Stable human regulatory T cells switch to glycolysis following TNF receptor 2 costimulation

Following activation, conventional T (T conv ) cells undergo an mTOR-driven glycolytic switch. Regulatory T (T reg ) cells reportedly repress the mTOR pathway and avoid glycolysis. However, here we demonstrate that human thymus-derived T reg (tT reg ) cells can become glycolytic in response to tumou...

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Vydané v:Nature metabolism Ročník 2; číslo 10; s. 1046 - 1061
Hlavní autori: de Kivit, Sander, Mensink, Mark, Hoekstra, Anna T., Berlin, Ilana, Derks, Rico J. E., Both, Demi, Aslam, Muhammad A., Amsen, Derk, Berkers, Celia R., Borst, Jannie
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: London Nature Publishing Group UK 01.10.2020
Nature Publishing Group
Predmet:
1-Phosphatidylinositol 3-kinase
631/250/1619/554
631/250/2152
631/443/319
631/45/320
Antigens
Biomedical and Life Sciences
Blood
Carbon
CD25 antigen
CD3 antigen
CD3 Complex - metabolism
Cell activation
Cell proliferation
Citric Acid Cycle - drug effects
Effector cells
Flow cytometry
Foxp3 protein
Glucose
Glucose - metabolism
Glucose - pharmacology
Glycolysis
Glycolysis - drug effects
Humans
Immunoregulation
Kinases
Lactic acid
Lactic Acid - blood
Lactic Acid - metabolism
Life Sciences
Lymphocytes
Lymphocytes T
Metabolism
Metabolites
Metabolome
Monoclonal antibodies
Phosphatidylinositol 3-Kinases - metabolism
Proteins
Protocol
Receptors, Tumor Necrosis Factor, Type II - drug effects
Receptors, Tumor Necrosis Factor, Type II - metabolism
RNA - chemistry
Sequence Analysis, RNA
Signal Transduction
Statistical analysis
T-Lymphocytes, Regulatory - metabolism
Thymus
TOR protein
TOR Serine-Threonine Kinases - metabolism
Tricarboxylic acid cycle
Tumor necrosis factor receptors
Tumor necrosis factor-TNF
Variance analysis
ISSN:2522-5812, 2522-5812
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Abstract Following activation, conventional T (T conv ) cells undergo an mTOR-driven glycolytic switch. Regulatory T (T reg ) cells reportedly repress the mTOR pathway and avoid glycolysis. However, here we demonstrate that human thymus-derived T reg (tT reg ) cells can become glycolytic in response to tumour necrosis factor receptor 2 (TNFR2) costimulation. This costimulus increases proliferation and induces a glycolytic switch in CD3-activated tT reg cells, but not in T conv cells. Glycolysis in CD3–TNFR2-activated tT reg cells is driven by PI3-kinase–mTOR signalling and supports tT reg cell identity and suppressive function. In contrast to glycolytic T conv cells, glycolytic tT reg cells do not show net lactate secretion and shuttle glucose-derived carbon into the tricarboxylic acid cycle. Ex vivo characterization of blood-derived TNFR2 hi CD4 + CD25 hi CD127 lo effector T cells, which were FOXP3 + IKZF2 + , revealed an increase in glucose consumption and intracellular lactate levels, thus identifying them as glycolytic tT reg cells. Our study links TNFR2 costimulation in human tT reg cells to metabolic remodelling, providing an additional avenue for drug targeting. After activation, conventional T cells undergo metabolic reprogramming. de Kivit et al. show that in human thymic regulatory T cells, TNFR2 stimulation promotes a glycolytic switch with a preferential glucose-derived carbon flux into the TCA cycle to support suppressive functions.
