Redox regulation of regulatory T-cell differentiation and functions

References

• Matzinger P. Tolerance, danger, and the extended family. Annu Rev Immunol. 1994;12(1):991–1045.
   PubMedGoogle Scholar
• Eberl G, Pradeu T. Towards a general theory of immunity? Trends Immunol. 2018;39(4):261–263.
   PubMed Web of Science ®Google Scholar
• Gostner JM, Becker K, Fuchs D, et al. Redox regulation of the immune response. Redox Rep. 2013;18(3):88–94.
   PubMed Web of Science ®Google Scholar
• Panduro M, Benoist C, Mathis D. Tissue Tregs. Annu Rev Immunol. 2016;34(1):609–633.
   PubMed Web of Science ®Google Scholar
• Vasanthakumar A, Moro K, Xin A, et al. The transcriptional regulators IRF4, BATF and IL-33 orchestrate development and maintenance of adipose tissue-resident regulatory T cells. Nat Immunol. 2015;16(3):276–285.
   PubMed Web of Science ®Google Scholar
• Schiering C, Krausgruber T, Chomka A, et al. The alarmin IL-33 promotes regulatory T-cell function in the intestine. Nature. 2014;513(7519):564–568.
   PubMed Web of Science ®Google Scholar
• Pierini A, Nishikii H, Baker J, et al. Foxp3. Nat Commun. 2017;8(1):15068.
   PubMedGoogle Scholar
• Hirata Y, Furuhashi K, Ishii H, et al. CD150 high bone marrow Tregs maintain hematopoietic stem cell quiescence and immune privilege via adenosine. Cell Stem Cell. 2018;22(3):445–453.e5.
   PubMed Web of Science ®Google Scholar
• Josefowicz SZ, Lu LF, Rudensky AY. Regulatory T cells: mechanisms of differentiation and function. Annu Rev Immunol. 2012;30(1):531–564.
   PubMed Web of Science ®Google Scholar
• Chen X, Song M, Zhang B, et al. Reactive oxygen species regulate T Cell immune response in the tumor microenvironment. Oxid Med Cell Longev. 2016;2016:1580967.
   Google Scholar
• Weinberg F, Ramnath N, Nagrath D. Reactive Oxygen Species in the Tumor Microenvironment: An Overview. Cancers(Basel). 2019;11(8):E1191.
   Google Scholar
• Mak TW, Grusdat M, Duncan GS, et al. Glutathione primes T cell metabolism for inflammation. Immunity. 2017;46(4):675–689.
   PubMed Web of Science ®Google Scholar
• Sena LA, Li S, Jairaman A, et al. Mitochondria are required for antigen-specific T cell activation through reactive oxygen species signaling. Immunity. 2013;38(2):225–236.
   PubMed Web of Science ®Google Scholar
• Checker R, Sharma D, Sandur SK, et al. Plumbagin inhibits proliferative and inflammatory responses of T cells independent of ROS generation but by modulating intracellular thiols. J Cell Biochem. 2010;110(5):1082–1093.
   PubMed Web of Science ®Google Scholar
• Banerjee R. Redox outside the box: linking extracellular redox remodeling with intracellular redox metabolism. J Biol Chem. 2012;287(7):4397–4402.
   PubMed Web of Science ®Google Scholar
• Brand KA, Hermfisse U. Aerobic glycolysis by proliferating cells: a protective strategy against reactive oxygen species. FASEB J. 1997;11(5):388–395.
   PubMed Web of Science ®Google Scholar
• Wang R, Dillon CP, Shi LZ, et al. The transcription factor Myc controls metabolic reprogramming upon T lymphocyte activation. Immunity. 2011;35(6):871–882.
   PubMed Web of Science ®Google Scholar
• Buck MD, O’Sullivan D, Pearce EL. T cell metabolism drives immunity. J Exp Med. 2015;212(9):1345–1360.
   PubMed Web of Science ®Google Scholar
• Guy CS, Vignali KM, Temirov J, Bettini ML, et al. Distinct TCR signaling pathways drive proliferation and cytokine production in T cells. Nat Immunol. 2013;14(3):262–270.
