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AHR drives the development of gut ILC22 cells and postnatal lymphoid tissues via pathways dependent on and independent of Notch
Open accessAbstract
Innate lymphoid cells (ILCs) of the ILC22 type protect the intestinal mucosa from infection by secreting interleukin 22 (IL-22). ILC22 cells include NKp46(+) and lymphoid tissue-inducer (LTi)-like subsets that express the aryl hydrocarbon receptor (AHR). Here we found that Ahr(-/-) mice had a considerable deficit in ILC22 cells that resulted in less secretion of IL-22 and inadequate protection against intestinal bacterial infection. Ahr(-/-) mice also lacked postnatally 'imprinted' cryptopatches and isolated lymphoid follicles (ILFs), but not embryonically 'imprinted' Peyer's patches. AHR induced the transcription factor Notch, which was required for NKp46(+) ILCs, whereas LTi-like ILCs, cryptopatches and ILFs were partially dependent on Notch signaling. Thus, AHR was essential for ILC22 cells and postnatal intestinal lymphoid tissues. Moreover, ILC22 subsets were heterogeneous in their requirement for Notch and their effect on the generation of intestinal lymphoid tissues.
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“This idea has been supported and expanded upon recently as additional evidence emerges detailing missing or impaired populations of resident immune cells in adult null mice at barrier tissues like the lung, intestine, and skin (Esser & Rannug, 2015; Kiss et al., 2011; Lee et al., 2012; Li et al., 2018; Qiu et al., 2012; Stockinger et al., 2014).”
From Rodent Genetic Models of Ah Receptor Signaling (2021) · cites this paper as Lee et al., 2012
In the citing paper
“Ahr−/− mice suffer from multiple immunological deficits, including reduced resistance to infection with the bacteria Listeria monocytogenes or Citrobacter rodentium, as well as the fungus Candida albicans; exacerbated DSS-induced colitis; and even altered susceptibility to experimental autoimmune encephalomyelitis (EAE)”
From Understanding the Holobiont: How Microbial Metabolites Affect Human Health and Shape the Immune System (2017) · cites this paper as Lee et al., 2011
In the citing paper
“the AhR is in fact required for postnatal maintenance of IL-22-producing ILC3s, as well as the formation of isolated lymphoid follicles (Kiss et al., 2011; Lee et al., 2011; Y. Li et al., 2011; J. Qiu et al., 2012).”
From Understanding the Holobiont: How Microbial Metabolites Affect Human Health and Shape the Immune System (2017) · cites this paper as Lee et al., 2011
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An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor
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Self-citationThe aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins
Veldhoen, M., Hirota, K., Westendorf, A. M., Buer, J., Dumoutier, L., Renauld, J.-C., & Stockinger, B. (2008) · Nature · doi:10.1038/nature06881 · Cited by 1,634
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A human natural killer cell subset provides an innate source of IL-22 for mucosal immunity
Cella, M., Fuchs, A. G., Vermi, W., Facchetti, F., Otero, K., Lennerz, J. K., Doherty, J. M., Mills, J. C., & Colonna, M. (2008) · Nature · doi:10.1038/nature07537 · Cited by 1,298
Self-citationSatoh‐Takayama, N., Vosshenrich, C. A. J., Lesjean‐Pottier, S., Sawa, S., Lochner, M., Rattis, F. M., Mention, J., Thiam, K., Cerf–Bensussan, N., Mandelboim, O., et al. (2008) · Immunity · doi:10.1016/j.immuni.2008.11.001 · Cited by 1,133
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Metadata
- Authors
- 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., & Colonna, M.
- Affiliations
- Washington University in St. Louis (US)
- University of Wisconsin–Madison (US)
- University of Milan (IT)
- Corresponding author
- Colonna, Marco
- ORCID
- Venue
- Nature Immunology
- Published
- 2011-11-20
- Volume
- 13
- Issue
- 2
- Pages
- 144-151
- ISSN
- 1529-2908 (ISSN-L)
- 1529-2916
- PMC
- PMC3468413
- OpenAlex
- W2068162195
- Cited by
- 777
- References
- 50
- Citations by year
- 2026: 27 · 2025: 36 · 2024: 57 · 2023: 40 · 2022: 51 · 2021: 61 · 2020: 54 · 2019: 61 · 2018: 59 · 2017: 60 · 2016: 59 · 2015: 58 · 2014: 58 · 2013: 61 · 2012: 34
- FWCI
- 21.70
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Immunology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- U.S. Public Health Service (A1067854)
- National Institute of General Medical Sciences (R01GM055479)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK064798, P30DK020579, P30DK052574)
- National Institute of Environmental Health Sciences (K08ES017283, R01ES005703)
- National Institute of Dental and Craniofacial Research (R01DE021255)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › IL-33, ST2, and ILC Pathways
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Health Sciences › Medicine › Gastroenterology › Inflammatory Bowel Disease
- Keywords
- aryl hydrocarbon receptor, innate lymphoid cells, IL-22, Notch signaling, isolated lymphoid follicles, Peyer's patches, intestinal mucosal immunity, bacterial intestinal infections
- MeSH terms
- Interleukin-22, Animals, Antigens, Ly, Female, Interleukins, Lymphoid Tissue, Male, Mice, Inbred C57BL, Mice, Transgenic, Signal Transduction, Receptors, Aryl Hydrocarbon, Gastrointestinal Tract, Mice, Receptor, Notch1, Receptor, Notch2, Natural Cytotoxicity Triggering Receptor 1
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