AustralieFrV1, PubMed, Curation, bibRecord, 002859

Glutamine-dependent α-ketoglutarate production regulates the balance between T helper 1 cell and regulatory T cell generation.

Identifieur interne : 002859 ( PubMed/Curation ); précédent : 002858; suivant : 002860

Glutamine-dependent α-ketoglutarate production regulates the balance between T helper 1 cell and regulatory T cell generation.

Auteurs : Dorota Klysz [France] ; Xuguang Tai [États-Unis] ; Philippe A. Robert [Allemagne] ; Marco Craveiro [France] ; Gaspard Cretenet [France] ; Leal Oburoglu [France] ; Cédric Mongellaz [France] ; Stefan Floess [Allemagne] ; Vanessa Fritz [France] ; Maria I. Matias [France] ; Carmen Yong [Australie] ; Natalie Surh [France] ; Julien C. Marie [Allemagne] ; Jochen Huehn [Allemagne] ; Valérie Zimmermann [France] ; Sandrina Kinet [France] ; Valérie Dardalhon [France] ; Naomi Taylor [France]

Source :

Science signaling [ 1937-9145 ] ; 2015.

RBID : pubmed:26420908

Descripteurs français

English descriptors

KwdEn :
- Animals, Cell Differentiation (immunology), Glutamine (immunology), Glutamine (metabolism), Ketoglutaric Acids (immunology), Ketoglutaric Acids (metabolism), Mice, Multiprotein Complexes (immunology), Multiprotein Complexes (metabolism), T-Lymphocytes, Regulatory (immunology), T-Lymphocytes, Regulatory (metabolism), TOR Serine-Threonine Kinases (immunology), TOR Serine-Threonine Kinases (metabolism), Th1 Cells (immunology), Th1 Cells (metabolism).
MESH :
- chemical , immunology : Glutamine, Ketoglutaric Acids, Multiprotein Complexes, TOR Serine-Threonine Kinases.
- immunology : Cell Differentiation, T-Lymphocytes, Regulatory, Th1 Cells.
- chemical , metabolism : Glutamine, Ketoglutaric Acids, Multiprotein Complexes, T-Lymphocytes, Regulatory, TOR Serine-Threonine Kinases, Th1 Cells.
- Animals, Mice.

Abstract

T cell activation requires that the cell meet increased energetic and biosynthetic demands. We showed that exogenous nutrient availability regulated the differentiation of naïve CD4(+) T cells into distinct subsets. Activation of naïve CD4(+) T cells under conditions of glutamine deprivation resulted in their differentiation into Foxp3(+) (forkhead box P3-positive) regulatory T (Treg) cells, which had suppressor function in vivo. Moreover, glutamine-deprived CD4(+) T cells that were activated in the presence of cytokines that normally induce the generation of T helper 1 (TH1) cells instead differentiated into Foxp3(+) Treg cells. We found that α-ketoglutarate (αKG), the glutamine-derived metabolite that enters into the mitochondrial citric acid cycle, acted as a metabolic regulator of CD4(+) T cell differentiation. Activation of glutamine-deprived naïve CD4(+) T cells in the presence of a cell-permeable αKG analog increased the expression of the gene encoding the TH1 cell-associated transcription factor Tbet and resulted in their differentiation into TH1 cells, concomitant with stimulation of mammalian target of rapamycin complex 1 (mTORC1) signaling. Together, these data suggest that a decrease in the intracellular amount of αKG, caused by the limited availability of extracellular glutamine, shifts the balance between the generation of TH1 and Treg cells toward that of a Treg phenotype.

