL{music sharp sign}3, a biotherapeutic agent, in the treatment of inflammatory bowel disease. Inflamm. Bowel Dis. 2009, 15, 1721-1736.
54. Soo, I., Madsen, K. L., Tejpar, Q., Sydora, B. C. et al., VSL{music sharp sign}3 probiotic upregulates intestinal mucosal alkaline sphingomyelinase and reduces inflammation. Can. J. Gastroenterol. 2008, 22, 237-242.
55. Liu, Z., Zhang, P., Ma, Y., Chen, H. et al., Lactobacillus plantarum prevents the development of colitis in IL-10-deficient mouse by reducing the intestinal permeability. Mol. Biol. Rep. 2011, 38, 1353-1361.
56. Chu, Z. X., Chen, H. Q., Ma, Y. L., Zhou, Y. K. et al., Lactobacillus plantarum prevents the upregulation of adhesion molecule expression in an experimental colitis model. Dig. Dis. Sci. 2010, 55, 2505-2513.
57. Chen, H. Q., Shen, T. Y., Zhou, Y. K., Zhang, M. et al., Lactobacillus plantarum consumption increases PepT1-mediated amino acid absorption by enhancing protein kinase C activity in spontaneously colitic mice. J. Nutr. 2010, 140, 2201-2206.
58. Chen, H. Q., Yang, J., Zhang, M., Zhou, Y. K. et al., Lactobacillus plantarum ameliorates colonic epithelial barrier dysfunction by modulating the apical junctional complex and PepT1 in IL-10 knockout mice. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299, G1287-G1297.
59. Schultz, M., Veltkamp, C., Dieleman, L. A., Grenther, W. B. et al., Lactobacillus plantarum 299V in the treatment and prevention of spontaneous colitis in interleukin-10-deficient mice. Inflamm. Bowel Dis. 2002, 8, 71-80.
60. McCarthy, J., O'Mahony, L., O'Callaghan, L., Sheil, B. et al., Double blind, placebo controlled trial of two probiotic strains in interleukin 10 knockout mice and mechanistic link with cytokine balance. Gut 2003, 52, 975-980.
61. O'Mahony, L., Feeney, M., O'Halloran, S., Murphy, L. et al., Probiotic impact on microbial flora, inflammation and tumour development in IL-10 knockout mice. Aliment. Pharmacol. Ther. 2001, 15, 1219-1225.
62. Sheil, B., McCarthy, J., O'Mahony, L., Bennett, M. W. et al., Is the mucosal route of administration essential for probiotic function? Subcutaneous administration is associated with attenuation of murine colitis and arthritis. Gut 2004, 53, 694-700.
63. Carroll, I. M., Andrus, J. M., Bruno-Barcena, J. M., Klaenhammer, T. R. et al., Anti-inflammatory properties of Lactobacillus gasseri expressing manganese superoxide dismutase using the interleukin 10-deficient mouse model of colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 293, G729-G738.
64. Pena, J. A., Rogers, A. B., Ge, Z., Ng, V. et al., Probiotic Lactobacillus spp. diminish Helicobacter hepaticus-induced inflammatory bowel disease in interleukin-10-deficient mice. Infect. Immun. 2005, 73, 912-920.
65. Pizarro, T. T., Arseneau, K. O., Bamias, G., Cominelli, F., Mouse models for the study of Crohn's disease. Trends Mol. Med. 2003, 9, 218-222.
66. Veiga, P., Gallini, C. A., Beal, C., Michaud, M. et al., Bifidobacterium animalis subsp. lactis fermented milk product reduces inflammation by altering a niche for colitogenic microbes. Proc. Natl. Acad. Sci. USA 2010, 107, 18132-18137.
67. Kim, N., Kunisawa, J., Kweon, M. N., Eog Ji, G., Kiyono, H., Oral feeding of Bifidobacterium bifidum (BGN4) prevents CD4(+) CD45RB(high) T cell-mediated inflammatory bowel disease by inhibition of disordered T cell activation. Clin. Immunol. 2007, 123, 30-39.
68. Moller, P. L., Paerregaard, A., Gad, M., Kristensen, N. N., Claesson, M. H., Colitic SCID mice fed Lactobacillus spp. show an ameliorated gut histopathology and an altered cytokine profile by local T cells. Inflamm. Bowel Dis. 2005, 11, 814-819.
69. Higgins, L. M., Frankel, G., Douce, G., Dougan, G., MacDonald, T. T., Citrobacter rodentium infection in mice elicits a mucosal Th1 cytokine response and lesions similar to those in murine inflammatory bowel disease. Infect. Immun. 1999, 67, 3031-3039.
70. Chen, C. C., Louie, S., Shi, H. N., Walker, W. A., Preinoculation with the probiotic Lactobacillus acidophilus early in life effectively inhibits murine Citrobacter rodentium colitis. Pediatr. Res. 2005, 58, 1185-1191.
