Cited by 145T-cell and B-cell ImmunologyPsoriasis: Treatment and PathogenesisImmunodeficiency and Autoimmune Disorders

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Functional reprogramming of regulatory T cells in the absence of Foxp3

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Charbonnier, Louis-Marie, Cui, Ye, Stephen-Victor, Emmanuel, Harb, Hani, Lopez, David, Bleesing, Jack J., Garcia-Lloret, Maria I., Chen, Karin, Ozen, Ahmet, Carmeliet, Peter, Li, Ming O., Pellegrini, Matteo, Chatila, Talal A.·2019·Nature Immunology

DOI 10.1038/s41590-019-0442-xPMC PMC6707855

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Abstract

Regulatory T cells (T reg cells) deficient in the transcription factor Foxp3 lack suppressor function and manifest an effector T (T eff) cell-like phenotype. We demonstrate that Foxp3 deficiency dysregulates metabolic checkpoint kinase mammalian target of rapamycin (mTOR) complex 2 (mTORC2) signaling and gives rise to augmented aerobic glycolysis and oxidative phosphorylation. Specific deletion of the mTORC2 adaptor gene Rictor in Foxp3-deficient T reg cells ameliorated disease in a Foxo1 transcription factor-dependent manner. Rictor deficiency re-established a subset of T reg cell genetic circuits and suppressed the T eff cell-like glycolytic and respiratory programs, which contributed to immune dysregulation. Treatment of T reg cells from patients with FOXP3 deficiency with mTOR inhibitors similarly antagonized their T eff cell-like program and restored suppressive function. Thus, regulatory function can be re-established in Foxp3-deficient T reg cells by targeting their metabolic pathways, providing opportunities to restore tolerance in T reg cell disorders.

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Authors: Charbonnier, L.-M., Cui, Y., Stephen-Victor, E., Harb, H., Lopez, D., Bleesing, J. J., Garcia-Lloret, M. I., Chen, K., Ozen, A., Carmeliet, P., Li, M. O., Pellegrini, M., & Chatila, T. A.
Affiliations: Boston Children's Hospital (US)
University of California, Los Angeles (US)
Cincinnati Children's Hospital Medical Center (US)
University of Utah (US)
Marmara University (TR)
VIB-KU Leuven Center for Cancer Biology (BE)
Memorial Sloan Kettering Cancer Center (US)
Corresponding author: Chatila, Talal A.
ORCID: Charbonnier, Louis-Marie
Cui, Ye
Harb, Hani
Bleesing, Jack J.
Garcia-Lloret, Maria I.
Chen, Karin
Ozen, Ahmet
Carmeliet, Peter
Li, Ming O.
Pellegrini, Matteo
Chatila, Talal A.
Venue: Nature Immunology
Publisher: Springer Science and Business Media LLC
Published: 2019-08-05
Volume: 20
Issue: 9
Pages: 1208-1219
ISSN: 1529-2908 (ISSN-L)
1529-2916
DOI: 10.1038/s41590-019-0442-x
PMC: PMC6707855
OpenAlex: W2966678440
Cited by: 145
References: 55
Citations by year: 2026: 14 · 2025: 12 · 2024: 14 · 2023: 16 · 2022: 26 · 2021: 24 · 2020: 32 · 2019: 7
FWCI: 8.89
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Immunology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Dspace Repository (Marmara Üniversitesi) (submittedVersion, other-oa)
Lirias (KU Leuven) (submittedVersion)
Dspace Repository (Marmara Üniversitesi) (submittedVersion)
Funders: National Institutes of Health (5r01ai085090-10)
National Cancer Institute (P30CA008748, P30CA016042)
National Institute of Allergy and Infectious Diseases (R01-AI-085090, R01AI102888, R01AI065617)
National Institute of Diabetes and Digestive and Kidney Diseases (P30DK034854)
Topics: Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
Life Sciences › Immunology and Microbiology › Immunology › Immunodeficiency and Autoimmune Disorders
Keywords: regulatory T cells, mTORC2 signaling, Rictor, aerobic glycolysis, oxidative phosphorylation, FOXO1, mTOR inhibitors, immune tolerance, immune dysregulation
MeSH terms: Mechanistic Target of Rapamycin Complex 2, Rapamycin-Insensitive Companion of mTOR Protein, Animals, Cells, Cultured, Female, Gene Expression Regulation, Glycolysis, Humans, Male, Mice, Inbred C57BL, Oxidative Phosphorylation, Signal Transduction, Mice, Knockout, T-Lymphocytes, Regulatory, Mice, Forkhead Transcription Factors, Cellular Reprogramming

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Functional reprogramming of regulatory T cells in the absence of Foxp3

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