Probiotics Can Generate FoxP3 T-Cell Responses in the Small Intestine and Simultaneously Inducing CD4 and CD8 T Cell Activation in the Large Intestine

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Smelt, Maaike J ^a,b   de Haan, Bart J ^b   Bron, Peter A ^a,c   van Swam, Iris ^a,c   Meijerink, Marjolein ^a,d   Wells, Jerry M ^a,d   Faas, Marijke M ^b   de Vos, Paul ^a,b  

^a TOP INSTITUTE FOOD AND NUTRITION   (Netherlands)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c NIZO FOOD RESEARCH   (Netherlands)

^d WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN P 15095; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PROBIOTIC AGENT; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR T BET;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; DRUG EFFECT; FOXP3+ T LYMPHOCYTE; IMMUNOMODULATION; IMMUNOPHENOTYPING; LACTOBACILLUS DELBRUECKII; LACTOBACILLUS PLANTARUM; LACTOBACILLUS SALIVARIUS; LAMINA PROPRIA; LARGE INTESTINE; MALE; MOUSE; NONHUMAN; PEYER PATCH; PROTEIN EXPRESSION; SMALL INTESTINE; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH1 CELL; TH2 CELL; UPREGULATION;

ANIMALS; ANTIGENS, CD11C; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL COUNT; DENDRITIC CELLS; FORKHEAD TRANSCRIPTION FACTORS; GATA3 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION; HUMANS; INTESTINAL MUCOSA; INTESTINE, LARGE; INTESTINE, SMALL; LACTOBACILLUS; LYMPHOCYTE ACTIVATION; MALE; MICE; PEYER'S PATCHES; PROBIOTICS; SPECIES SPECIFICITY; T-BOX DOMAIN PROTEINS; TH1-TH2 BALANCE;

BACTERIA (MICROORGANISMS); MUS;

EID: 84879828069     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068952     Document Type: Article

References (60)

1. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R, (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489: 220-230.
2. Ottman N, Smidt H, de Vos WM, Belzer C, (2012) The function of our microbiota: who is out there and what do they do? Front Cell Infect Microbiol 2: 104.
3. Sartor RB (1997) Review article: Role of the enteric microflora in the pathogenesis of intestinal inflammation and arthritis. Aliment Pharmacol Ther 11 Suppl 3: 17-22; discussion 22-13.
4. Tamboli CP, Neut C, Desreumaux P, Colombel JF, (2004) Dysbiosis as a prerequisite for IBD. Gut 53: 1057.
5. Yasui H, Kiyoshima J, Hori T, (2004) Reduction of influenza virus titer and protection against influenza virus infection in infant mice fed Lactobacillus casei Shirota. Clin Diagn Lab Immunol 11: 675-679.
6. Hatakka K, Savilahti E, Ponka A, Meurman JH, Poussa T, et al. (2001) Effect of long term consumption of probiotic milk on infections in children attending day care centres: double blind, randomised trial. BMJ 322: 1327.
7. Hojsak I, Abdovic S, Szajewska H, Milosevic M, Krznaric Z, et al. (2010) Lactobacillus GG in the prevention of nosocomial gastrointestinal and respiratory tract infections. Pediatrics 125: e1171-1177.
8. Kawase M, He F, Kubota A, Harata G, Hiramatsu M, (2010) Oral administration of lactobacilli from human intestinal tract protects mice against influenza virus infection. Lett Appl Microbiol 51: 6-10.
9. Davidson LE, Fiorino AM, Snydman DR, Hibberd PL, (2011) Lactobacillus GG as an immune adjuvant for live-attenuated influenza vaccine in healthy adults: a randomized double-blind placebo-controlled trial. Eur J Clin Nutr 65: 501-507.
10. Xia Y, Chen HQ, Zhang M, Jiang YQ, Hang XM, et al. (2011) Effect of Lactobacillus plantarum LP-Onlly on gut flora and colitis in interleukin-10 knockout mice. J Gastroenterol Hepatol 26: 405-411.
11. Osman N, Adawi D, Ahrne S, Jeppsson B, Molin G, (2004) Modulation of the effect of dextran sulfate sodium-induced acute colitis by the administration of different probiotic strains of Lactobacillus and Bifidobacterium. Dig Dis Sci 49: 320-327.
12. Dicksved J, Schreiber O, Willing B, Petersson J, Rang S, et al. (2012) Lactobacillus reuteri maintains a functional mucosal barrier during DSS treatment despite mucus layer dysfunction. PLoS One 7: e46399.
13. Mimura T, Rizzello F, Helwig U, Poggioli G, Schreiber S, et al. (2004) Once daily high dose probiotic therapy (VSL#3) for maintaining remission in recurrent or refractory pouchitis. Gut 53: 108-114.
14. Gosselink MP, Schouten WR, van Lieshout LM, Hop WC, Laman JD, et al. (2004) Delay of the first onset of pouchitis by oral intake of the probiotic strain Lactobacillus rhamnosus GG. Dis Colon Rectum 47: 876-884.
15. Guandalini S, (2002) Use of Lactobacillus-GG in paediatric Crohn's disease. Dig Liver Dis 34Suppl 2: S63-65.
16. Kruis W, Fric P, Pokrotnieks J, Lukas M, Fixa B, et al. (2004) Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 53: 1617-1623.
17. Guandalini S, Magazzu G, Chiaro A, La Balestra V, Di Nardo G, et al. (2010) VSL#3 improves symptoms in children with irritable bowel syndrome: a multicenter, randomized, placebo-controlled, double-blind, crossover study. J Pediatr Gastroenterol Nutr 51: 24-30.
18. Smelt MJ, de Haan BJ, Bron PA, van Swam I, Meijerink M, et al. (2012) L. plantarum, L. salivarius, and L. lactis attenuate Th2 responses and increase Treg frequencies in healthy mice in a strain dependent manner. PLoS One 7: e47244.
19. Won TJ, Kim B, Oh ES, Bang JS, Lee YJ, et al. (2011) Immunomodulatory activity of Lactobacillus strains isolated from fermented vegetables and infant stool. Can J Physiol Pharmacol 89: 429-434.
20. van Baarlen P, Troost FJ, van Hemert S, van der Meer C, de Vos WM, et al. (2009) Differential NF-kappaB pathways induction by Lactobacillus plantarum in the duodenum of healthy humans correlating with immune tolerance. Proc Natl Acad Sci U S A 106: 2371-2376.
21. Yang HY, Liu SL, Ibrahim SA, Zhao L, Jiang JL, et al. (2009) Oral administration of live Bifidobacterium substrains isolated from healthy centenarians enhanced immune function in BALB/c mice. Nutr Res 29: 281-289.
22. Linton PJ, Dorshkind K, (2004) Age-related changes in lymphocyte development and function. Nat Immunol 5: 133-139.
23. Brooks-Worrell B, Narla R, Palmer JP, (2012) Biomarkers and immune-modulating therapies for type 2 diabetes. Trends Immunol 33: 546-553.
24. Chandra RK, Kumari S, (1994) Effects of nutrition on the immune system. Nutrition 10: 207-210.
25. Kaplan HB, (1991) Social psychology of the immune system: a conceptual framework and review of the literature. Soc Sci Med 33: 909-923.
26. Foligne B, Nutten S, Steidler L, Dennin V, Goudercourt D, et al. (2006) 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 51: 390-400.
27. Fuss IJ, Neurath M, Boirivant M, Klein JS, de la Motte C, et al. (1996) Disparate CD4+ lamina propria (LP) lymphokine secretion profiles in inflammatory bowel disease. Crohn's disease LP cells manifest increased secretion of IFN-gamma, whereas ulcerative colitis LP cells manifest increased secretion of IL-5. J Immunol 157: 1261-1270.
28. Turner JR, (2009) Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 9: 799-809.
29. Jaensson E, Uronen-Hansson H, Pabst O, Eksteen B, Tian J, et al. (2008) Small intestinal CD103+ dendritic cells display unique functional properties that are conserved between mice and humans. J Exp Med 205: 2139-2149.
30. Macdonald TT, Monteleone G, (2005) Immunity, inflammation, and allergy in the gut. Science 307: 1920-1925.
