Th17 cells as potential probiotic therapeutic targets in inflammatory bowel diseases

International Journal of Molecular Sciences

Volumn 16, Issue 9, 2015, Pages 20841-20858

  Owaga, Eddy ^a   Hsieh, Rong Hong ^b   Mugendi, Beatrice ^a   Masuku, Sakhile ^c   Shih, Chun Kuang ^b   Chang, Jung Su ^b  

^a DEDAN KIMATHI UNIVERSITY OF TECHNOLOGY   (Kenya)

^b TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^c UNIVERSITY OF SWAZILAND   (Swaziland)

Author keywords

IL 17; Inflammation; Inflammatory bowel diseases; Probiotics; Th17

Indexed keywords

ADENOSINE TRIPHOSPHATE; B7 ANTIGEN; CD40 ANTIGEN; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; PROBIOTIC AGENT; RETINOID RELATED ORPHAN RECEPTOR GAMMA; STAT3 PROTEIN; TOLL LIKE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA;

BIFIDOBACTERIACEAE; BIFIDOBACTERIUM; CLINICAL TRIAL (TOPIC); GENETIC SUSCEPTIBILITY; HOMEOSTASIS; HUMAN; IMMUNOMODULATION; INFLAMMATORY BOWEL DISEASE; INTESTINE EPITHELIUM CELL; LACTOBACILLUS; LAMINA PROPRIA; MUCOSAL IMMUNITY; NONHUMAN; PEPTOCLOSTRIDIUM DIFFICILE; PERMEABILITY BARRIER; REGULATORY T LYMPHOCYTE; REVIEW; RISK FACTOR; STREPTOCOCCUS; TH1 CELL; TH17 CELL; TH2 CELL; ANIMAL; GENETIC PREDISPOSITION; IMMUNOLOGY; IMMUNOTHERAPY; INFLAMMATORY BOWEL DISEASES; INTESTINE; METABOLISM; MICROBIOLOGY; PROCEDURES; SIGNAL TRANSDUCTION;

ANIMALS; GENETIC PREDISPOSITION TO DISEASE; HOMEOSTASIS; HUMANS; IMMUNOMODULATION; IMMUNOTHERAPY; INFLAMMATORY BOWEL DISEASES; INTESTINES; PROBIOTICS; RISK FACTORS; SIGNAL TRANSDUCTION; TH17 CELLS;

EID: 84940843952     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms160920841     Document Type: Review

References (109)

1. Dai, C.; Zheng, C.-Q.; Jiang, M.; Ma, X.Y.; Jiang, L.J. Probiotics and irritable bowel syndrome. World J. Gastroenterol. 2013, 19, 5973-5980
2. Khor, B.; Gardet, A.; Xavier, R.J. Genetics and pathogenesis of inflammatory bowel disease. Nature 2011, 474, 307-317
3. Sheil, B.; Shanahan, F.; O’Mahony, L. Probiotic effects on inflammatory bowel disease. J. Nutr. 2007, 137, 819S-824S
4. Gálvez, J. Role of Th17 cells in the pathogenesis of human IBD. ISRN Inflamm. 2014, 2014, 928461
5. Liu, Z.-J.; Yadav, P.K.; Su, J.-L.; Wang, J.S.; Fei, K. Potential role of Th17 cells in the pathogenesis of inflammatory bowel disease. J. Gastroenterol. 2009, 15, 5784-5788
6. Chen, L.; Zou, Y.; Peng, J.; Lu, F.; Yin, Y.; Li, F.; Yang, J. Lactobacillus acidophilus suppresses colitis-associated activation of the IL-23/Th17 axis. J. Immunol. Res. 2015, 2015, 909514
7. Sarra, M.; Pallone, F.; MacDonald, T.T.; Monteleone, G. IL-23/IL-17 axis in IBD. Inflamm. Bowel Dis. 2010, 16, 1808-1813
8. Sartor, R.B. Mechanisms of disease: Pathogenesis of Crohn’s disease and ulcerative colitis. Nat. Clin. Pract. Gastroenterol. Hepatol. 2006, 3, 390-407
9. Hölttä, V.; Klemetti, P.; Salo, H.M.; Koivusalo, A.; Pakarinen, M.; Westerholm-Ormio, M.; Kolho, K.L.; Vaarala, O. Interleukin-17 immunity in paediatric Crohn disease and ulcerative colitis. J. Pediatr. Gastroenterol. Nutr. 2013, 57, 287-292