AbstractList Following activation, conventional T (Tconv) cells undergo an mTOR-driven glycolytic switch. Regulatory T (Treg) cells reportedly repress the mTOR pathway and avoid glycolysis. However, here we demonstrate that human thymus-derived Treg (tTreg) cells can become glycolytic in response to tumour necrosis factor receptor 2 (TNFR2) costimulation. This costimulus increases proliferation and induces a glycolytic switch in CD3-activated tTreg cells, but not in Tconv cells. Glycolysis in CD3-TNFR2-activated tTreg cells is driven by PI3-kinase-mTOR signalling and supports tTreg cell identity and suppressive function. In contrast to glycolytic Tconv cells, glycolytic tTreg cells do not show net lactate secretion and shuttle glucose-derived carbon into the tricarboxylic acid cycle. Ex vivo characterization of blood-derived TNFR2hiCD4+CD25hiCD127lo effector T cells, which were FOXP3+IKZF2+, revealed an increase in glucose consumption and intracellular lactate levels, thus identifying them as glycolytic tTreg cells. Our study links TNFR2 costimulation in human tTreg cells to metabolic remodelling, providing an additional avenue for drug targeting.Following activation, conventional T (Tconv) cells undergo an mTOR-driven glycolytic switch. Regulatory T (Treg) cells reportedly repress the mTOR pathway and avoid glycolysis. However, here we demonstrate that human thymus-derived Treg (tTreg) cells can become glycolytic in response to tumour necrosis factor receptor 2 (TNFR2) costimulation. This costimulus increases proliferation and induces a glycolytic switch in CD3-activated tTreg cells, but not in Tconv cells. Glycolysis in CD3-TNFR2-activated tTreg cells is driven by PI3-kinase-mTOR signalling and supports tTreg cell identity and suppressive function. In contrast to glycolytic Tconv cells, glycolytic tTreg cells do not show net lactate secretion and shuttle glucose-derived carbon into the tricarboxylic acid cycle. Ex vivo characterization of blood-derived TNFR2hiCD4+CD25hiCD127lo effector T cells, which were FOXP3+IKZF2+, revealed an increase in glucose consumption and intracellular lactate levels, thus identifying them as glycolytic tTreg cells. Our study links TNFR2 costimulation in human tTreg cells to metabolic remodelling, providing an additional avenue for drug targeting.
Following activation, conventional T (Tconv) cells undergo an mTOR-driven glycolytic switch. Regulatory T (Treg) cells reportedly repress the mTOR pathway and avoid glycolysis. However, here we demonstrate that human thymus-derived Treg (tTreg) cells can become glycolytic in response to tumour necrosis factor receptor 2 (TNFR2) costimulation. This costimulus increases proliferation and induces a glycolytic switch in CD3-activated tTreg cells, but not in Tconv cells. Glycolysis in CD3–TNFR2-activated tTreg cells is driven by PI3-kinase–mTOR signalling and supports tTreg cell identity and suppressive function. In contrast to glycolytic Tconv cells, glycolytic tTreg cells do not show net lactate secretion and shuttle glucose-derived carbon into the tricarboxylic acid cycle. Ex vivo characterization of blood-derived TNFR2hiCD4+CD25hiCD127lo effector T cells, which were FOXP3+IKZF2+, revealed an increase in glucose consumption and intracellular lactate levels, thus identifying them as glycolytic tTreg cells. Our study links TNFR2 costimulation in human tTreg cells to metabolic remodelling, providing an additional avenue for drug targeting.After activation, conventional T cells undergo metabolic reprogramming. de Kivit et al. show that in human thymic regulatory T cells, TNFR2 stimulation promotes a glycolytic switch with a preferential glucose-derived carbon flux into the TCA cycle to support suppressive functions.
Following activation, conventional T (T ) cells undergo an mTOR-driven glycolytic switch. Regulatory T (T ) cells reportedly repress the mTOR pathway and avoid glycolysis. However, here we demonstrate that human thymus-derived T (tT ) cells can become glycolytic in response to tumour necrosis factor receptor 2 (TNFR2) costimulation. This costimulus increases proliferation and induces a glycolytic switch in CD3-activated tT cells, but not in T cells. Glycolysis in CD3-TNFR2-activated tT cells is driven by PI3-kinase-mTOR signalling and supports tT cell identity and suppressive function. In contrast to glycolytic T cells, glycolytic tT cells do not show net lactate secretion and shuttle glucose-derived carbon into the tricarboxylic acid cycle. Ex vivo characterization of blood-derived TNFR2 CD4 CD25 CD127 effector T cells, which were FOXP3 IKZF2 , revealed an increase in glucose consumption and intracellular lactate levels, thus identifying them as glycolytic tT cells. Our study links TNFR2 costimulation in human tT cells to metabolic remodelling, providing an additional avenue for drug targeting.