   PubMed Web of Science ®Google Scholar
• Waickman AT, Powell JD. Mammalian target of rapamycin integrates diverse inputs to guide the outcome of antigen recognition in T cells. J Immunol. 2012;188(10):4721–4729.
   PubMed Web of Science ®Google Scholar
• Quintana A, Schwindling C, Wenning AS, Becherer U, et al. T cell activation requires mitochondrial translocation to the immunological synapse. Proc Natl Acad Sci USA. 2007;104(36):14418–14423.
   PubMed Web of Science ®Google Scholar
• Jackson SH, Devadas S, Kwon J, et al. T cells express a phagocyte-type NADPH oxidase that is activated after T cell receptor stimulation. Nat Immunol. 2004;5(8):818–827.
   PubMed Web of Science ®Google Scholar
• Kwon J, Shatynski KE, Chen H, et al. The nonphagocytic NADPH oxidase Duox1 mediates a positive feedback loop during T cell receptor signaling. Sci Signal. 2010;3(133):ra59–ra59.
   PubMed Web of Science ®Google Scholar
• Wherry EJ. T cell exhaustion. Nat Immunol. 2011;12(6):492–499.
   PubMed Web of Science ®Google Scholar
• Sukumar M, Liu J, Mehta GU, et al. Mitochondrial membrane potential identifies cells with enhanced stemness for cellular therapy. Cell Metab. 2016;23(1):63–76.
   PubMed Web of Science ®Google Scholar
• Gambhir L, Checker R, Thoh M, et al. 1,4-Naphthoquinone, a pro-oxidant, suppresses immune responses via KEAP-1 glutathionylation. Biochem Pharmacol. 2014;88(1):95–105.
   PubMed Web of Science ®Google Scholar
• Düvel K, Yecies JL, Menon S, et al. Activation of a metabolic gene regulatory network downstream of mTOR complex 1. Mol Cell. 2010;39(2):171–183.
   PubMed Web of Science ®Google Scholar
• De Rosa V, Galgani M, Porcellini A, et al. Glycolysis controls the induction of human regulatory T cells by modulating the expression of FOXP3 exon 2 splicing variants. Nat Immunol. 2015;16(11):1174–1184.
   PubMed Web of Science ®Google Scholar
• Baron U, Floess S, Wieczorek G, et al. DNA demethylation in the human FOXP3 locus discriminates regulatory T cells from activated FOXP3(+) conventional T cells. Eur J Immunol. 2007;37(9):2378–2389.
   PubMed Web of Science ®Google Scholar
• Toker A, Engelbert D, Garg G, et al. Active demethylation of the Foxp3 locus leads to the generation of stable regulatory T cells within the thymus. J Immunol. 2013;190(7):3180–3188.
   PubMed Web of Science ®Google Scholar
• Feng Y, Arvey A, Chinen T, et al. Control of the inheritance of regulatory T cell identity by a cis element in the Foxp3 locus. Cell. 2014;158(4):749–763.
   PubMed Web of Science ®Google Scholar
• Zheng Y, Josefowicz S, Chaudhry A, et al. Role of conserved non-coding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature. 2010;463(7282):808–812.
   PubMed Web of Science ®Google Scholar
• Salminen A, Kauppinen A, Kaarniranta K. 2-Oxoglutarate-dependent dioxygenases are sensors of energy metabolism, oxygen availability, and iron homeostasis: potential role in the regulation of aging process. Cell Mol Life Sci. 2015;72(20):3897–3914.
   PubMed Web of Science ®Google Scholar
• Yue X, Trifari S, Äijö T, et al. Control of Foxp3 stability through modulation of TET activity. J Exp Med. 2016;213(3):377–397.
   PubMed Web of Science ®Google Scholar
• Nair VS, Song MH, Ko M, et al. DNA demethylation of the Foxp3 enhancer is maintained through modulation of ten-eleven-translocation and DNA methyltransferases. Mol Cells. 2016;39(12):888–897.
   PubMed Web of Science ®Google Scholar
• Almeida L, Lochner M, Berod L, et al. Metabolic pathways in T cell activation and lineage differentiation. Semin Immunol. 2016;28(5):514–524.