10. Ueno, A.; Jijon, H.; Chan, R.; Ford, K.; Hirota, C.; Kaplan, G.G.; Beck, P.L.; Iacucci, M.; Fort, G.M.; Barkema, H.W.; et al. Increased prevalence of circulating novel IL-17 secreting Foxp3 expressing CD4+ T cells and defective suppressive function of circulating Foxp3+ regulatory cells support plasticity between Th17 and regulatory T cells in inflammatory bowel disease patients. Inflamm. Bowel Dis. 2013, 19, 2522-2534
11. Sahin, A.; Calhan, T.; Cengiz, M.; Kahraman, R.; Aydin, K.; Ozdil, K.; Korachi, M.; Sokmen, H.M. Serum interleukin 17 levels in patients with Crohn’s disease: Real life data. Dis. Markers 2014, 2014, 690853
12. Raza, A.; Shata, M. Letter: Pathogenicity of Th17 cells may differ in ulcerative colitis compared with Crohn’s disease. Aliment. Pharmacol. Ther. 2012, 36, 204-204
13. Ito, R.; Kita, M.; Shin-Ya, M.; Kishida, T.; Urano, A.; Takada, R.; Sakagami, J.; Imanishi, J.; Iwakura, Y.; Okanoue, T.; et al. Involvement of IL-17A in the pathogenesis of DSS-induced colitis in mice. Biochem. Biophys. Res. Commun. 2008, 377, 12-16
14. Zhang, Z.; Zheng, M.; Bindas, J.; Schwarzenberger, P.; Kolls, J.K. Critical role of IL-17 receptor signaling in acute TNBS-induced colitis. Inflamm. Bowel Dis. 2006, 12, 382-388
15. Bedoya, S.K.; Lam, B.; Lau, K.; Larkin, J., III. Th17 cells in immunity and autoimmunity. Clin. Dev. Immunol. 2013, 2013, 986789
16. Awasthi, A.; Kuchroo, V.K. Th17 cells: From precursors to players in inflammation and infection. Int. Immunol. 2009, 21, 489-498
17. Tanabe, S. The effect of probiotics and gut microbiota on Th17 cells. Int. Rev. Immunol. 2013, 32, 511-525
18. Fitzpatrick, L.R. Novel pharmacological approaches for inflammatory bowel disease: Targeting key intracellular pathways and the IL-23/IL-17 axis. Int. J. Inflamm. 2012, 2012, 389404
19. Annunziato, F.; Cosmi, L.; Liotta, F.; Maggi, E.; Romagnani, S. The phenotype of human Th17 cells and their precursors, the cytokines that mediate their differentiation and the role of Th17 cells in inflammation. Int. Immunol. 2008, 20, 1361-1368
20. Jin W.; Dong, C. IL-17 cytokines in immunity and inflammation. Emerg. Microbes Infect. 2013, 2, e60
21. Kinugasa, T.; Sakaguchi, T.; Gu, X.; Reinecker, H.C. Claudins regulate the intestinal barrier in response to immune mediators. Gastroenterology 2000, 118, 1001-1011
22. Ogawa, A.; Andoh, A.; Araki, Y.; Bamba, T.; Fujiyama, Y. Neutralization of interleukin-17 aggravates dextran sulfate sodium-induced colitis in mice. Clin. Immunol. 2004, 110, 55-62
23. Strzępa, A.; Szczepanik, M. IL-17-expressing cells as a potential therapeutic target for treatment of immunological disorders. Pharmacol. Rep. 2011, 63, 30-44
24. O’Connor, W., Jr.; Kamanaka, M.; Booth, C.J.; Town, T.; Nakae, S.; Iwakura, Y.; Kolls, J.K.; Flavell, R.A. A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat. Immunol. 2009, 10, 603-609
25. Yang, X.O.; Chang, S.H.; Park, H.; Nurieva, R.; Shah, B.; Acero, L.; Wang, Y.H.; Schluns, K.S.; Broaddus, R.R.; Zhu, Z.; et al. Regulation of inflammatory responses by IL-17F. J. Exp. Med. 2008, 205, 1063-1075