71. Buset, M., Lipkin, M., Winawer, S., Swaroop, S., Friedman, E., Inhibition of human colonic epithelial cell proliferation in vivo and in vitro by calcium. Cancer Res. 1986, 46, 5426-5430.
72. Leonard, F., Collnot, E. M., Lehr, C. M., A three-dimensional coculture of enterocytes, monocytes and dendritic cells to model inflamed intestinal mucosa in vitro. Mol. Pharm. 2010, 7, 2103-2119.
73. Seksik, P., Dray, X., Sokol, H., Marteau, P., Is there any place for alimentary probiotics, prebiotics or synbiotics, for patients with inflammatory bowel disease? Mol. Nutr. Food Res. 2008, 52, 906-912.
74. Vanderpool, C., Yan, F., Polk, D. B., Mechanisms of probiotic action: implications for therapeutic applications in inflammatory bowel diseases. Inflamm. Bowel Dis. 2008, 14, 1585-1596.
75. Shen, J., Ran, H. Z., Yin, M. H., Zhou, T. X., Xiao, D. S., Meta-analysis: the effect and adverse events of lactobacilli versus placebo in maintenance therapy for Crohn disease. Intern. Med. J. 2009, 39, 103-109.
76. Geier, M. S., Butler, R. N., Giffard, P. M., Howarth, G. S., Lactobacillus fermentum BR11, a potential new probiotic, alleviates symptoms of colitis induced by dextran sulfate sodium (DSS) in rats. Int. J. Food Microbiol. 2007, 114, 267-274.
77. Waterston, R. H., Lindblad-Toh, K., Birney, E., Rogers, J. et al., Initial sequencing and comparative analysis of the mouse genome. Nature 2002, 420, 520-562.
78. Ley, R. E., Turnbaugh, P. J., Klein, S., Gordon, J. I., Microbial ecology: human gut microbes associated with obesity. Nature 2006, 444, 1022-1023.
79. Wagner, R. D., Johnson, S. J., Kurniasih Rubin, D., Probiotic bacteria are antagonistic to Salmonella enterica and Campylobacter jejuni and influence host lymphocyte responses in human microbiota-associated immunodeficient and immunocompetent mice. Mol. Nutr. Food Res. 2009, 53, 377-388.
80. Mahler, M., Bristol, I. J., Leiter, E. H., Workman, A. E. et al., Differential susceptibility of inbred mouse strains to dextran sulfate sodium-induced colitis. Am. J. Physiol. 1998, 274, G544-G551.
81. Preidis, G. A., Versalovic, J., Targeting the human microbiome with antibiotics, probiotics, and prebiotics: gastroenterology enters the metagenomics era. Gastroenterology 2009, 136, 2015-2031.
82. Hugot, J. P., Chamaillard, M., Zouali, H., Lesage, S. et al., Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn's disease. Nature 2001, 411, 599-603.
83. Ogura, Y., Bonen, D. K., Inohara, N., Nicolae, D. L. et al., A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 2001, 411, 603-606.
84. Packey, C. D., Sartor, R. B., Commensal bacteria, traditional and opportunistic pathogens, dysbiosis and bacterial killing in inflammatory bowel diseases. Curr. Opin. Infect. Dis. 2009, 22, 292-301.
85. Pagnini, C., Saeed, R., Bamias, G., Arseneau, K. O. et al., Probiotics promote gut health through stimulation of epithelial innate immunity. Proc. Natl. Acad. Sci. USA 2010, 107, 454-459.
86. Chung, Y. W., Choi, J. H., Oh, T. Y., Eun, C. S., Han, D. S., Lactobacillus casei prevents the development of dextran sulphate sodium-induced colitis in Toll-like receptor 4 mutant mice. Clin. Exp. Immunol. 2008, 151, 182-189.
87. Herias, M. V., Koninkx, J. F., Vos, J. G., Huis in't Veld, J. H., van Dijk, J. E., Probiotic effects of Lactobacillus casei on DSS-induced ulcerative colitis in mice. Int. J. Food Microbiol. 2005, 103, 143-155.
88. Matsumoto, S., Hara, T., Nagaoka, M., Mike, A. et al., A component of polysaccharide peptidoglycan complex on Lactobacillus induced an improvement of murine model of inflammatory bowel disease and colitis-associated cancer. Immunology 2009, 128, e170-e180.
89. Doron, S., Snydman, D. R., Gorbach, S. L., Lactobacillus GG: bacteriology and clinical applications. Gastroenterol. Clin. North Am. 2005, 34, 483-498, ix.
90. Ginsburg, I., Role of lipoteichoic acid in infection and inflammation. Lancet Infect. Dis. 2002, 2, 171-179.
91. von Aulock, S., Morath, S., Hareng, L., Knapp, S. et al., Lipoteichoic acid from Staphylococcus aureus is a potent stimulus for neutrophil recruitment. Immunobiology 2003, 208, 413-422.
92. Lebeer, S., Vanderleyden, J., De Keersmaecker, S. C., Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat. Rev. Microbiol. 2010, 8, 171-184.
