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Aryl hydrocarbon receptor ligand production by the gut microbiota is decreased in celiac disease leading to intestinal inflammation
Open accessAbstract
, or pharmacological stimulation using 6-formylindolo (3,2-b) carbazole (Ficz) decreased immunopathology in NOD/DQ8 mice exposed to gluten. We then determined AhR ligand production by the fecal microbiota and AhR activation in patients with active celiac disease compared to nonceliac control individuals. Patients with active celiac disease demonstrated reduced AhR ligand production and lower intestinal AhR pathway activation. These results highlight gut microbiota-dependent modulation of the AhR pathway in celiac disease and suggest a new therapeutic strategy for treating this disorder.
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“the importance of the GM’s ability to metabolize tryptophan into aryl hydrocarbon receptor ligands and, therefore, modulate gut inflammation, was demonstrated in patients with celiac disease (202).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [202]
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“On the opposite, patients with celiac diseases had lower tryptophan and AhR agonists in stool while kynurenine metabolites were increased compare to healthy participants [224].”
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Vacca, M., Porrelli, A., Calabrese, F. M., Lippolis, T., Iacobellis, I., Celano, G., Pinto, D., Russo, F., Giannelli, G., & Angelis, M. D. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.859467 · Cited by 33
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“Indole derivatives are in fact involved in the homeostasis of the immune system and in the inhibition of the activation of the actin regulatory protein MyoIIA that modulates the functional integrity of tight junctions and the permeability of the intestinal barrier [45,46].”
BackgroundGonzález, A., Guerra‐Ojeda, S., Villa, M. A. C., Valls, A., Alegre, E., Quintero-Bernal, R., Martorell, P., Chenoll, E., Serna‐García, M., Mauricio, M. D., et al. (2024) · Foods · doi:10.3390/foods13213479 · Cited by 26
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BackgroundInfluentialTryptophan Metabolism and COVID-19-Induced Skeletal Muscle Damage: Is ACE2 a Key Regulator?
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“Defective activation of AHR is associated with active coeliac disease and AHR activation through modification of the microbiota in response to increased dietary tryptophan or direct administration of AHR ligands reduced the risk of coeliac disease in a mouse model 131 .”
Hu, S., Luo, L., & Zeng, L. (2022) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2022.2040945 · Cited by 21
Vicentini, F., Mathews, A. J., Pittman, Q. J., Swain, M. G., Sharkey, K. A., & Hirota, S. A. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.08.228 · Cited by 22
Intestinal permeability, food antigens and the microbiome: a multifaceted perspective
Valitutti, F., Mennini, M., Monacelli, G., Fagiolari, G., Piccirillo, M., Nardo, G. D., & Cara, G. D. (2025) · Frontiers in Allergy · doi:10.3389/falgy.2024.1505834 · Cited by 23
Shi, T., Feng, Y., Liu, W., Liu, H., Li, T., Wang, M., Li, Z., Lu, J., Abudurexiti, A., Maimaitireyimu, A., et al. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.1020977 · Cited by 21
Turning Microbial AhR Agonists into Therapeutic Agents via Drug Delivery Systems
Puccetti, M., Pariano, M., Wojtylo, P., Schoubben, A., Giovagnoli, S., & Ricci, M. (2023) · Pharmaceutics · doi:10.3390/pharmaceutics15020506 · Cited by 19
“For instance, 3IAld production was reduced in patients with atopic dermatitis [42,44], inflammatory bowel disease [45], and celiac disease [46] and in hematologic patients with fungal pneumonia [47].”