26. Tanabe, S.; Kinuta, Y.; Saito, Y. Bifidobacterium infantis suppresses proinflammatory interleukin-17 production in murine splenocytes and dextran sodium sulfate-induced intestinal inflammation. Int. J. Mol. Med. 2008, 22, 181-185
27. Griffin, G.K.; Newton, G.; Tarrio, M.L.; Bu, D.X.; Maganto-Garcia, E.; Azcutia, V.; Alcaide, P.; Grabie, N.; Luscinskas, F.W.; Croce, K.J.; et al. IL-17 and TNF-α sustain neutrophil recruitment during inflammation through synergistic effects on endothelial activation. J. Immunol. 2012, 15, 6287-6299
28. Taylor, P.R.; Roy, S.; Leal, S.M.; Sun, Y.; Howell, S.J.; Cobb, B.A.; Li, X.; Pearlman, E. Activation of neutrophils by autocrine IL-17A-IL-17RC interactions during fungal infection is regulated by IL-6, IL-23, RORγt and dectin-2. Nat. Immunol. 2014, 15, 143-152
29. Prause, O.; Miyamoto, M.; Sjöstrand, M.; Laan, M.; Lötvall, J.; Lindén, A. Endogenous IL-17 as a mediator of neutrophil recruitment caused by endotoxin exposure in mouse airways. J. Immunol. 2003, 170, 4665-4672
30. Neurath, M.F.; Atreya, R. Molecular pathways controlling barrier function in IBD. Nat. Rev. Gastroenterol. Hepatol. 2015, 12, 67-68
31. Hedin, C.; Whelan, K.; Lindsay, J.O. Evidence for the use of probiotics and prebiotics in inflammatory bowel disease: A review of clinical trials. Proc. Nutr. Soc. 2007, 66, 307-315
32. Miyauchi, E.; Ogita, T.; Miyamoto, J.; Kawamoto, S.; Morita, H.; Ohno, H.; Suzuki, T.; Tanabe, S. Bifidobacterium longum alleviates dextran sulfate sodium-induced colitis by suppressing IL-17A response: Involvement of intestinal epithelial costimulatory molecules. PLoS ONE 2013, 8, e79735
33. Ghadimi, D.; Helwig, U.; Schrezenmeir, J.; Heller, K.J.; de Vrese, M. Epigenetic imprinting by commensal probiotics inhibits the IL-23/IL-17 axis in an in vitro model of the intestinal mucosal immune system. J. Leukoc. Biol. 2012, 92, 895-911
34. Dotan, I.; Allez, M.; Nakazawa, A.; Brimnes, J.; Schulder-Katz, M.; Mayer, L. Intestinal epithelial cells from inflammatory bowel disease patients preferentially stimulate CD4+ T cells to proliferate and secrete interferon-γ. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 292, G1630-G1640
35. Dubinsky, M.C.; Wang, D.; Picornell, Y.; Wrobel, I.; Katzir, L.; Quiros, A.; Dutridge, D.; Wahbeh, G.; Silber, G.; Bahar, R.; et al. IL-23 receptor (IL-23R) gene protects against pediatric Crohn’s disease. Inflamm. Bowel Dis. 2007, 13, 511-515
36. Siakavellas, S.I.; Bamias, G. Role of the IL-23/IL-17 axis in Crohn’s disease. Discov. Med. 2012, 14, 253-262
37. Bogaert, S.; Lauens, D.; Peeters, H.; Melis, L.; Olievier1, K.; Boon, N.; Verbruggen, G.; Vandesompele, J.; Elewaut, D.; de Vos, M. Differential mucosal expression of Th17-related genes between the inflamed colon and ileum patients with inflammatory bowel disease. BMC Immunol. 2010, 11, 1-12
38. Seiderer, J.; Elben, I.; Diegelmann, J.; Glas, J.; Stallhofer, J.; Tillack, C.; Pfennig, S.; Jürgens, M.; Schmechel, S.; Konrad, A.; et al. Role of the novel Th17 cytokine IL-17F in inflammatory bowel disease (IBD): Upregulated colonic IL-17F expression in active Crohn’s disease and analysis of the IL17F p.His161Arg polymorphism in IBD. Inflamm. Bowel Dis. 2008, 14, 437-445
