Tryptophan metabolite activation of the aryl hydrocarbon receptor regulates IL-10 receptor expression on intestinal epithelia

Candela, 2008, Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: adhesion properties, competition against enteropathogens and modulation of IL-8 production, Int. J. Food Microbiol., 125, 286, 10.1016/j.ijfoodmicro.2008.04.012 Lozupone, 2012, Diversity, stability and resilience of the human gut microbiota, Nature, 489, 220, 10.1038/nature11550 Fukuda, 2011, Bifidobacteria can protect from enteropathogenic infection through production of acetate, Nature, 469, 543, 10.1038/nature09646 Olszak, 2012, Microbial exposure during early life has persistent effects on natural killer T cell function, Science (New York, NY), 336, 489, 10.1126/science.1219328 Sonnenburg, 2005, Glycan foraging in vivo by an intestine-adapted bacterial symbiont, Science (New York, NY), 307, 1955, 10.1126/science.1109051 Xavier, 2007, Unravelling the pathogenesis of inflammatory bowel disease, Nature, 448, 427, 10.1038/nature06005 Chaudhry, 2011, Interleukin-10 signaling in regulatory T cells is required for suppression of Th17 cell-mediated inflammation, Immunity, 34, 566, 10.1016/j.immuni.2011.03.018 Kuhn, 1993, Interleukin-10-deficient mice develop chronic enterocolitis, Cell, 75, 263, 10.1016/0092-8674(93)80068-P Pils, 2010, Monocytes/macrophages and/or neutrophils are the target of IL-10 in the LPS endotoxemia model, Eur. J. Immunol., 40, 443, 10.1002/eji.200939592 Engelhardt, 2014, IL-10 in humans: lessons from the gut, IL-10/IL-10 receptor deficiencies, and IL-10 polymorphisms, Curr. Top. Microbiol. Immunol., 380, 1 Glocker, 2009, Inflammatory bowel disease and mutations affecting the interleukin-10 receptor, N. Engl. J. Med., 361, 2033, 10.1056/NEJMoa0907206 Loren, 2015, Interleukin-10 enhances the intestinal epithelial barrier in the presence of corticosteroids through p38 MAPK activity in Caco-2 Monolayers: a possible mechanism for steroid responsiveness in ulcerative colitis, PLoS One, 10, e0130921, 10.1371/journal.pone.0130921 Kominsky, 2014, IFN-gamma-mediated induction of an apical IL-10 receptor on polarized intestinal epithelia, J. Immunol. (Baltimore, MD: 1950), 192, 1267, 10.4049/jimmunol.1301757 Mankertz, 2000, Expression from the human occludin promoter is affected by tumor necrosis factor alpha and interferon gamma, J. Cell Sci., 113, 2085, 10.1242/jcs.113.11.2085 Youakim, 1999, Interferon-gamma decreases barrier function in T84 cells by reducing ZO-1 levels and disrupting apical actin, Am. J. Physiol., 276, G1279 Yoshida, 1981, Induction of pulmonary indoleamine 2,3-dioxygenase by interferon, Proc. Natl Acad. Sci. USA, 78, 129, 10.1073/pnas.78.1.129 Yasui, 1986, Interferon enhances tryptophan metabolism by inducing pulmonary indoleamine 2,3-dioxygenase: its possible occurrence in cancer patients, Proc. Natl Acad. Sci. USA, 83, 6622, 10.1073/pnas.83.17.6622 Higuchi, 1967, Enzymic formation of D-kynurenine from D-tryptophan, Arch. Biochem. Biophys., 120, 397, 10.1016/0003-9861(67)90256-1 Munn, 1999, Inhibition of T cell proliferation by macrophage tryptophan catabolism, J. Exp. Med., 189, 1363, 10.1084/jem.189.9.1363 Matteoli, 2010, Gut CD103+ dendritic cells express indoleamine 2,3-dioxygenase which influences T regulatory/T effector cell balance and oral tolerance