   PubMed Web of Science ®Google Scholar
• Yan Z, Banerjee R. Redox remodeling as an immunoregulatory strategy. Biochemistry. 2010;49(6):1059–1066.
   PubMed Web of Science ®Google Scholar
• Yan Z, Garg SK, Kipnis J, et al. Extracellular redox modulation by regulatory T cells. Nat Chem Biol. 2009;5(10):721–723.
   PubMed Web of Science ®Google Scholar
• Wang YA, Li XL, Mo YZ, et al. Effects of tumor metabolic microenvironment on regulatory T cells. Mol Cancer. 2018;17(1):168.
   PubMed Web of Science ®Google Scholar
• Angelin A, Gil-de-Gómez L, Dahiya S, et al. Foxp3 reprograms t cell metabolism to function in low-glucose, high-lactate environments. Cell Metab. 2017;25(6):1282–1293.e7.
   PubMed Web of Science ®Google Scholar
• van Loosdregt J, Vercoulen Y, Guichelaar T, et al. Regulation of Treg functionality by acetylation-mediated Foxp3 protein stabilization. Blood. 2010;115(5):965–974.
   PubMed Web of Science ®Google Scholar
• Fan MY, Turka LA. Immunometabolism and PI (3) K signaling as a link between IL-2, Foxp3 expression, and suppressor function in regulatory T cells. Front Immunol. 2018;9:69.
   PubMed Web of Science ®Google Scholar
• Michalek RD, Gerriets VA, Jacobs SR, et al. Cutting edge: distinct glycolytic and lipid oxidative metabolic programs are essential for effector and regulatory CD4+ T cell subsets. J Immunol. 2011;186(6):3299–3303.
   PubMed Web of Science ®Google Scholar
• Coe DJ, Kishore M, Marelli-Berg F. Metabolic regulation of regulatory T cell development and function. Front Immunol. 2014;5:590.
   PubMed Web of Science ®Google Scholar
• Weinberg SE, Singer BD, Steinert EM, et al. Mitochondrial complex III is essential for suppressive function of regulatory T cells. Nature. 2019;565(7740):495–499.
   PubMed Web of Science ®Google Scholar
• Howie D, Cobbold SP, Adams E, et al. Foxp3 drives oxidative phosphorylation and protection from lipotoxicity. JCI Insight. 2017;2(3):e89160.
   Web of Science ®Google Scholar
• Kraaij MD, Savage ND, van der Kooij SW, et al. Induction of regulatory T cells by macrophages is dependent on production of reactive oxygen species. Proc Natl Acad Sci USA. 2010;107(41):17686–17691.
   PubMed Web of Science ®Google Scholar
• Kim HR, Lee A, Choi EJ, et al. Attenuation of experimental colitis in glutathione peroxidase 1 and catalase double knockout mice through enhancing regulatory T cell function. PLoS One. 2014;9(4):e95332.
   PubMed Web of Science ®Google Scholar
• Tagaya Y, Maeda Y, Mitsui A, et al. ATL-derived factor (ADF), an IL-2 receptor/Tac inducer homologous to thioredoxin; possible involvement of dithiol-reduction in the IL-2 receptor induction. EMBO J. 1989;8(3):757–764.
   PubMed Web of Science ®Google Scholar
• Schenk H, Vogt M, Dröge W, et al. Thioredoxin as a potent costimulus of cytokine expression. J Immunol. 1996;156(2):765–771.
   PubMed Web of Science ®Google Scholar
• Lorenzen I, Mullen L, Bekeschus S, et al. Redox regulation of inflammatory processes is enzymatically controlled. Oxid Med Cell Longev. 2017;2017:1–23.
   Web of Science ®Google Scholar
• Mougiakakos D, Johansson CC, Jitschin R, et al. Increased thioredoxin-1 production in human naturally occurring regulatory T cells confers enhanced tolerance to oxidative stress. Blood. 2011;117(3):857–861.