39. Takahashi, N.; Vereecke, L.; Bertrand, M.J.; Duprez, L.; Berger, S.B.; Divert, T.; Gonçalves, A.; Sze, M.; Gilbert, B.; Kourula, S.; et al. RIPK1 ensures intestinal homeostasis by protecting the epithelium against apoptosis. Nature 2014, 513, 95-99
40. Sanders, M.E.; Guarner, F.; Guerrant, R.; Holt, P.R.; Quigley, E.M.; Sartor, R.B.; Sherman, P.M.; Mayer, E.A. An update on the use and investigation of probiotics in health and disease. Gut 2013, 62, 787-796
41. Spiller, R. Review article: Probiotics and prebiotics in irritable bowel syndrome. Aliment. Pharmacol. Ther. 2008, 28, 385-396
42. Dupaul-Chicoine, J.; Dagenais, M.; Saleh, M. Crosstalk between the intestinal microbiota and the innate immune system in intestinal homeostasis and inflammatory bowel disease. Inflamm. Bowel Dis. 2013, 19, 2227-2237
43. Abraham, C.; Medzhitov, R. Interactions between the host innate immune system and microbes in inflammatory bowel disease. Gastroenterology 2011, 140, 1729-1737
44. Bien, J.; Palagani, V.; Bozko, P. The intestinal microbiota dysbiosis and Clostridium difficile infection: Is there a relationship with inflammatory bowel disease? Ther. Adv. Gastroenterol. 2013, 6, 53-68
45. Shanahan, F. Probiotics and inflammatory bowel disease: From fads and fantasy to facts and future. Br. J. Nutr. 2002, 88, S5-S9
46. Lepage, P.; Häsler, R.; Spehlmann, M.E.; Rehman, A.; Zvirbliene, A.; Begun, A.; Ott, S.; Kupcinskas, L.; Doré, J.; Raedler, A.; et al. Twin study indicates loss of interaction between microbiota and mucosa of patients with ulcerative colitis. Gastroenterology 2011, 141, 227-236
47. Takaishi, H.; Matsuki, T.; Nakazawa, A.; Takada, T.; Kado, S.; Asahara, T.; Kamada, N.; Sakuraba, A.; Yajima, T.; Higuchi, H.; et al. Imbalance in intestinal microflora constitution could be involved in the pathogenesis of inflammatory bowel disease. Int. J. Med. Microbiol. 2008, 298, 463-472
48. Yoon, H.; Yoon, Y.-S.; Kim, M.-S.; Chung, M.J.; Yum, D.Y. A probiotic preparation duolac-gold ameliorates dextran sulphate sodium-induced mouse colitis by downregulating the expression of IL-6. Toxicol. Res. 2014, 30, 27-32
49. Heuvelin, E.; Lebreton, C.; Grangette, C.; Pot, B.; Cerf-Bensussan, N.; Heyman, M. Mechanisms involved in alleviation of intestinal inflammation by Bifidobacterium breve soluble factors. PLoS ONE 2009, 4, e5184
50. Peran, L.; Camuesco, D.; Comalada, M.; Nieto, A.; Concha, A.; Adrio, J.L.; Olivares, M.; Xaus, J.; Zarzuelo, A.; Galvez, J. Lactobacillus fermentum, a probiotic capable to release glutathione, prevents colonic inflammation in the TNBS model of rat colitis. Int. J. Colorectal Dis. 2006, 21, 737-746
51. Damaskos, D.; Kolios, G. Probiotics and prebiotics in inflammatory bowel disease: Microflora “on the scope”. Br. J. Clin. Pharmacol. 2008, 65, 453-467
52. Ewaschuk, J.B.; Dieleman, L.A. Probiotics and prebiotics in chronic inflammatory bowel diseases. World J. Gastroenterol. 2006, 12, 5941-5950
53. 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