BackgroundRegulation of host immune responses by Lactobacillus through aryl hydrocarbon receptors
Huang, Z., Xie, L., & Huang, Z. (2023) · Medicine in Microecology · doi:10.1016/j.medmic.2023.100081 · Cited by 19
Intestinal tryptophan metabolism in disease prevention and swine production
Hu, Z., Feng, L., Jiang, Q., Wang, W., Tan, B., Tang, X., & Yin, Y. (2023) · Animal nutrition · doi:10.1016/j.aninu.2023.08.002 · Cited by 20
Churchward, M. A., Michaud, E. R., Mullish, B. H., Blanco, J. M., Perez, I. G., Marchesi, J. R., Xu, H., Kao, D. H., & Todd, K. G. (2023) · Heliyon · doi:10.1016/j.heliyon.2023.e16908 · Cited by 20
Nikoloudaki, O., Celano, G., Polo, A., Cappello, C., Granehäll, L., Costantini, A., Vacca, M., Speckmann, B., Cagno, R. D., Francavilla, R., et al. (2024) · Microbiology Spectrum · doi:10.1128/spectrum.03524-23 · Cited by 18
“All these responses are beneficial to gluten-related disorders (70).”
BackgroundMicrobiota, IgA and Multiple Sclerosis
Boussamet, L., Rajoka, M. S. R., & Berthelot, L. (2022) · Microorganisms · doi:10.3390/microorganisms10030617 · Cited by 20
“Finally, other compounds arising from bacterial activity, such as aryl hydrocarbon receptor (AhR) ligands or specific sphingolipids, are known to have regulatory effects on the immune system [32,33].”
BackgroundNieves, K., Flannigan, K. L., Hughes, E., Stephens, M., Thorne, A. J., Delanne-Cuménal, A., Strayer, K., Kola-Ilesanmi, D., Wickramasinghe, S., Mirzadzare, N., et al. (2025) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00256.2024 · Cited by 18
Molecular Genetics and Probiotic Mechanisms of Saccharomyces cerevisiae var. boulardii
Ting, T., Lee, W.-J., & Goh, H. (2025) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-025-10634-y · Cited by 16
Faber, S., Lahoti, T., Taylor, E., Lewis, L., Sapiro, J., Toledo Sales, V., Dragan, Y., & Jeffy, B. (2022) · Cells · doi:10.3390/cells11101708 · Cited by 16
“As a selective human AhR antagonist, UroA has been shown to attenuate inflammation and maintain tight junction formation within Caco-2 cells following inhibition of IL-6 and PTGS2 transcription in an AhR-specific manner [45,49].”
BackgroundRayan, M., Sayed, T. S., Hussein, O., Therachiyil, L., Maayah, Z. H., Maccalli, C., Shahab Uddin, M. S., Prehn, J. H. M., & Korashy, H. M. (2024) · Cellular & Molecular Biology Letters · doi:10.1186/s11658-024-00538-0 · Cited by 20
“Patients with celiac disease have reduced levels of endogenous AhR ligands and consequently less intestinal AhR activity [146], and AhR knockout mice were found to be more susceptible to dextran sulfate sodium -induced colitis.”
BackgroundCen, Q., Cui, Y., Feng, J., Li, Z., Wei, J., Wang, L., Chang, C., Pang, R., Wang, J., & Zhang, A. (2025) · Probiotics and Antimicrobial Proteins · doi:10.1007/s12602-025-10545-y · Cited by 17
Ongoing Clinical Trials in Aging-Related Tissue Fibrosis and New Findings Related to AhR Pathways
Yu, H., Feng, Z., Lin, W., Yang, K., Liu, R., Li, J., Liu, X., Pei, M., & Yang, H. (2022) · Aging and Disease · doi:10.14336/ad.2021.1105 · Cited by 16
“Aging and Disease • Volume 13, Number 3, June 2022 735 hydrocarbons and hazardous environmental toxins, endogenous AhR ligands from tryptophan metabolism, including FICZ [42], kynurenine [43], kynurenic acid [44], xanthurenic acid [45], cinnabarinic acid [46], serotonin [47], 5-hydroxyindole-3-acetic acid [33], trypta…”
BackgroundRelevance of gut microbiome research in food safety assessment
Garrido‐Romero, M., Pazos, F., Sánchez‐Martínez, E., Benito, C., Ruiz, J. Á. G., Borrego‐Yaniz, G., Bowes, C., Broll, H., Caminero, A., Caro, E., et al. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2410476 · Cited by 16
“72,73 Overall, chemical contaminants in food are known to persist in the environment (air, soil, and water) 74 and their bioaccumulation in the agri-food chain could represent a health risk leading to alterations in the human gut microbiome composition and function.”