   PubMed Web of Science ®Google Scholar
• Mougiakakos D, Johansson CC, Kiessling R. Naturally occurring regulatory T cells show reduced sensitivity toward oxidative stress-induced cell death. Blood. 2009;113(15):3542–3545.
   PubMed Web of Science ®Google Scholar
• Jang Y-Y, Sharkis SJ. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood. 2007;110(8):3056–3063.
   PubMed Web of Science ®Google Scholar
• Sundaresan M, Yu Z-X, Ferrans VJ, et al. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science. 1995;270(5234):296–299.
   PubMed Web of Science ®Google Scholar
• André-Lévigne D, Modarressi A, Pepper M, et al. Reactive oxygen species and NOX enzymes are emerging as key players in cutaneous wound repair. Int J Mol Sci. 2017;18(10):2149.
   Web of Science ®Google Scholar
• Mathur AN, Zirak B, Boothby IC, et al. Treg-cell control of a CXCL5-IL-17 inflammatory axis promotes hair-follicle-stem-cell differentiation during skin-barrier repair. Immunity. 2019;50(3):655–667. e4.
   PubMed Web of Science ®Google Scholar
• Jauniaux E, Gulbis B, Burton GJ. The human first trimester gestational sac limits rather than facilitates oxygen transfer to the foetus: a review. Placenta. 2003;24:S86–S93.
   PubMed Web of Science ®Google Scholar
• Jauniaux E, Poston L, Burton GJ. Placental-related diseases of pregnancy: Involvement of oxidative stress and implications in human evolution. Hum Reprod Update. 2006;12(6):747–755.
   PubMed Web of Science ®Google Scholar
• Okazaki KM, Maltepe E. Oxygen, epigenetics and stem cell fate. 2006.
   Google Scholar
• Jauniaux E, Watson AL, Hempstock J, et al. Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am J Pathol. 2000;157(6):2111–2122.
   PubMed Web of Science ®Google Scholar
• Jauniaux E, Pahal G, Gervy C, et al. Blood biochemistry and endocrinology in the human fetus between 11 and 17 weeks of gestation. Reprod Biomed Online. 2000;1(2):38–44.
   PubMedGoogle Scholar
• Burton GJ, Hempstock J, Jauniaux E. Oxygen, early embryonic metabolism and free radical-mediated embryopathies. Reprod Biomed Online. 2003;6(1):84–96.
   PubMedGoogle Scholar
• Halliwell B, Gutteridge JM. Free radicals in biology and medicine. USA: Oxford University Press; 2015.
   Google Scholar
• Imanirad P, Dzierzak E. Hypoxia and HIFs in regulating the development of the hematopoietic system. Blood Cells Mol Dis. 2013;51(4):256–263.
   PubMed Web of Science ®Google Scholar
• Simon MC, Keith B. The role of oxygen availability in embryonic development and stem cell function. Nat Rev Mol Cell Biol. 2008;9(4):285–296.
   PubMed Web of Science ®Google Scholar
• Maltepe E, Schmidt JV, Baunoch D, et al. Abnormal angiogenesis and responses to glucose and oxygen deprivation in mice lacking the protein ARNT. Nature. 1997;386(6623):403–407.
   PubMed Web of Science ®Google Scholar
• Scortegagna M, Morris MA, Oktay Y, et al. The HIF family member EPAS1/HIF-2α is required for normal hematopoiesis in mice. Blood. 2003;102(5):1634–1640.
   PubMed Web of Science ®Google Scholar
• McGovern N, Shin A, Low G, et al. Human fetal dendritic cells promote prenatal T-cell immune suppression through arginase-2. Nature. 2017;546(7660):662–666.
   PubMed Web of Science ®Google Scholar
• Michaëlsson J, Mold JE, McCune JM, Nixon DF. Regulation of T cell responses in the developing human fetus. J Immunol. 2006;176(10):5741–5748.
   PubMed Web of Science ®Google Scholar
• Mold JE, Venkatasubrahmanyam S, Burt TD, et al. Fetal and adult hematopoietic stem cells give rise to distinct T cell lineages in humans. Science. 2010;330(6011):1695–1699.