54. Ford, A.C.; Quigley, E.M.; Lacy, B.E.; Lembo, A.J.; Saito, Y.A.; Schiller, L.R.; Soffer, E.E.; Spiegel, B.M.; Moayyedi, P. Efficacy of prebiotics, probiotics, and synbiotics in irritable bowel syndrome and chronic idiopathic constipation: Systematic review and meta-analysis. Am. J. Gastroenterol. 2014, 1547-1561
55. Zocco, M.; Dal Verme, L.Z.; Cremonini, F.; Piscaglia, A.C.; Nista, E.C.; Candelli, M.; Novi, M.; Rigante, D.; Cazzato, I.A.; Ojetti, V.; et al. Efficacy of Lactobacillus GG in maintaining remission of ulcerative colitis. Aliment. Pharmacol. Ther. 2006, 23, 1567-1574
56. Ishikawa, H.; Akedo, I.; Umesaki, Y.; Tanaka, R.; Imaoka, A.; Otani, T. Randomized controlled trial of the effect of bifidobacteria-fermented milk on ulcerative colitis. J. Am. Coll. Nutr. 2003, 22, 56-63
57. Bibiloni, R.; Fedorak, R.N.; Tannock, G.W.; Madsen, K.L.; Gionchetti, P.; Campieri, M.; de Simone, C.; Sartor, R.B. VSL#3 Probiotic-mixture induces remission in patients with active ulcerative colitis. Am. J. Gastroenterol. 2005, 100, 1539-1546
58. Rembacken, B.; Snelling, A.; Hawkey, P.; 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
59. Campieri, M.; Rizzello, F.; Venturi, A.; Poggioli, G.; Ugolini, F. Combination of antibiotic and probiotic treatment is efficacious in prophylaxis of post-operative recurrence of Crohn’s disease: A randomized controlled study vs mesalamine. Gastroenterology 2000, 118, A178
60. Guslandi, M.; Mezzi, G.; Sorghi, M.; Testoni, P.A. Saccharomyces boulardii in maintenance treatment of Crohn’s disease. Dig. Dis. Sci. 2000, 45, 1462-1464
61. Prantera, C.; Scribano, M.; Falasco, G.; Andreoli, A.; Luzi, C. Ineffectiveness of probiotics in preventing recurrence after curative resection for Crohn’s disease: A randomised controlled trial with Lactobacillus GG. Gut 2002, 51, 405-409
62. Schultz, M.; Timmer, A.; Herfarth, H.H.; Sartor, R.B.; Vanderhoof, J.A.; Rath, H.C. Lactobacillus GG in inducing and maintaining remission of Crohn’s disease. BMC Gastroenterol. 2004, 4, 5
63. Bousvaros, A.; Guandalini, S.; Baldassano, R.N.; Botelho, C.; Evans, J.; Ferry, G.D.; Goldin, B.; Hartigan, L.; Kugathasan, S.; Levy, J.; et al. A randomized, double-blind trial of Lactobacillus GG versus placebo in addition to standard maintenance therapy for children with Crohn’s disease. Inflamm. Bowel Dis. 2005, 11, 833-839
64. Gupta, P.; Andrew, H.; Kirschner, B.S.; Guandalini, S. Is Lactobacillus GG helpful in children with Crohn’s disease? Results of a preliminary, open-label study. J. Pediatr. Gastroenterol. Nutr. 2000, 31, 453-457
65. Marteau, P.; Lémann, M.; Seksik, P.; Laharie, D.; Colombel, J.F.; Bouhnik, Y.; Cadiot, G.; Soulé, J.C.; Bourreille, A.; Metman, E.; et al. Ineffectiveness of Lactobacillus johnsonii LA1 for prophylaxis of postoperative recurrence in Crohn’s disease: A randomised, double blind, placebo controlled GETAID trial. Gut 2006, 55, 842-847
66. Van Gossum, A.; Dewit, O.; Louis, E.; de Hertogh, G.; Baert, F.; Fontaine, F.; DeVos, M.; Enslen, M.; Paintin, M.; Franchimont, D. Multicenter randomized-controlled clinical trial of probiotics (Lactobacillus johnsonii, LA1) on early endoscopic recurrence of Crohn’s disease after ileocaecal resection. Inflamm. Bowel Dis. 2007, 13, 135-142