Following activation, conventional T (T conv ) cells undergo an mTOR-driven glycolytic switch. Regulatory T (T reg ) cells reportedly repress the mTOR pathway and avoid glycolysis. However, here we demonstrate that human thymus-derived T reg (tT reg ) cells can become glycolytic in response to tumour necrosis factor receptor 2 (TNFR2) costimulation. This costimulus increases proliferation and induces a glycolytic switch in CD3-activated tT reg cells, but not in T conv cells. Glycolysis in CD3–TNFR2-activated tT reg cells is driven by PI3-kinase–mTOR signalling and supports tT reg cell identity and suppressive function. In contrast to glycolytic T conv cells, glycolytic tT reg cells do not show net lactate secretion and shuttle glucose-derived carbon into the tricarboxylic acid cycle. Ex vivo characterization of blood-derived TNFR2 hi CD4 + CD25 hi CD127 lo effector T cells, which were FOXP3 + IKZF2 + , revealed an increase in glucose consumption and intracellular lactate levels, thus identifying them as glycolytic tT reg cells. Our study links TNFR2 costimulation in human tT reg cells to metabolic remodelling, providing an additional avenue for drug targeting. After activation, conventional T cells undergo metabolic reprogramming. de Kivit et al. show that in human thymic regulatory T cells, TNFR2 stimulation promotes a glycolytic switch with a preferential glucose-derived carbon flux into the TCA cycle to support suppressive functions.
Author de Kivit, Sander
Berkers, Celia R.
Berlin, Ilana
Hoekstra, Anna T.
Derks, Rico J. E.
Mensink, Mark
Both, Demi
Aslam, Muhammad A.
Amsen, Derk
Borst, Jannie
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  orcidid: 0000-0002-2470-6919
  surname: Mensink
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  organization: Department of Immunohematology and Blood Transfusion, Leiden University Medical Center, Oncode Institute, Leiden University Medical Center, Division of Tumor Biology & Immunology, The Netherlands Cancer Institute
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  givenname: Anna T.
  surname: Hoekstra
  fullname: Hoekstra, Anna T.
  organization: Biomolecular Mass Spectrometry and Proteomics, Bijvoet Center for Biomolecular Research, Utrecht University
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  surname: Berlin
  fullname: Berlin, Ilana
  organization: Oncode Institute, Leiden University Medical Center, Department of Cell and Chemical Biology, Leiden University Medical Center
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  fullname: Aslam, Muhammad A.
  organization: Division of Tumor Biology & Immunology, The Netherlands Cancer Institute
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  surname: Amsen
  fullname: Amsen, Derk
  organization: Department of Hematopoiesis, Sanquin Research and Landsteiner Laboratory
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  givenname: Celia R.
  orcidid: 0000-0003-0746-8565
  surname: Berkers
  fullname: Berkers, Celia R.
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  organization: Department of Immunohematology and Blood Transfusion, Leiden University Medical Center, Oncode Institute, Leiden University Medical Center, Division of Tumor Biology & Immunology, The Netherlands Cancer Institute
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Snippet Following activation, conventional T (T conv ) cells undergo an mTOR-driven glycolytic switch. Regulatory T (T reg ) cells reportedly repress the mTOR pathway...
Following activation, conventional T (T ) cells undergo an mTOR-driven glycolytic switch. Regulatory T (T ) cells reportedly repress the mTOR pathway and avoid...
Following activation, conventional T (Tconv) cells undergo an mTOR-driven glycolytic switch. Regulatory T (Treg) cells reportedly repress the mTOR pathway and...
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StartPage 1046
SubjectTerms 1-Phosphatidylinositol 3-kinase
631/250/1619/554
631/250/2152
631/443/319
631/45/320
Antigens
Biomedical and Life Sciences
Blood
Carbon
CD25 antigen
CD3 antigen
CD3 Complex - metabolism
Cell activation
Cell proliferation
Citric Acid Cycle - drug effects
Effector cells
Flow cytometry
Foxp3 protein
Glucose
Glucose - metabolism
Glucose - pharmacology
Glycolysis
Glycolysis - drug effects
Humans
Immunoregulation
Kinases
Lactic acid
Lactic Acid - blood
Lactic Acid - metabolism
Life Sciences
Lymphocytes
Lymphocytes T
Metabolism
Metabolites
Metabolome
Monoclonal antibodies
Phosphatidylinositol 3-Kinases - metabolism
Proteins
Protocol
Receptors, Tumor Necrosis Factor, Type II - drug effects
Receptors, Tumor Necrosis Factor, Type II - metabolism
RNA - chemistry
Sequence Analysis, RNA
Signal Transduction
Statistical analysis
T-Lymphocytes, Regulatory - metabolism
Thymus
TOR protein
TOR Serine-Threonine Kinases - metabolism
Tricarboxylic acid cycle
Tumor necrosis factor receptors
Tumor necrosis factor-TNF
Variance analysis
Title Stable human regulatory T cells switch to glycolysis following TNF receptor 2 costimulation
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