   PubMed Web of Science ®Google Scholar
• Semenza GL. Oxygen sensing, homeostasis, and disease. N Engl J Med. 2011;365(6):537–547.
   PubMed Web of Science ®Google Scholar
• Wenger RH, Stiehl DP, Camenisch G. Integration of oxygen signaling at the consensus HRE. Sci STKE. 2005;2005(306):re12–re12.
   PubMedGoogle Scholar
• Semenza GL. Hypoxia-inducible factor 1 and cardiovascular disease. Annu Rev Physiol. 2014;76(1):39–56.
   PubMedGoogle Scholar
• Clambey ET, McNamee EN, Westrich JA, et al. Hypoxia-inducible factor-1 alpha-dependent induction of FoxP3 drives regulatory T-cell abundance and function during inflammatory hypoxia of the mucosa. Proc Natl Acad Sci USA. 2012;109(41):E2784–E2793.
   PubMed Web of Science ®Google Scholar
• Ben-Shoshan J, Maysel-Auslender S, Mor A, et al. Hypoxia controls CD4 + CD25+ regulatory T-cell homeostasis via hypoxia-inducible factor-1alpha. Eur J Immunol. 2008;38(9):2412–2418.
   PubMed Web of Science ®Google Scholar
• Kenneth NS, Rocha S. Regulation of gene expression by hypoxia. Biochem J. 2008;414(1):19–29.
   PubMedGoogle Scholar
• Thome JJ, Bickham KL, Ohmura Y, et al. Early-life compartmentalization of human T cell differentiation and regulatory function in mucosal and lymphoid tissues. Nat Med. 2016;22(1):72–77.
   PubMed Web of Science ®Google Scholar
• Maj T, Wang W, Crespo J, et al. Oxidative stress controls regulatory T cell apoptosis and suppressor activity and PD-L1-blockade resistance in tumor. Nat Immunol. 2017;18(12):1332–1341.
   PubMed Web of Science ®Google Scholar
• Hytten F. Blood volume changes in normal pregnancy. Clin Haematol. 1985;14(3):601–612.
   PubMedGoogle Scholar
• Jauniaux E, Cindrova-Davies T, Johns J, et al. Distribution and transfer pathways of antioxidant molecules inside the first trimester human gestational sac. J Clin Endocrinol Metab. 2004;89(3):1452–1458.
   PubMed Web of Science ®Google Scholar
• Sasaki Y, Sakai M, Miyazaki S, et al. Decidual and peripheral blood CD4+ CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. MHR: Basic Sci Reprod Med. 2004;10(5):347–353.
   Google Scholar
• Gerriets VA, Kishton RJ, Nichols AG, et al. Metabolic programming and PDHK1 control CD4+ T cell subsets and inflammation. J Clin Invest. 2015;125(1):194–207.
   PubMed Web of Science ®Google Scholar
• Lain KY, Catalano PM. Metabolic changes in pregnancy. Clin Obstet Gynecol. 2007;50(4):938–948.
   PubMed Web of Science ®Google Scholar
• van der Veeken J, Gonzalez AJ, Cho H, et al. Memory of inflammation in regulatory T cells. Cell. 2016;166(4):977–990.
   PubMed Web of Science ®Google Scholar
• Masson N, Singleton RS, Sekirnik R, et al. The FIH hydroxylase is a cellular peroxide sensor that modulates HIF transcriptional activity. EMBO Rep. 2012;13(3):251–257.
   PubMed Web of Science ®Google Scholar
• Dang EV, Barbi J, Yang HY, et al. Control of T(H)17/T(reg) balance by hypoxia-inducible factor 1. Cell. 2011;146(5):772–784.
   PubMed Web of Science ®Google Scholar
• Doedens AL, Phan AT, Stradner MH, et al. Hypoxia-inducible factors enhance the effector responses of CD8(+) T cells to persistent antigen. Nat Immunol. 2013;14(11):1173–1182.
   PubMed Web of Science ®Google Scholar
• Lee JH, Elly C, Park Y, et al. E3 ubiquitin ligase VHL regulates hypoxia-inducible factor-1α to maintain regulatory T cell stability and suppressive capacity. Immunity. 2015;42(6):1062–1074.