67. Gionchetti, P.; Rizzello, F.; Helwig, U.; Venturi, A.; Lammers, K.M.; Brigidi, P.; Vitali, B.; Poggioli, G.; Miglioli, M.; Campieri, M. Prophylaxis of pouchitis onset with probiotic therapy: A double-blind, placebo-controlled trial. Gastroenterology 2003, 124, 1202-1209
68. Mimura, T.; Rizzello, F.; Helwig, U.; Poggioli, G.; Schreiber, S.; Talbot, I.C.; Nicholls, R.J.; Gionchetti, P.; Campieri, M.; Kamm, M.A. Once daily high dose probiotic therapy (VSL#3) for maintaining remission in recurrent or refractory pouchitis. Gut 2004, 53, 108-114
69. Gosselink, M.P.; Schouten, W.R.; van Lieshout, L.M.; Hop, W.C.; Laman, J.D.; van Embden, J.G. Delay of the first onset of pouchitis by oral intake of the probiotic strain Lactobacillus rhamnosus GG. Dis. Colon Rectum. 2004, 47, 876-884
70. Shen, B.; Brzezinski, A.; Fazio, V.W.; Remzi, F.H.; Achkar, J.P.; Bennett, A.E.; Sherman, K.; Lashner, B.A. Maintenance therapy with a probiotic in antibiotic-dependent pouchitis: Experience in clinical practice. Aliment. Pharmacol. Ther. 2005, 22, 721-728
71. Kuisma, J.; Mentula, S.; Jarvinen, H.; Kahri, A.; Saxelin, M.; Farkkila, M. Effect of Lactobacillus rhamnosus GG on ileal pouch inflammation and microbial flora. Aliment. Pharmacol. Ther. 2003, 17, 509-515
72. 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
73. Zoumpopoulou, G.; Foligne, B.; Christodoulou, K.; Grangetteb, C.; Potb, B.; Tsakalidou E. 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
74. Mañé, J.; Lorén, V.; Pedrosa, E.; Ojanguren, I.; Xaus, J.; Cabré, E.; Domènech, E.; Gassull, M.A. Lactobacillus fermentum CECT 5716 prevents and reverts intestinal damage on TNBS-induced colitis in mice. Inflamm. Bowel Dis. 2009, 15, 1155-1163
75. Chen, L.-L.; Zou, Y.-Y.; Lu, F.-G.; Li, F.J.; Lian, G.H. Efficacy profiles for different concentrations of Lactobacillus acidophilus in experimental colitis. World J. Gastroenterol. 2013, 19, 5347-5356
76. Sans, M. Probiotics for inflammatory bowel disease: A critical appraisal. Dig. Dis. 2009, 27, 111-114
77. Rolhion, N.; Darfeuille-Michaud, A. Adherent-invasive Escherichia coli in inflammatory bowel disease. Inflamm. Bowel Dis. 2007, 13, 1277-1283
78. Bartlett, J.G. Clostridium difficile: Old and new observations. J. Clin. Gastroenterol. 2007, 41, S24-S29
79. Venturi, A.; Gionchetti, P.; Rizzello, F.; Johansson, R.; Zucconi, E.; Brigidi, P.; Matteuzzi, D.; Campieri, M. Impact on the composition of the faecal ora by a new probiotic preparation: Preliminary data on maintenance treatment of patients with ulcerative colitis. Aliment. Pharmacol. Ther. 1999, 13, 1103-1108
80. Venkatraman, A.; Ramakrishna, B.; Pulimood, A.B.; Patra, S.; Murthy, S. Increased permeability in dextran sulphate colitis in rats: Time course of development and effect of butyrate. Scand. J. Gastroenterol. 2000, 35, 1053-1059
81. Claes, I.J.; de Keersmaecker, S.C.; Vanderleyden, J.; Lebeer, S. Lessons from probiotic—Host interaction studies in murine models of experimental colitis. Mol. Nutr. Food Res. 2011, 55, 1441-1453