BackgroundMetabolomics and metagenomics in mice reveal the role of the gut microbiota in tryptophan metabolism
Levé, M., Manghi, P., Bredon, M., Lefèvre, A., Manara, S., Armanini, F., Emond, P., Planchais, J., Rolhion, N., Segata, N., et al. (2025) · iScience · doi:10.1016/j.isci.2025.113751 · Cited by 16
Akkerman, R., Logtenberg, M. J., Beukema, M., de Haan, B. J., Faas, M. M., Zoetendal, E. G., Schols, H. A., & de Vos, P. (2022) · Food & Function · doi:10.1039/d2fo00550f · Cited by 14
Pani, G. (2023) · Cancers · doi:10.3390/cancers15092583 · Cited by 16
Keppeler, K., Pesi, A., Lange, S., Helmstädter, J., Strohm, L., Ubbens, H., Kuntić, M., Kuntić, I., Mihaliková, D., Vujačić-Mirski, K., et al. (2024) · Redox Biology · doi:10.1016/j.redox.2024.103071 · Cited by 13
“We used a novel human transgenic mouse model of CeD that replicates the central mechanistic and immunological features of the disease ) [25,26].”
Method
Metadata
- Authors
- Lamas, B., Hernandez-Galan, L., Galipeau, H. J., Constante, M., Clarizio, A., Jury, J., Breyner, N. M., Caminero, A., Rueda, G., Hayes, C. L., McCarville, J. L., Bermudez Brito, M., Planchais, J., Rolhion, N., Murray, J. A., Langella, P., Loonen, L. M. P., Wells, J. M., Bercik, P., Sokol, H., & Verdu, E. F.
- Affiliations
- McMaster University (CA)
- Farncombe Family Digestive Health Research Institute, Department of Medicine, McMaster University, Hamilton, Ontario, Canada.
- AgroParisTech (FR)
- Inserm (FR)
- Mayo Clinic (US)
- Wageningen University & Research (NL)
- Corresponding author
- Lamas, Bruno
- Sokol, Harry
- Verdu, Elena F.
- ORCID
- Lamas, Bruno
- Galipeau, Heather J.
- Constante, Marco
- Clarizio, Alexandra
- Jury, Jennifer
- Breyner, Natalia M.
- Caminero, Alberto
- Rueda, Gaston
- Hayes, Christina L.
- McCarville, Justin L.
- Planchais, Julien
- Rolhion, Nathalie
- Murray, Joseph A.
- Langella, Philippe
- Loonen, Linda M. P.
- Wells, Jerry M.
- Bercik, Premysl
- Sokol, Harry
- Verdu, Elena F.
- Venue
- Science Translational Medicine
- Published
- 2020-10-21
- Volume
- 12
- Issue
- 566
- Pages
- eaba0624
- ISSN
- 1946-6234 (ISSN-L)
- 1946-6242
- OpenAlex
- W3094545640
- Cited by
- 179
- References
- 59
- Citations by year
- 2026: 20 · 2025: 26 · 2024: 33 · 2023: 27 · 2022: 43 · 2021: 27 · 2020: 3
- FWCI
- 21.72
- Type
- journal article
- Language
- en
- Open access
- green
- research.wur.nl
- Locations
- Science Translational Medicine (publishedVersion)
- PubMed (publishedVersion)
- Socio-Environmental Systems Modeling (acceptedVersion)
- HAL (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Joint Programming Initiative A healthy diet for a healthy life (ANR-15-HDIM-0001-1, JPI-HDHL 50-52905-98-601)
- Canadian Institutes of Health Research (CIHR-143922, 168840)
- Topics
- Health Sciences › Medicine › Gastroenterology › Celiac Disease Research and Management
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Inflammatory Bowel Disease
- Keywords
- aryl hydrocarbon receptor, celiac disease, gut microbiota, intestinal inflammation, gluten, FICZ, fecal microbiota, immunopathology
- MeSH terms
- Gastrointestinal Microbiome, Animals, Celiac Disease, Humans, Inflammation, Ligands, RNA, Ribosomal, 16S, Receptors, Aryl Hydrocarbon, Mice
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