31. Shida K, Nanno M, (2008) Probiotics and immunology: separating the wheat from the chaff. Trends Immunol 29: 565-573.
32. Kwon HK, Lee CG, So JS, Chae CS, Hwang JS, et al. (2010) Generation of regulatory dendritic cells and CD4+Foxp3+ T cells by probiotics administration suppresses immune disorders. Proc Natl Acad Sci U S A 107: 2159-2164.
33. Sipos F, Muzes G, Galamb O, Spisak S, Krenacs T, et al. (2010) The possible role of isolated lymphoid follicles in colonic mucosal repair. Pathol Oncol Res 16: 11-18.
34. Foligne B, Dessein R, Marceau M, Poiret S, Chamaillard M, et al. (2007) Prevention and treatment of colitis with Lactococcus lactis secreting the immunomodulatory Yersinia LcrV protein. Gastroenterology 133: 862-874.
35. Foligne B, Nutten S, Grangette C, Dennin V, Goudercourt D, et al. (2007) Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World J Gastroenterol 13: 236-243.
36. Kleerebezem M, Boekhorst J, van Kranenburg R, Molenaar D, Kuipers OP, et al. (2003) Complete genome sequence of Lactobacillus plantarum WCFS1. Proc Natl Acad Sci U S A 100: 1990-1995.
37. Fang F, Flynn S, Li Y, Claesson MJ, van Pijkeren JP, et al. (2008) Characterization of endogenous plasmids from Lactobacillus salivarius UCC118. Appl Environ Microbiol 74: 3216-3228.
38. Wegmann U, O'Connell-Motherway M, Zomer A, Buist G, Shearman C, et al. (2007) Complete genome sequence of the prototype lactic acid bacterium Lactococcus lactis subsp. cremoris MG1363. J Bacteriol 189: 3256-3270.
39. Kinoshita M, Kayama H, Kusu T, Yamaguchi T, Kunisawa J, et al. (2012) Dietary folic acid promotes survival of Foxp3+ regulatory T cells in the colon. J Immunol 189: 2869-2878.
40. Smelt MJ, de Haan BJ, Bron PA, van Swam I, Meijerink M, et al. (2013) The Impact of Lactobacillus plantarum WCFS1 Teichoic Acid D-Alanylation on the Generation of Effector and Regulatory T-cells in Healthy Mice. PLoS One 8: e63099.
41. Mowat AM, (2003) Anatomical basis of tolerance and immunity to intestinal antigens. Nat Rev Immunol 3: 331-341.
42. Sonnenberg GF, Fouser LA, Artis D, (2011) Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat Immunol 12: 383-390.
43. Hansson GC, Johansson ME, (2010) The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Gut Microbes 1: 51-54.
44. Johansson ME, Gustafsson JK, Holmen-Larsson J, Jabbar KS, Xia L, et al. (2013) Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis. Gut [ahead of epub].
45. Meijerink M, van HS, Taverne N, Wels M, de VP, et al. (2010) Identification of genetic loci in Lactobacillus plantarum that modulate the immune response of dendritic cells using comparative genome hybridization. PLoSOne 5: e10632.
46. VanHemert S, Meijerink M, Molenaar D, Kleerebezem M, Wells J,et al. Immunomodulation by different strains of Lactobacillus plantarum. In: VanHemert S, editor. LAB9 2008/08/31/; Egmond aan Zee, the Netherlands.
47. Meijerink M, Wells JM, Taverne N, de Zeeuw Brouwer ML, Hilhorst B, et al. (2012) Immunomodulatory effects of potential probiotics in a mouse peanut sensitization model. FEMS Immunol Med Microbiol 65: 488-496.
48. Wells JM, Rossi O, Meijerink M, van BP, (2011) Epithelial crosstalk at the microbiota-mucosal interface. ProcNatlAcadSciUSA 108Suppl 1: 4607-4614.
49. Lemon KP, Armitage GC, Relman DA, Fischbach MA, (2012) Microbiota-targeted therapies: an ecological perspective. Sci Transl Med 4: 137rv135.
50. Iijima H, Takahashi I, Kiyono H, (2001) Mucosal immune network in the gut for the control of infectious diseases. Rev Med Virol 11: 117-133.
51. McDole JR, Wheeler LW, McDonald KG, Wang B, Konjufca V, et al. (2012) Goblet cells deliver luminal antigen to CD103+ dendritic cells in the small intestine. Nature 483: 345-349.
52. Johansson ME, Gustafsson JK, Sjoberg KE, Petersson J, Holm L, et al. (2010) Bacteria penetrate the inner mucus layer before inflammation in the dextran sulfate colitis model. PLoS One 5: e12238.
53. Grangette C, Nutten S, Palumbo E, Morath S, Hermann C, et al. (2005) Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. Proc Natl Acad Sci U S A 102: 10321-10326.
54. Pathmakanthan S, Li CK, Cowie J, Hawkey CJ, (2004) Lactobacillus plantarum 299: beneficial in vitro immunomodulation in cells extracted from inflamed human colon. J Gastroenterol Hepatol 19: 166-173.
55. Schultz M, Veltkamp C, Dieleman LA, Grenther WB, Wyrick PB, et al. (2002) Lactobacillus plantarum 299V in the treatment and prevention of spontaneous colitis in interleukin-10-deficient mice. Inflamm Bowel Dis 8: 71-80.
56. Meijerink M, van Hemert S, Taverne N, Wels M, de Vos P, et al. (2010) Identification of genetic loci in Lactobacillus plantarum that modulate the immune response of dendritic cells using comparative genome hybridization. PLoS One 5: e10632.
57. Perez-Machado MA, Ashwood P, Thomson MA, Latcham F, Sim R, et al. (2003) Reduced transforming growth factor-beta1-producing T cells in the duodenal mucosa of children with food allergy. Eur J Immunol 33: 2307-2315.
58. Feighery LM, Smith P, O'Mahony L, Fallon PG, Brayden DJ, (2008) 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 53: 2495-2506.
59. Dunne C, Murphy L, Flynn S, O'Mahony L, O'Halloran S, et al. (1999) Probiotics: from myth to reality. Demonstration of functionality in animal models of disease and in human clinical trials. Antonie Van Leeuwenhoek 76: 279-292.
60. O'Mahony L, McCarthy J, Kelly P, Hurley G, Luo F, et al. (2005) Lactobacillus and bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. Gastroenterology 128: 541-551.