Human retinoic acid–regulated CD161+ regulatory T cells support wound repair in intestinal mucosa
Open accessAbstract
Repair of tissue damaged during inflammatory processes is key to the return of local homeostasis and restoration of epithelial integrity. Here we describe CD161+ regulatory T (T reg) cells as a distinct, highly suppressive population of T reg cells that mediate wound healing. These T reg cells were enriched in intestinal lamina propria, particularly in Crohn's disease. CD161+ T reg cells had an all-trans retinoic acid (ATRA)-regulated gene signature, and CD161 expression on T reg cells was induced by ATRA, which directly regulated the CD161 gene. CD161 was co-stimulatory, and ligation with the T cell antigen receptor induced cytokines that accelerated the wound healing of intestinal epithelial cells. We identified a transcription-factor network, including BACH2, RORγt, FOSL2, AP-1 and RUNX1, that controlled expression of the wound-healing program, and found a CD161+ T reg cell signature in Crohn's disease mucosa associated with reduced inflammation. These findings identify CD161+ T reg cells as a population involved in controlling the balance between inflammation and epithelial barrier healing in the gut.
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ATRA regulates the activity of CD161+-Treg cells that support wound repair in intestinal mucosa.
“ATRA regulates the activity of CD161+-Treg cells that support wound repair in intestinal mucosa14.”
From Advances and challenges in retinoid delivery systems in regenerative and therapeutic medicine (2020) · cites this paper as [14]
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Ramanan, D., Pratama, A., Zhu, Y., Venezia, O., Sassone-Corsi, M., Chowdhary, K., Galván-Peña, S., Sefik, E., Brown, C., Gélineau, A., et al. (2023) · Nature Reviews Immunology · doi:10.1038/s41577-023-00890-w · Cited by 126 · see citing works
Treg cell therapy: How cell heterogeneity can make the difference
Giganti, G., Atif, M., Mohseni, Y., Mastronicola, D., Grageda, N., Povoleri, G. A., Miyara, M., & Scottà, C. (2021) · European Journal of Immunology · doi:10.1002/eji.201948131 · Cited by 82 · see citing works
Self-citationInnate Control of Tissue-Reparative Human Regulatory T Cells
Lam, A. J., MacDonald, K. N., Pesenacker, A. M., Juvet, S. C., Morishita, K. A., Bressler, B., iGenoMed Consortium, Pan, J. G., Sidhu, S. S., Rioux, J. D., et al. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1801330 · Cited by 47 · see citing works
- Authors
- Povoleri, G. A. M., Nova-Lamperti, E., Scottà, C., Fanelli, G., Chen, Y.-C., Becker, P. D., Boardman, D., Costantini, B., Romano, M., Pavlidis, P., McGregor, R., Pantazi, E., Chauss, D., Sun, H.-W., Shih, H.-Y., Cousins, D. J., Cooper, N., Powell, N., Kemper, C., Pirooznia, M., Laurence, A., Kordasti, S., Kazemian, M., Lombardi, G., & Afzali, B.
- Affiliations
- King's College London (GB)
- National Institutes of Health (US)
- University of Leicester (GB)
- Imperial College London (GB)
- Newcastle University (GB)
- Purdue University West Lafayette (US)
- Corresponding author
- Afzali, Behdad
- ORCID
- Povoleri, Giovanni A. M.
- Scottà, Cristiano
- Fanelli, Giorgia
- Chen, Yun-Ching
- Becker, Pablo D.
- Boardman, Dominic
- Romano, Marco
- Pavlidis, Polychronis
- McGregor, Reuben
- Pantazi, Eirini
- Chauss, Daniel
- Sun, Hong-Wei
- Shih, Han-Yu
- Cousins, David J.
- Cooper, Nichola
- Powell, Nick
- Kemper, Claudia
- Pirooznia, Mehdi
- Laurence, Arian
- Kordasti, Shahram
- Kazemian, Majid
- Lombardi, Giovanna
- Afzali, Behdad
- Venue
- Nature Immunology
- Published
- 2018-11-05
- Volume
- 19
- Issue
- 12
- Pages
- 1403-1414
- ISSN
- 1529-2908 (ISSN-L)
- 1529-2916
- PMC
- PMC6474659
- OpenAlex
- W2898609550
- Cited by
- 114
- References
- 75
- Citations by year
- 2026: 7 · 2025: 13 · 2024: 9 · 2023: 14 · 2022: 15 · 2021: 19 · 2020: 25 · 2019: 12
- FWCI
- 6.12
- 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)
- Figshare (submittedVersion, cc-by)
- Università Politecnica delle Marche (Università Politecnica delle Marche) (submittedVersion)
- Research Portal (King's College London) (submittedVersion, other-oa)
- Spiral (Imperial College London) (submittedVersion)
- Newcastle University ePrints (Newcastle Univesity)
- Funders
- Crohn's and Colitis Foundation of America
- Purdue University
- Ohio State University
- Wellcome Trust (097261/Z/11/Z, WT101159, 101159/Z/13/Z)
- National Institute for Health and Care Research
- British Heart Foundation (RG/13/12/30395, RG/08/005/25303)
- King's College London
- Crohn's and Colitis UK (M15-1)
- National Institutes of Health (Z99 DK999999, Z99 AR999999, Z99 HL999999)
- National Heart, Lung, and Blood Institute (K22HL125593)
- National Institute of Diabetes and Digestive and Kidney Diseases
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
- Keywords
- retinoic acid, all-trans retinoic acid, intestinal wound healing, intestinal mucosa, Crohn's disease, intestinal lamina propria, epithelial barrier repair, BACH2, RORγt, FOSL2, AP-1, RUNX1, transcriptional regulatory networks, peripheral tolerance, tissue regeneration
- MeSH terms
- Crohn Disease, Humans, Intestinal Mucosa, Tretinoin, Wound Healing, T-Lymphocyte Subsets, T-Lymphocytes, Regulatory, NK Cell Lectin-Like Receptor Subfamily B
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