Induction of Colonic Regulatory T Cells by Mesalamine by Activating the Aryl Hydrocarbon Receptor

Kyoko Oh-oka1, Yuko Kojima2, Koichiro Uchida3, Kimiko Yoda4, Kayoko Ishimaru1, Shotaro Nakajima1, Jun Hemmi5, Hiroshi Kano5, Yoshiaki Fujii-Kuriyama6, Ryohei Katoh4, Hiroyuki Ito5, Atsuhito Nakao1,3
1Department of Immunology, Faculty of Medicine, University of Yamanashi, Yamanashi, Japan
2The Laboratory of Morphology and Image Analysis, Research Support Center, Juntendo University School of Medicine, Tokyo, Japan
3Atopy Research Center, Juntendo University School of Medicine, Tokyo, Japan
4Department of Pathology, Faculty of Medicine, University of Yamanashi, Yamanashi, Japan
5Food Science Research Laboratories, Division of Research and Development, Meiji Co, Ltd, Kanagawa, Japan
6Medical Research Institute, Tokyo Medical and Dental University Tokyo Japan

Tài liệu tham khảo

Hauso, 2015, 5-Aminosalicylic acid, a specific drug for ulcerative colitis, Scand J Gastroenterology, 50, 933, 10.3109/00365521.2015.1018937 Perrotta, 2015, Five-aminosalicylic acid: an update for the reappraisal of an old drug, Gastroenterol Res Pract, 2015, 456895, 10.1155/2015/456895 Bohm, 2014, Long-term efficacy and safety of once-daily mesalazine granules for the treatment of active ulcerative colitis, Clin Exp Gastroenterol, 7, 369, 10.2147/CEG.S35691 Stolfi, 2013, Mechanisms of action of non-steroidal anti-inflammatory drugs (NSAIDs) and mesalazine in the chemoprevention of colorectal cancer, Int J Mol Sci, 14, 17972, 10.3390/ijms140917972 Ohkura, 2013, Development and maintenance of regulatory T cells, Immunity, 38, 414, 10.1016/j.immuni.2013.03.002 Tanoue, 2016, Development and maintenance of intestinal regulatory T cells, Nat Rev Immunol, 16, 295, 10.1038/nri.2016.36 Atarashi, 2011, Induction of colonic regulatory T cells by indigenous Clostridium species, Science, 331, 337, 10.1126/science.1198469 Liu, 2003, CD4+CD25+ regulatory T cells cure murine colitis: the role of IL-10, TGF-β, and CTLA4, J Immunol, 171, 5012, 10.4049/jimmunol.171.10.5012 Mottet, 2003, Cutting edge: cure of colitis by CD4+CD25+ regulatory T cells, J Immunol, 170, 3939, 10.4049/jimmunol.170.8.3939 Foussat, 2003, A comparative study between T regulatory type 1 and CD4+CD25+ T cells in the control of inflammation, J Immunol, 171, 5018, 10.4049/jimmunol.171.10.5018 Eastaff-Leung, 2010, Foxp3+ regulatory T cells, Th17 effector cells, and cytokine environment in inflammatory bowel disease, J Clin Immunol, 30, 80, 10.1007/s10875-009-9345-1 Pedros, 2016, Disrupted regulatory T cell homeostasis in inflammatory bowel diseases, World J Gastroenterol, 22, 974, 10.3748/wjg.v22.i3.974 Shale, 2013, CD4+ T-cell subsets in intestinal inflammation, Immunol Rev, 252, 164, 10.1111/imr.12039 Mimura, 1997, Loss of teratogenic response to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in mice lacking the Ah (dioxin) receptor, Genes Cells, 2, 645, 10.1046/j.1365-2443.1997.1490345.x Kasai, 2006, High levels of dioxin-like potential in cigarette smoke evidenced by in vitro and in vivo biosensing, Cancer Res, 66, 7143, 10.1158/0008-5472.CAN-05-4541 Cipriani, 2013, Activation of the bile acid receptor GPBAR1 protects against gastrointestinal injury caused by non-steroidal anti-inflammatory drugs and aspirin in mice, Br J Pharmacol, 168, 225, 10.1111/j.1476-5381.2012.02128.x Petersen, 2008, Oral administration of GW788388, an inhibitor of TGF-β type I and II receptor kinases, decreases renal fibrosis, Kidney Int, 73, 705, 10.1038/sj.ki.5002717 Tesseur, 2006, Highly sensitive and specific bioassay for measuring bioactive TGF-β, BMC Cell Biol, 7, 15, 10.1186/1471-2121-7-15 Cooper, 1993, Clinicopathologic study of dextran sulfate sodium experimental murine colitis, Lab Invest, 69, 238 Wang, 2016, Oral 5-aminosalicylic acid for maintenance of remission in ulcerative colitis, Cochrane Database Syst Rev, 5, CD000544 Hankinson, 1995, The aryl hydrocarbon receptor complex, Annu Rev Pharmacol Toxicol, 35, 307, 10.1146/annurev.pa.35.040195.001515 Mulero-Navarro, 2016, New trends in aryl hydrocarbon receptor biology, Front Cell Dev Biol, 4, 45, 10.3389/fcell.2016.00045 Singh, 2011, Activation of aryl hydrocarbon receptor (AhR) leads to reciprocal epigenetic regulation of FoxP3 and IL-17 expression and amelioration of experimental colitis, PLoS One, 6, e23522, 10.1371/journal.pone.0023522 Quintana, 2008, Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor, Nature, 453, 65, 10.1038/nature06880 Annes, 2003, Making sense of latent TGF-β activation, J Cell Sci, 116, 217, 10.1242/jcs.00229 Crawford, 