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Cited by 174Inflammatory Bowel DiseaseT-cell and B-cell ImmunologyIL-33, ST2, and ILC Pathways

Repression of the aryl-hydrocarbon receptor prevents oxidative stress and ferroptosis of intestinal intraepithelial lymphocytes

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Panda, Santosh K., Peng, Vincent, Sudan, Raki, Ulezko Antonova, Alina, Di Luccia, Blanda, Ohara, Takahiro E., Fachi, Jose Luis, Grajales-Reyes, Gary E. +5 more·2023·Immunity
DOI 10.1016/j.immuni.2023.01.023PMC PMC10101911
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Abstract

The aryl-hydrocarbon receptor (AHR) is a ligand-activated transcription factor that buoys intestinal immune responses. AHR induces its own negative regulator, the AHR repressor (AHRR). Here, we show that AHRR is vital to sustaining intestinal intraepithelial lymphocytes (IELs). AHRR deficiency reduced IEL representation in a cell-intrinsic fashion. Single-cell RNA sequencing revealed an oxidative stress profile in Ahrr-/- IELs. AHRR deficiency unleashed AHR-induced expression of CYP1A1, a monooxygenase that generates reactive oxygen species, increasing redox imbalance, lipid peroxidation, and ferroptosis in Ahrr-/- IELs. Dietary supplementation with selenium or vitamin E to restore redox homeostasis rescued Ahrr-/- IELs. Loss of IELs in Ahrr-/- mice caused susceptibility to Clostridium difficile infection and dextran sodium-sulfate-induced colitis. Inflamed tissue of inflammatory bowel disease patients showed reduced Ahrr expression that may contribute to disease. We conclude that AHR signaling must be tightly regulated to prevent oxidative stress and ferroptosis of IELs and to preserve intestinal immune responses.

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Authors
Panda, S. K., Peng, V., Sudan, R., Ulezko Antonova, A., Di Luccia, B., Ohara, T. E., Fachi, J. L., Grajales-Reyes, G. E., Jaeger, N., Trsan, T., Gilfillan, S., Cella, M., & Colonna, M.
Affiliations
Washington University in St. Louis (US)
Corresponding author
Colonna, Marco
ORCID
Venue
Immunity
Publisher
Elsevier BV
Published
2023-04
Volume
56
Issue
4
Pages
797-812.e4
ISSN
1074-7613 (ISSN-L)
DOI
10.1016/j.immuni.2023.01.023
PMC
PMC10101911
OpenAlex
W4321116781
Cited by
174
References
8
Citations by year
2026: 45 · 2025: 59 · 2024: 52 · 2023: 18
FWCI
28.89
Type
journal article
Language
en
Open access
Licence
Locations
  • Immunity (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • Pfizer
  • Kenneth Rainin Foundation (20220038)
  • National Institutes of Health (R01 AI134035, R01 AI134236, R01 DK124699)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
  • Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
  • Life Sciences › Immunology and Microbiology › Immunology › IL-33, ST2, and ILC Pathways
Keywords
aryl hydrocarbon receptor, AHRR, intestinal intraepithelial lymphocytes, ferroptosis, oxidative stress, CYP1A1, lipid peroxidation, redox homeostasis, selenium, vitamin E, Clostridium difficile infection, DSS-induced colitis, inflammatory bowel disease, intestinal immunity
MeSH terms
Intraepithelial Lymphocytes, Ferroptosis, Animals, Hydrocarbons, Repressor Proteins, Receptors, Aryl Hydrocarbon, Oxidative Stress, Mice, Basic Helix-Loop-Helix Transcription Factors, Basic Helix-Loop-Helix Proteins

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