induction, Gut, 59, 595, 10.1136/gut.2009.185108 Nguyen, 2010, Aryl hydrocarbon receptor negatively regulates dendritic cell immunogenicity via a kynurenine-dependent mechanism, Proc. Natl Acad. Sci. USA, 107, 19961, 10.1073/pnas.1014465107 Pallotta, 2011, Indoleamine 2,3-dioxygenase is a signaling protein in long-term tolerance by dendritic cells, Nat. Immunol., 12, 870, 10.1038/ni.2077 Ciorba, 2010, Induction of IDO-1 by immunostimulatory DNA limits severity of experimental colitis, J. Immunol. (Baltimore, MD: 1950), 184, 3907, 10.4049/jimmunol.0900291 Muzaki, 2015, Intestinal CD103CD11b dendritic cells restrain colitis via IFN-gamma-induced anti-inflammatory response in epithelial cells, Mucosal Immunol., 9, 336, 10.1038/mi.2015.64 Thaker, 2013, IDO1 metabolites activate beta-catenin signaling to promote cancer cell proliferation and colon tumorigenesis in mice, Gastroenterology, 145, 416, 10.1053/j.gastro.2013.05.002 Opitz, 2011, An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor, Nature, 478, 197, 10.1038/nature10491 Bessede, 2014, Aryl hydrocarbon receptor control of a disease tolerance defence pathway, Nature, 511, 184, 10.1038/nature13323 Fernandez-Salguero, 1996, Aryl-hydrocarbon receptor-deficient mice are resistant to 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced toxicity, Toxicol. Appl. Pharmacol., 140, 173, 10.1006/taap.1996.0210 Gielen, 1972, Genetic regulation of aryl hydrocarbon hydroxylase induction. II. Simple Mendelian expression in mouse tissues in vivo, J. Biol. Chem., 247, 1125, 10.1016/S0021-9258(19)45624-X Nguyen, 2008, The search for endogenous activators of the aryl hydrocarbon receptor, Chem. Res. Toxicol., 21, 102, 10.1021/tx7001965 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 Monteleone, 2011, Aryl hydrocarbon receptor-induced signals up-regulate IL-22 production and inhibit inflammation in the gastrointestinal tract, Gastroenterology, 141, e231, 10.1053/j.gastro.2011.04.007 Mascanfroni, 2015, Metabolic control of type 1 regulatory T cell differentiation by AHR and HIF1-alpha, Nat. Med., 21, 638, 10.1038/nm.3868 Heller, 2011, Nuclear receptors take center stage in Th17 cell-mediated autoimmunity, J. Clin. Invest., 121, 519, 10.1172/JCI45939 Kimura, 2008, Aryl hydrocarbon receptor regulates Stat1 activation and participates in the development of Th17 cells, Proc. Natl Acad. Sci. USA, 105, 9721, 10.1073/pnas.0804231105 Colgan, 2016, Hypoxia and mucosal inflammation, Ann. Rev. Pathol., 11, 77, 10.1146/annurev-pathol-012615-044231 Taylor, 1991, Relationship between interferon-gamma, indoleamine 2,3-dioxygenase, and tryptophan catabolism, FASEB J., 5, 2516, 10.1096/fasebj.5.11.1907934 Kominsky, 2011, An endogenously anti-inflammatory role for methylation in mucosal inflammation identified through metabolite profiling, J. Immunol. (Baltimore, MD: 1950), 186, 6505, 10.4049/jimmunol.1002805 Kontoyiannis, 1999, Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies, Immunity, 10, 387, 10.1016/S1074-7613(00)80038-2 Poland, 1976, 3,4,3‘,4‘-Tetrachloro azoxybenzene and azobenzene: potent inducers of aryl hydrocarbon hydroxylase, Science (New York, NY), 194, 627, 10.1126/science.136041 Wincent, 2012, Inhibition of cytochrome P4501-dependent clearance of the endogenous agonist FICZ as a mechanism for activation of the aryl hydrocarbon