1998, Thrombospondin-1 is a major activator of TGF-β1 in vivo, Cell, 93, 1159, 10.1016/S0092-8674(00)81460-9 Travis, 2007, Loss of integrin α(v)β8 on dendritic cells causes autoimmunity and colitis in mice, Nature, 449, 361, 10.1038/nature06110 Cong, 2009, A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota, Proc Natl Acad Sci U S A, 106, 19256, 10.1073/pnas.0812681106 Ohtsuka, 2000, Transforming growth factor-β: an important cytokine in the mucosal immune response, Curr Opin Gastroenterol, 16, 541, 10.1097/00001574-200011000-00014 Kiesler, 2015, Experimental models of inflammatory bowel diseases, Cell Mol Gastroenterol Hepatol, 1, 154, 10.1016/j.jcmgh.2015.01.006 Aumais, 2003, Rectal tissue, plasma and urine concentrations of mesalazine after single and multiple administrations of 500 mg suppositories to healthy volunteers and ulcerative proctitis patients, Aliment Pharmacol Ther, 17, 93, 10.1046/j.1365-2036.2003.01409.x Veldhoen, 2008, The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins, Nature, 453, 106, 10.1038/nature06881 Rijk, 1988, Disposition of 5-aminosalicylic acid by 5-aminosalicylic acid-delivering compounds, Scand J Gastroenterol, 23, 107, 10.3109/00365528809093858 Arpaia, 2013, Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation, Nature, 504, 451, 10.1038/nature12726 Smith, 2013, The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis, Science, 341, 569, 10.1126/science.1241165 Obata, 2014, The epigenetic regulator Uhrf1 facilitates the proliferation and maturation of colonic regulatory T cells, Nat Immunol, 15, 571, 10.1038/ni.2886 Geem, 2016, Contribution of mesenteric lymph nodes and GALT to the intestinal Foxp3+ regulatory T-Cell compartment, Cell Mol Gastroenterol Hepatol, 2, 274, 10.1016/j.jcmgh.2015.12.009 Lathrop, 2011, Peripheral education of the immune system by colonic commensal microbiota, Nature, 478, 250, 10.1038/nature10434 Quintana, 2010, An endogenous aryl hydrocarbon receptor ligand acts on dendritic cells and T cells to suppress experimental autoimmune encephalomyelitis, Proc Natl Acad Sci U S A, 107, 20768, 10.1073/pnas.1009201107 Nguyen, 2010, Aryl hydrocarbon receptor negatively regulates dendritic cell immunogenicity via a kynurenine-dependent mechanism, Proc Natl Acad Sci U S A, 107, 19961, 10.1073/pnas.1014465107 Dabir, 2008, Aryl hydrocarbon receptor is activated by glucose and regulates the thrombospondin-1 gene promoter in endothelial cells, Circ Res, 102, 1558, 10.1161/CIRCRESAHA.108.176990 Silginer, 2016, The aryl hydrocarbon receptor links integrin signaling to the TGF-β pathway, Oncogene, 35, 3260, 10.1038/onc.2015.387 Monteleone, 2012, The aryl hydrocarbon receptor in inflammatory bowel disease: linking the environment to disease pathogenesis, Curr Opin Gastroenterol, 28, 310, 10.1097/MOG.0b013e328352ad69 Takamura, 2010, Activation of the aryl hydrocarbon receptor pathway may ameliorate dextran sodium sulfate-induced colitis in mice, Immunol. Cell Biol, 88, 685, 10.1038/icb.2010.35 Benson, 2011, Aryl hydrocarbon receptor activation by TCDD reduces inflammation associated with Crohn's disease, Toxicol Sci, 120, 68, 10.1093/toxsci/kfq360 Furumatsu, 2011, A role of the aryl hydrocarbon receptor in attenuation of colitis, Dig Dis Sci, 56, 2532, 10.1007/s10620-011-1643-9 Sugimoto, 2016, Indole compounds may be promising medicines for ulcerative colitis, J Gastroenterol, 51, 853, 10.1007/s00535-016-1220-2 Fukumoto, 2014, Identification of a probiotic bacteria-derived activator of the aryl hydrocarbon receptor that inhibits colitis, Immunol Cell Biol, 92, 460, 10.1038/icb.2014.2 Rousseaux, 2005, Intestinal antiinflammatory effect of 5-aminosalicylic acid is dependent on peroxisome proliferator-activated receptor-gamma, J Exp Med, 201, 1205, 10.1084/jem.20041948 Wohlfert, 2007, Peroxisome proliferator-activated receptor-γ (PPAR-γ) and immunoregulation: enhancement of regulatory T cells through PPAR-γ-dependent and -independent mechanisms, J Immunol, 178, 4129, 10.4049/jimmunol.178.7.4129 Hontecillas, 2007, Peroxisome proliferator-activated receptor-γ is required for regulatory CD4+ T cell-mediated protection against colitis, J Immunol, 178, 2940, 10.4049/jimmunol.178.5.2940 Hawley, 2012, The ancient drug salicylate directly activates AMP-activated protein kinase, Science, 336, 918, 10.1126/science.1215327 Michalek, 2011, Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets, J Immunol, 186, 3299, 10.4049/jimmunol.1003613 Sridharan, 2014, Prediction and quantification of bioactive microbiota metabolites in the mouse gut, Nat Commun, 5, 5492, 10.1038/ncomms6492