@article{3667a96c51f64891bdbe38f3db76fb7c,
title = "Glutathione Restricts Serine Metabolism to Preserve Regulatory T Cell Function",
abstract = "Regulatory T cells (Tregs) maintain immune homeostasis and prevent autoimmunity. Serine stimulates glutathione (GSH) synthesis and feeds into the one-carbon metabolic network (1CMet) essential for effector T cell (Teff) responses. However, serine's functions, linkage to GSH, and role in stress responses in Tregs are unknown. Here, we show, using mice with Treg-specific ablation of the catalytic subunit of glutamate cysteine ligase (Gclc), that GSH loss in Tregs alters serine import and synthesis and that the integrity of this feedback loop is critical for Treg suppressive capacity. Although Gclc ablation does not impair Treg differentiation, mutant mice exhibit severe autoimmunity and enhanced anti-tumor responses. Gclc-deficient Tregs show increased serine metabolism, mTOR activation, and proliferation but downregulated FoxP3. Limitation of cellular serine in vitro and in vivo restores FoxP3 expression and suppressive capacity of Gclc-deficient Tregs. Our work reveals an unexpected role for GSH in restricting serine availability to preserve Treg functionality. Regulatory T cells (Tregs) rely on oxidative metabolism, which triggers the generation of reactive oxygen species (ROS). Accumulating ROS are controlled by the antioxidant glutathione (GSH). Kurniawan et al. reveal an unexpected subset-specific role of GSH in serine metabolism and Treg function.",
keywords = "FoxP3, ROS, Treg, autoimmunity, cancer, diet, glutamate cysteine ligase, glutathione, one carbon metabolism, serine metabolism",
author = "Henry Kurniawan and Franchina, {Davide G.} and Luana Guerra and Lynn Bonetti and Baguet, {Leticia Soriano} and Melanie Grusdat and Lisa Schlicker and Oliver Hunewald and Catherine Dostert and Merz, {Myriam P.} and Carole Binsfeld and Duncan, {Gordon S.} and Sophie Farinelle and Yannic Nonnenmacher and Jillian Haight and {Das Gupta}, Dennis and Anouk Ewen and Rabia Taskesen and Rashi Halder and Ying Chen and Christian J{\"a}ger and Markus Ollert and Paul Wilmes and Vasilis Vasiliou and Harris, {Isaac S.} and Knobbe-Thomsen, {Christiane B.} and Turner, {Jonathan D.} and Mak, {Tak W.} and Michael Lohoff and Johannes Meiser and Karsten Hiller and Dirk Brenner",
note = "Funding Information: We thank S. Storn, A. Oudin (LIH, Luxembourg), and LIH's Animal Welfare Structure for animal services, and we are grateful to the Metabolomics Platform of Luxembourg Centre for Systems Biomedicine (LCSB). We also thank B. Camara (Univ. Marburg, Germany) for technical help; M. Brenner for general support; and Croix-Rouge Luxembourgeoise and all study blood donors. D.B. is supported by FNR-ATTRACT (A14/BM/7632103) and FNR-CORE grants (C15/BM/10355103) and (C18/BM/12691266). D.B. L.B. L.G. J.T. M.Z. and L.S.B are funded by FNR-PRIDE (PRIDE/11012546/NEXTIMMUNE) and D.B. A.E. and P.W. by (PRIDE17/11823097/MicrOH). D.B. and D.G.F. are supported by FNR-RIKEN (TregBar/11228353). V.V. holds grant NIH/NIAAA (5R24AA022057). J.T. was funded by FNR-CORE (C16/BM/11342695). M.L. and D.D.G. are funded by Deutsches Zentrum f?r Infektionsforschung and University Hospital Giessen Marburg. T.W.M. is funded by grants from the National Multiple Sclerosis Society and Canadian Institutes of Health Research. C.B.K.T. and R.T. are supported by DKH (110663, CBKT, RT) and BMBF (01ZX1401B, CBKT). J.M. is supported by FNR-ATTRACT (A18/BM/11809970) and INTER-BMBF grant (18/13399110). D.B. and H.K.: study conception and manuscript writing. H.K. D.G.F. L.G. L.B. L.S.B. M.G. L.S. C.D. M.P.M. C.B. G.S.D. S.F. Y.N. J.H. D.D.G. and A.E.: data generation and analysis. R.T. and C.B.K.: histology. R.H. and P.W.: RNA sequencing. O.H.: bioinformatics. H.K. D.G.F. L.S.B. L.S. C.J. J.M. K.H. Y.N. and D.B.: metabolic analyses. T.W.M. M.L. I.S.H. Y.C. M.O. and V.V.: expert comments and reagents. D.B.: study supervision. The authors declare no competing interests. Funding Information: We thank S. Storn, A. Oudin (LIH, Luxembourg), and LIH{\textquoteright}s Animal Welfare Structure for animal services, and we are grateful to the Metabolomics Platform of Luxembourg Centre for Systems Biomedicine (LCSB). We also thank B. Camara (Univ. Marburg, Germany) for technical help; M. Brenner for general support; and Croix-Rouge Luxembourgeoise and all study blood donors. D.B. is supported by FNR -ATTRACT ( A14/BM/7632103 ) and FNR-CORE grants ( C15/BM/10355103 ) and ( C18/BM/12691266 ). D.B., L.B., L.G., J.T., M.Z., and L.S.B are funded by FNR-PRIDE (PRIDE/ 11012546 /NEXTIMMUNE) and D.B., A.E., and P.W. by (PRIDE17/ 11823097 /MicrOH). D.B. and D.G.F. are supported by FNR-RIKEN (TregBar/ 11228353 ). V.V. holds grant NIH/ NIAAA ( 5R24AA022057 ). J.T. was funded by FNR-CORE ( C16/BM/11342695 ). M.L. and D.D.G. are funded by Deutsches Zentrum f{\"u}r Infektionsforschung and University Hospital Giessen Marburg . T.W.M. is funded by grants from the National Multiple Sclerosis Society and Canadian Institutes of Health Research . C.B.K.T. and R.T. are supported by DKH ( 110663 , CBKT, RT) and BMBF ( 01ZX1401B , CBKT). J.M. is supported by FNR-ATTRACT ( A18/BM/11809970 ) and INTER-BMBF grant ( 18/13399110 ). Publisher Copyright: {\textcopyright} 2020 Elsevier Inc.",
year = "2020",
month = may,
day = "5",
doi = "10.1016/j.cmet.2020.03.004",
language = "English",
volume = "31",
pages = "920--936.e7",
journal = "Cell Metabolism",
issn = "1550-4131",
publisher = "Cell Press",
number = "5",
}