93. Foligne, B., Grangette, C., Pot, B., Probiotics in IBD: mucosal and systemic routes of administration may promote similar effects. Gut 2005, 54, 727-728.
94. Castagliuolo, I., Galeazzi, F., Ferrari, S., Elli, M. et al., Beneficial effect of auto-aggregating Lactobacillus crispatus on experimentally induced colitis in mice. FEMS Immunol. Med. Microbiol. 2005, 43, 197-204.
95. Ma, D., Forsythe, P., Bienenstock, J., Live Lactobacillus reuteri is essential for the inhibitory effect on tumor necrosis factor alpha-induced interleukin-8 expression. Infect. Immun. 2004, 72, 5308-5314.
96. Miyauchi, E., Morita, H., Tanabe, S., Lactobacillus rhamnosus alleviates intestinal barrier dysfunction in part by increasing expression of zonula occludens-1 and myosin light-chain kinase in vivo. J. Dairy Sci. 2009, 92, 2400-2408.
97. Maslowski, K. M., Vieira, A. T., Ng, A., Kranich, J. et al., Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 2009, 461, 1282-1286.
98. Konstantinov, S. R., Smidt, H., de Vos, W. M., Bruijns, S. C. et al., S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proc. Natl. Acad. Sci. USA 2008, 105, 19474-19479.
99. Lammers, K. M., Brigidi, P., Vitali, B., Gionchetti, P. et al., Immunomodulatory effects of probiotic bacteria DNA: IL-1 and IL-10 response in human peripheral blood mononuclear cells. FEMS Immunol. Med. Microbiol. 2003, 38, 165-172.
100. Yan, F., Cao, H., Cover, T. L., Whitehead, R. et al., Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 2007, 132, 562-575.
101. Rochat, T., Bermudez-Humaran, L., Gratadoux, J. J., Fourage, C. et al., Anti-inflammatory effects of Lactobacillus casei BL23 producing or not a manganese-dependant catalase on DSS-induced colitis in mice. Microb. Cell Fact. 2007, 6, 22.
102. Chen, L. L., Wang, X. H., Cui, Y., Lian, G. H. et al., Therapeutic effects of four strains of probiotics on experimental colitis in mice. World J. Gastroenterol. 2009, 15, 321-327.
103. Fitzpatrick, L. R., Small, J., Hoerr, R. A., Bostwick, E. F. et al., In vitro and in vivo effects of the probiotic Escherichia coli strain M-17: immunomodulation and attenuation of murine colitis. Br. J. Nutr. 2008, 100, 530-541.
104. Hong, Y. S., Ahn, Y. T., Park, J. C., Lee, J. H. et al., (1)H NMR-based metabonomic assessment of probiotic effects in a colitis mouse model. Arch. Pharm. Res. 2010, 33, 1091-1101.
105. Lee, H. S., Han, S. Y., Bae, E. A., Huh, C. S. et al., Lactic acid bacteria inhibit proinflammatory cytokine expression and bacterial glycosaminoglycan degradation activity in dextran sulfate sodium-induced colitic mice. Int. Immunopharmacol. 2008, 8, 574-580.
106. Nishitani, Y., Tanoue, T., Yamada, K., Ishida, T. et al., Lactococcus lactis subsp. cremoris FC alleviates symptoms of colitis induced by dextran sulfate sodium in mice. Int. Immunopharmacol. 2009, 9, 1444-1451.
107. Ohkawara, S., Furuya, H., Nagashima, K., Asanuma, N., Hino, T., Effect of oral administration of Butyrivibrio fibrisolvens MDT-1 on experimental enterocolitis in mice. Clin. Vaccine Immunol. 2006, 13, 1231-1236.
108. Raz, I., Gollop, N., Polak-Charcon, S., Schwartz, B., Isolation and characterisation of new putative probiotic bacteria from human colonic flora. Br. J. Nutr. 2007, 97, 725-734.
109. van der Kleij, H., O'Mahony, C., Shanahan, F., O'Mahony, L., Bienenstock, J., Protective effects of Lactobacillus reuteri and Bifidobacterium infantis in murine models for colitis do not involve the vagus nerve. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 295, R1131-R1137.
110. Foligne, B., Nutten, S., Steidler, L., Dennin, V. et al., Recommendations for improved use of the murine TNBS-induced colitis model in evaluating anti-inflammatory properties of lactic acid bacteria: technical and microbiological aspects. Dig. Dis. Sci. 2006, 51, 390-400.
111. Foligne, B., Dewulf, J., Breton, J., Claisse, O. et al., Probiotic properties of non-conventional lactic acid bacteria: immunomodulation by Oenococcus oeni. Int. J. Food Microbiol. 2010, 140, 136-145.
112. Foligne, B., Dewulf, J., Vandekerckove, P., Pignede, G., Pot, B., Probiotic yeasts: anti-inflammatory potential of various non-pathogenic strains in experimental colitis in mice. World J. Gastroenterol. 2010, 16, 2134-2145.