   PubMed Web of Science ®Google Scholar
• Hsiao HW, Hsu TS, Liu WH, et al. Deltex1 antagonizes HIF-1α and sustains the stability of regulatory T cells in vivo. Nat Commun. 2015;6(1):6353.
   PubMedGoogle Scholar
• Mascanfroni ID, Takenaka MC, Yeste A, et al. Metabolic control of type 1 regulatory T cell differentiation by AHR and HIF1α. Nat Med. 2015;21(6):638–646.
   PubMed Web of Science ®Google Scholar
• Feldhoff LM, Rueda CM, Moreno-Fernandez ME, et al. IL-1β induced HIF-1α inhibits the differentiation of human FOXP3. Sci Rep. 2017;7(1):465.
   PubMedGoogle Scholar
• Tao JH, Barbi J, Pan F. Hypoxia-inducible factors in T lymphocyte differentiation and function. A review in the theme: cellular responses to hypoxia. Am J Physiol Cell Physiol. 2015;309(9):C580–C589.
   PubMed Web of Science ®Google Scholar
• Tsai JJ, Velardi E, Shono Y, et al. Nrf2 regulates CD4+ T cell-induced acute graft-versus-host disease in mice. Blood. 2018;132(26):2763–2774.
   PubMed Web of Science ®Google Scholar
• Suzuki T, Murakami S, Biswal SS, et al. Systemic activation of NRF2 alleviates lethal autoimmune inflammation in scurfy mice. Mol Cell Biol. 2017;37(15):e00063–e00017.
   PubMed Web of Science ®Google Scholar
• Liguori I, Russo G, Curcio F, et al. Oxidative stress, aging, and diseases. Clin Interv Aging. 2018;13:757–772.
   PubMed Web of Science ®Google Scholar
• Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature. 2000;408(6809):239–247.
   PubMed Web of Science ®Google Scholar
• López-Otín C, Blasco MA, Partridge L, et al. The hallmarks of aging. Cell. 2013;153(6):1194–1217.
   PubMed Web of Science ®Google Scholar
• Espinosa-Diez C, Miguel V, Mennerich D, et al. Antioxidant responses and cellular adjustments to oxidative stress. Redox Biol. 2015;6:183–197.
   PubMed Web of Science ®Google Scholar
• Jones DP, Mody VC Jr., Carlson JL, et al. Redox analysis of human plasma allows separation of pro-oxidant events of aging from decline in antioxidant defenses. Free Radical Biol Med. 2002;33(9):1290–1300.
   PubMed Web of Science ®Google Scholar
• Jones DP, Carlson JL, Mody VC, Jr, et al. Redox state of glutathione in human plasma. Free Radical Biol Med. 2000;28(4):625–635.
   PubMed Web of Science ®Google Scholar
• Marengo B, Nitti M, Furfaro AL, et al. Redox homeostasis and cellular antioxidant systems: crucial players in cancer growth and therapy. Oxid Med Cell Longevity . 2016;2016:1–16.
   Web of Science ®Google Scholar
• Garg SK, Delaney C, Toubai T, et al. Aging is associated with increased regulatory T‐cell function. Aging Cell. 2014;13(3):441–448.
   PubMed Web of Science ®Google Scholar
• Hayakawa S, Ohno N, Okada S, et al. Significant augmentation of regulatory T cell numbers occurs during the early neonatal period. Clin Exp Immunol. 2017;190(2):268–279.
   PubMed Web of Science ®Google Scholar
• Wang G, Miyahara Y, Guo Z, et al. Default” generation of neonatal regulatory T cells. JI. 2010;185(1):71–78.
   Google Scholar
• Miyara M, Yoshioka Y, Kitoh A, et al. Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity. 2009;30(6):899–911.
   PubMed Web of Science ®Google Scholar
• Hou P-F, Zhu L-J, Chen X-Y, et al. Age-related changes in CD4+ CD25+ FOXP3+ regulatory T cells and their relationship with lung cancer. PloS One. 2017;12(3):e0173048.
   PubMed Web of Science ®Google Scholar