receptor, Proc. Natl Acad. Sci. USA, 109, 4479, 10.1073/pnas.1118467109 Bacsi, 1995, Orientation of the heterodimeric aryl hydrocarbon (dioxin) receptor complex on its asymmetric DNA recognition sequence, Mol. Pharmacol., 47, 432 Ji, 2015, Aryl hydrocarbon receptor activation down-regulates IL-7 and reduces inflammation in a mouse model of DSS-induced colitis, Dig. Dis. Sci., 60, 1958, 10.1007/s10620-015-3632-x Kelchtermans, 2008, How interferon-gamma keeps autoimmune diseases in check, Trends Immunol., 29, 479, 10.1016/j.it.2008.07.002 Sheikh, 2010, Cutting edge: IFN-gamma is a negative regulator of IL-23 in murine macrophages and experimental colitis, J. Immunol. (Baltimore, MD: 1950), 184, 4069, 10.4049/jimmunol.0903600 Carlin, 1989, Interferons and indoleamine 2,3-dioxygenase: role in antimicrobial and antitumor effects, Experientia, 45, 535, 10.1007/BF01990503 MacKenzie, 1999, Inhibition of indoleamine 2,3-dioxygenase in human macrophages inhibits interferon-gamma-induced bacteriostasis but does not abrogate toxoplasmastasis, Eur. J. Immunol., 29, 3254, 10.1002/(SICI)1521-4141(199910)29:10<3254::AID-IMMU3254>3.0.CO;2-0 Poland, 1974, Genetic expression of aryl hydrocarbon hydroxylase activity. Induction of monooxygenase activities and cytochrome P1-450 formation by 2,3,7,8-tetrachlorodibenzo-p-dioxin in mice genetically “nonresponsive” to other aromatic hydrocarbons, J. Biol. Chem., 249, 5599, 10.1016/S0021-9258(20)79769-3 Xu, 2005, Induction of phase I, II and III drug metabolism/transport by xenobiotics, Arch. Pharm. Res., 28, 249, 10.1007/BF02977789 Fernandez-Salguero, 1995, Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor, Science (New York, NY), 268, 722, 10.1126/science.7732381 Esser, 2009, The aryl hydrocarbon receptor in immunity, Trends Immunol., 30, 447, 10.1016/j.it.2009.06.005 Esser, 2015, The aryl hydrocarbon receptor in barrier organ physiology, immunology, and toxicology, Pharmacol. Rev., 67, 259, 10.1124/pr.114.009001 Li, 2011, Exogenous stimuli maintain intraepithelial lymphocytes via aryl hydrocarbon receptor activation, Cell, 147, 629, 10.1016/j.cell.2011.09.025 Gupta, 2012, Serum analysis of tryptophan catabolism pathway: correlation with Crohn's disease activity, Inflamm. Bowel Dis, 18, 1214, 10.1002/ibd.21849 Albrecht, 2014, Metabolite profiling reveals new insights into the regulation of serum urate in humans, Metabolomics, 10, 141, 10.1007/s11306-013-0565-2 Walisser, 2005, Aryl hydrocarbon receptor-dependent liver development and hepatotoxicity are mediated by different cell types, Proc Natl Acad Sci USA, 102, 17858, 10.1073/pnas.0504757102 Frick, 2009, Contribution of adenosine A2B receptors to inflammatory parameters of experimental colitis, J. Immunol., 182, 4957, 10.4049/jimmunol.0801324 Tomita, 2000, Conditional disruption of the aryl hydrocarbon receptor nuclear translocator (Arnt) gene leads to loss of target gene induction by the aryl hydrocarbon receptor and hypoxia-inducible factor 1alpha, Mol. Endocrinol., 14, 1674 Dieleman, 1998, Chronic experimental colitis induced by dextran sulphate sodium (DSS) is characterized by Th1 and Th2 cytokines, Clin. Exp. Immunol., 114, 385, 10.1046/j.1365-2249.1998.00728.x Pfaffl, 2001, A new mathematical model for relative quantification in real-time RT-PCR, Nucleic Acids Res., 29, e45, 10.1093/nar/29.9.e45