82. Ogita, T.; Tanii, Y.; Morita, H.; Suzuki, T.; Tanabe, S. Suppression of Th17 response by Streptococcus thermophilus ST28 through induction of IFN-γ. Int. J. Mol. Med. 2011, 28, 817-822
83. Fitzpatrick, L.R.; Deml, L.; Hofmann, C.; Small, J.S.; Groeppel, M.; Hamm, S.; Lemstra, S.; Leban, J.; Ammendola, A. 4SC-101, a novel immunosuppressive drug, inhibits IL-17 and attenuates colitis in two murine models of inflammatory bowel disease. Inflamm. Bowel Dis. 2010, 16, 1763-1777
84. Fitzpatrick, L.R.; Small, J.S.; Doblhofer, R.; Ammendola, A. Vidofludimus inhibits colonic interleukin-17 and improves hapten-induced colitis in rats by a unique dual mode of action. J. Pharmacol. Exp. Ther. 2012, 342, 850-860
85. Iwakura, Y.; Ishigame, H. The IL-23/IL-17 axis in inflammation. J. Clin. Investig. 2006, 116, 1218-1222
86. Mangan, P.R.; Harrington, L.E.; O’Quinn, D.B.; Helms, W.S.; Bullard, D.C.; Elson, C.O.; Hatton, R.D.; Wahl, S.M.; Schoeb, T.R.; Weaver, C.T. Transforming growth factor-β induces development of the Th17 lineage. Nature 2006, 441, 231-234
87. Kumar, N.; Navalpur, S.; Balamurugan, R.; Pulimood, A.; Pugazhendhi, S.; Ramakrishna, B.S. Probiotic administration alters the gut flora and attenuates colitis in mice administered dextran sodium sulfate. J. Gastroenterol. Hepatol. 2008, 23, 1834-1839
88. Mach, T. Clinical usefulness of probiotics. J. Physiol. Pharmacol. 2006, 57, 23-33
89. Ueno, N.; Fujiya, M.; Segawa, S.; Nata, T.; Moriichi, K.; Tanabe, H.; Mizukami, Y.; Kobayashi, N.; Ito, K.; Kohgo, Y. Heat-killed body of Lactobacillus brevis SBC8803 ameliorates intestinal injury in a murine model of colitis by enhancing the intestinal barrier function. Inflamm. Bowel Dis. 2011, 17, 2235-2250
90. Lee, H.-S.; Han, S.-Y.; Bae, E.-A.; Huh, C.S.; Ahn, Y.T.; Lee, J.H.; Kim, D.H. 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
91. Roselli, M.; Finamore, A.; Nuccitelli, S.; Carnevali, P.; Brigidi, P.; Vitali, B.; Nobili, F.; Rami, R.; Garaguso, I.; Mengheri, E. Prevention of TNBS-induced colitis by different Lactobacillus and Bifidobacterium strains is associated with an expansion of γδT and regulatory T cells of intestinal intraepithelial lymphocytes. Inflamm. Bowel Dis. 2009, 15, 1526-1536
92. Peran, L.; Sierra, S.; Comalada, M.; Lara-Villoslada, F.; Bailón, E.; Nieto, A.; Concha, A.; Olivares, M.; Zarzuelo, A.; Xaus, J.; et al. A comparative study of the preventative effects exerted by two probiotics, Lactobacillus reuteri and Lactobacillus fermentum, in the trinitrobenzenesulfonic acid model of rat colitis. Br. J. Nutr. 2007, 97, 96-103
93. Peran, L.; Camuesco, D.; Comalada, M.; Nieto, A.; Concha, A.; Diaz-Ropero, M.P.; Olivares, M.; Xaus, J.; Zarzuelo, A.; Galvez, J. Preventative effects of a probiotic, Lactobacillus salivarius ssp. salivarius, in the TNBS model of rat colitis. World J. Gastroenterol. 2005, 11, 5185-5192
94. Gad, M.; Ravn, P.; Søborg, D.A.; Lund-Jensen, K.; Ouwehand, A.C.; Jensen, S.S. Regulation of the IL-10/IL-12 axis in human dendritic cells with probiotic bacteria. FEMS Immunol. Med. Microbiol. 2011, 63, 93-107
