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Gut Microbiota-Derived Tryptophan Metabolites Maintain Gut and Systemic Homeostasis

Xiaomin Su, Yunhuan Gao, Rongcun Yang

Cells · 2022 · Review · CC BY

doi:10.3390/cells11152296 (opens in a new tab)

Abstract

Tryptophan is an essential amino acid from dietary proteins. It can be metabolized into different metabolites in both the gut microbiota and tissue cells. Tryptophan metabolites such as indole-3-lactate (ILA), indole-3-acrylate (IAC), indole-3-propionate (IPA), indole-3-aldehyde (IAID), indoleacetic acid (IAA), indole-3-acetaldehyde and Kyn can be produced by intestinal microorganisms through direct Trp transformation and also, partly, the kynurenine (Kyn) pathway. These metabolites play a critical role in maintaining the homeostasis of the gut and systematic immunity and also potentially affect the occurrence and development of diseases such as inflammatory bowel diseases, tumors, obesity and metabolic syndrome, diseases in the nervous system, infectious diseases, vascular inflammation and cardiovascular diseases and hepatic fibrosis. They can not only promote the differentiation and function of anti-inflammatory macrophages, Treg cells, CD4+CD8αα+ regulatory cells, IL-10+ and/or IL-35+B regulatory cells but also IL-22-producing innate lymphoid cells 3 (ILC3), which are involved in maintaining the gut mucosal homeostasis. These findings have important consequences in the immunotherapy against tumor and other immune-associated diseases. We will summarize here the recent advances in understanding the generation and regulation of tryptophan metabolites in the gut microbiota, the role of gut microbiota-derived tryptophan metabolites in different immune cells, the occurrence and development of diseases and immunotherapy against immune-associated diseases.

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    Lee J.S., Cella M., McDonald K.G., Garlanda C., Kennedy G.D., Nukaya M., Mantovani A., Kopan R., Bradfield C.A., Newberry R.D., et al. AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch. Nat. Immunol. 2011;13:144-151.

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    Gomez de Aguero M., Ganal-Vonarburg S.C., Fuhrer T., Rupp S., Uchimura Y., Li H., Steinert A., Heikenwalder M., Hapfelmeier S., Sauer U., et al. The maternal microbiota drives early postnatal innate immune development. Science. 2016;351:1296-1302.

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    Ebihara T., Song C., Ryu S.H., Plougastel-Douglas B., Yang L., Levanon D., Groner Y., Bern M.D., Stappenbeck T.S., Colonna M., et al. Runx3 specifies lineage commitment of innate lymphoid cells. Nat. Immunol. 2015;16:1124-1133.

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    Li S., Heller J.J., Bostick J.W., Lee A., Schjerven H., Kastner P., Chan S., Chen Z.E., Zhou L. Ikaros Inhibits Group 3 Innate Lymphoid Cell Development and Function by Suppressing the Aryl Hydrocarbon Receptor Pathway. Immunity. 2016;45:185-197.

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    Kiss E.A., Vonarbourg C., Kopfmann S., Hobeika E., Finke D., Esser C., Diefenbach A. Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science. 2011;334:1561-1565.

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    Li S., Bostick J.W., Ye J., Qiu J., Zhang B., Urban J.F., Avram D., Zhou L. Aryl Hydrocarbon Receptor Signaling Cell Intrinsically Inhibits Intestinal Group 2 Innate Lymphoid Cell Function. Immunity. 2018;49:915-928.e5.

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    Chen W., Pu A., Sheng B., Zhang Z., Li L., Liu Z., Wang Q., Li X., Ma Y., Yu M., et al. Aryl hydrocarbon receptor activation modulates CD8αα+TCRαβ+ IELs and suppression of colitis manifestations in mice. Biomed. Pharmacother. 2017;87:127-134.

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    Wang J., Simonavicius N., Wu X., Swaminath G., Reagan J., Tian H., Ling L. Kynurenic acid as a ligand for orphan G protein-coupled receptor GPR35. J. Biol. Chem. 2006;281:22021-22028.

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    Frumento G., Rotondo R., Tonetti M., Damonte G., Benatti U., Ferrara G.B. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. J. Exp. Med. 2002;196:459-468.

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    Fallarino F., Grohmann U., Vacca C., Bianchi R., Orabona C., Spreca A., Fioretti M.C., Puccetti P. T cell apoptosis by tryptophan catabolism. Cell Death Differ. 2002;9:1069-1077.

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    Orabona C., Puccetti P., Vacca C., Bicciato S., Luchini A., Fallarino F., Bianchi R., Velardi E., Perruccio K., Velardi A., et al. Toward the identification of a tolerogenic signature in IDO-competent dendritic cells. Blood. 2006;107:2846-2854.

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    Lanz T.V., Becker S., Mohapatra S.R., Opitz C.A., Wick W., Platten M. Suppression of Th1 differentiation by tryptophan supplementation in vivo. Amino Acids. 2017;49:1169-1175.

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    Bacterial Metabolite Indole Modulates Incretin Secretion from Intestinal Enteroendocrine L Cells · 2014
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    Whitfield-Cargile C.M., Cohen N.D., Chapkin R.S., Weeks B.R., Davidson L.A., Goldsby J.S., Hunt C.L., Steinmeyer S.H., Menon R., Suchodolski J.S., et al. The microbiota-derived metabolite indole decreases mucosal inflammation and injury in a murine model of NSAID enteropathy. Gut Microbes. 2016;7:246-261.

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    Sofia M.A., Ciorba M.A., Meckel K., Lim C.K., Guillemin G.J., Weber C.R., Bissonnette M., Pekow J.R. Tryptophan Metabolism through the Kynurenine Pathway is Associated with Endoscopic Inflammation in Ulcerative Colitis. Inflamm. Bowel Dis. 2018;24:1471-1480.

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    Ramos F.J., Kaeberlein M. Ageing: A healthy diet for stem cells. Nature. 2012;486:477-478.

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    Ala M. Tryptophan metabolites modulate inflammatory bowel disease and colorectal cancer by affecting immune system. Int. Rev. Immunol. 2022;41:326-345.

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    Hanahan D. Hallmarks of Cancer: New Dimensions. Cancer Discov. 2022;12:31-46.

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    Platten M., Nollen E.A.A., Rohrig U.F., Fallarino F., Opitz C.A. Tryptophan metabolism as a common therapeutic target in cancer, neurodegeneration and beyond. Nat. Rev. Drug Discov. 2019;18:379-401.

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    Sivaprakasam S., Bhutia Y.D., Ramachandran S., Ganapathy V. Cell-Surface and Nuclear Receptors in the Colon as Targets for Bacterial Metabolites and Its Relevance to Colon Health. Nutrients. 2017;9:856.

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    Dai G., Chen X., He Y. The Gut Microbiota Activates AhR Through the Tryptophan Metabolite Kyn to Mediate Renal Cell Carcinoma Metastasis. Front. Nutr. 2021;8:712327.

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    Park E.M., Chelvanambi M., Bhutiani N., Kroemer G., Zitvogel L., Wargo J.A. Targeting the gut and tumor microbiota in cancer. Nat. Med. 2022;28:690-703.

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    Trezeguet V., Fatrouni H., Merched A.J. Immuno-Metabolic Modulation of Liver Oncogenesis by the Tryptophan Metabolism. Cells. 2021;10:3469.

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