95. Shida, K.; Nanno, M.; Nagata, S. Flexible cytokine production by macrophages and T cells in response to probiotic bacteria: A possible mechanism by which probiotics exert multifunctional immune regulatory activities. Gut Microbes 2011, 2, 109-114
96. Latvala, S.; Miettinen, M.; Kekkonen, R. A.; Korpela, R.; Julkunen, I. Lactobacillus rhamnosus GG and Streptococcus thermophilus induce suppressor of cytokine signalling 3 (SOCS3) gene expression directly and indirectly via interleukin-10 in human primary macrophages. Clin. Exp. Immunol. 2011, 165, 94-103
97. Hart, A.L.; Lammers, K.; Brigidi, P.; Vitali, B.; Rizzello, F.; Gionchetti, P.; Campieri, M.; Kamm, M.A.; Knight, S.C.; Stagg, A.J. Modulation of human dendritic cell phenotype and function by probiotic bacteria. Gut 2004, 53, 1602-1609
98. You, J.; Yaqoob, P. Evidence of immunomodulatory effects of a novel probiotic, Bifidobacterium longum bv. infantis CCUG 52486. FEMS Immunol. Med. Microbiol. 2012, 66, 353-362
99. Chen, R.B.Y. Insights from mouse models of colitis, J. Leukoc. Biol. 2000, 67, 267-278
100. Annunziato, S.R.F. Do studies in humans better depict Th17 cells? Blood 2009, 114, 2213-2219
101. Hershberg, R.M.; Mayer, L.F. Antigen processing and presentation by intestinal epithelial cells—Polarity and complexity. Immunol. Today 2000, 21, 123-128
102. Westendorf, A.M.; Fleissner, D.; Groebe, L.; Jung, S.; Gruber, A.D.; Hansen, W.; Buer J. CD4+ Foxp3+ regulatory T cell expansion induced by antigen-driven interaction with intestinal epithelial cells independent of local dendritic cells. Gut 2009, 58, 211-219
103. Borcherding, F.; Nitschke, M.; Hundorfean, G.; Rupp, J.; von Smolinski, D.; Bieber, K.; van Kooten, C.; Lehnert, H.; Fellermann, K.; Büning, J. The CD40-CD40L pathway contributes to the proinflammatory function of intestinal epithelial cells in inflammatory bowel disease. Am. J. Pathol. 2010, 176, 1816-1827
104. Ivanov, I.I.; McKenzie, B.S.; Zhou, L.; Tadokoro1, C.E.; Lepelley, A.; Lafaille, J.J.; Cua, D.J.; Littman, D.R. The orphan nuclear receptor RORγt directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006, 126, 1121-1133
105. Yang, X.O.; Panopoulos, A.D.; Nurieva, R.; Chang, S.H.; Wang, D.; Watowich, S.S.; Dong, C. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J. Biol. Chem. 2007, 282, 9358-9363
106. Ghadimi, D.; de Vrese, M.; Heller, K.J.; Schrezenmeir, J. Effect of natural commensal-origin DNA on toll-like receptor 9 (TLR9) signaling cascade, chemokine IL-8 expression, and barrier integritiy of polarized intestinal epithelial cells. Inflamm. Bowel Dis. 2010, 16, 410-427
107. Menard, S.; Candalh, C.; Bambou, J.C.; Terpend, N. Lactic acid bacteria secrete metabolites retaining anti-inflammatory properties after intestinal transport. Gut 2004, 53, 821-828
108. Atarashi, T.T.K.; Honda, K. Induction of lamina propria Th17 cells by intestinal commensal bacteria. Vaccine 2010, 28, 8036-8038
109. Atarashi, K.T.K.; Honda, K. Mechanism of Th17 cell differentiation in the intestinal lamina propria, Inflamm. Regen. 2009, 29, 263-269