DOI: 10.1126/scisignal.aab2610
PubMed: 26420908

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<author><name sortKey="Matias, Maria I" sort="Matias, Maria I" uniqKey="Matias M" first="Maria I" last="Matias">Maria I. Matias</name>
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<author><name sortKey="Kinet, Sandrina" sort="Kinet, Sandrina" uniqKey="Kinet S" first="Sandrina" last="Kinet">Sandrina Kinet</name>
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<country xml:lang="fr">France</country>
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<author><name sortKey="Taylor, Naomi" sort="Taylor, Naomi" uniqKey="Taylor N" first="Naomi" last="Taylor">Naomi Taylor</name>
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<author><name sortKey="Tai, Xuguang" sort="Tai, Xuguang" uniqKey="Tai X" first="Xuguang" last="Tai">Xuguang Tai</name>
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<author><name sortKey="Robert, Philippe A" sort="Robert, Philippe A" uniqKey="Robert P" first="Philippe A" last="Robert">Philippe A. Robert</name>
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<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Institut de Génétique Moléculaire de Montpellier, CNRS, UMR 5535, Université de Montpellier, F-34293 Montpellier, France. Department of Systems Immunology, Braunschweig Integrated Centre of Systems Biology, 38124 Braunschweig</wicri:regionArea>
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<author><name sortKey="Craveiro, Marco" sort="Craveiro, Marco" uniqKey="Craveiro M" first="Marco" last="Craveiro">Marco Craveiro</name>
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<country xml:lang="fr">France</country>
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<author><name sortKey="Cretenet, Gaspard" sort="Cretenet, Gaspard" uniqKey="Cretenet G" first="Gaspard" last="Cretenet">Gaspard Cretenet</name>
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<country xml:lang="fr">France</country>
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<author><name sortKey="Oburoglu, Leal" sort="Oburoglu, Leal" uniqKey="Oburoglu L" first="Leal" last="Oburoglu">Leal Oburoglu</name>
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<country xml:lang="fr">France</country>
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</affiliation>
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<author><name sortKey="Mongellaz, Cedric" sort="Mongellaz, Cedric" uniqKey="Mongellaz C" first="Cédric" last="Mongellaz">Cédric Mongellaz</name>
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<country xml:lang="fr">France</country>
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</affiliation>
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<author><name sortKey="Floess, Stefan" sort="Floess, Stefan" uniqKey="Floess S" first="Stefan" last="Floess">Stefan Floess</name>
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<wicri:regionArea>Department of Experimental Immunology, Helmholtz Centre for Infection Research, 38124 Braunschweig</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Fritz, Vanessa" sort="Fritz, Vanessa" uniqKey="Fritz V" first="Vanessa" last="Fritz">Vanessa Fritz</name>
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<country xml:lang="fr">France</country>
<wicri:regionArea>Institut de Génétique Moléculaire de Montpellier, CNRS, UMR 5535, Université de Montpellier, F-34293 Montpellier</wicri:regionArea>
</affiliation>
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<author><name sortKey="Matias, Maria I" sort="Matias, Maria I" uniqKey="Matias M" first="Maria I" last="Matias">Maria I. Matias</name>
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<country xml:lang="fr">France</country>
<wicri:regionArea>Institut de Génétique Moléculaire de Montpellier, CNRS, UMR 5535, Université de Montpellier, F-34293 Montpellier</wicri:regionArea>
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<author><name sortKey="Yong, Carmen" sort="Yong, Carmen" uniqKey="Yong C" first="Carmen" last="Yong">Carmen Yong</name>
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<country xml:lang="fr">Australie</country>
<wicri:regionArea>Institut de Génétique Moléculaire de Montpellier, CNRS, UMR 5535, Université de Montpellier, F-34293 Montpellier, France. Cancer Immunology Research Program, Sir Peter MacCallum Department of Oncology, University of Melbourne, Parkville, Victoria 3010</wicri:regionArea>
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<author><name sortKey="Surh, Natalie" sort="Surh, Natalie" uniqKey="Surh N" first="Natalie" last="Surh">Natalie Surh</name>
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<country xml:lang="fr">France</country>
<wicri:regionArea>Institut de Génétique Moléculaire de Montpellier, CNRS, UMR 5535, Université de Montpellier, F-34293 Montpellier</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Marie, Julien C" sort="Marie, Julien C" uniqKey="Marie J" first="Julien C" last="Marie">Julien C. Marie</name>
<affiliation wicri:level="1"><nlm:affiliation>Cancer Research Center of Lyon, INSERM U1052, CNRS 5286, Université Lyon 1, 69373 Lyon cedex 03, France. DKFZ German Cancer Research Center, 69121 Heidelberg, Germany.</nlm:affiliation>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Cancer Research Center of Lyon, INSERM U1052, CNRS 5286, Université Lyon 1, 69373 Lyon cedex 03, France. DKFZ German Cancer Research Center, 69121 Heidelberg</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Huehn, Jochen" sort="Huehn, Jochen" uniqKey="Huehn J" first="Jochen" last="Huehn">Jochen Huehn</name>
<affiliation wicri:level="1"><nlm:affiliation>Department of Experimental Immunology, Helmholtz Centre for Infection Research, 38124 Braunschweig, Germany.</nlm:affiliation>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Department of Experimental Immunology, Helmholtz Centre for Infection Research, 38124 Braunschweig</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Zimmermann, Valerie" sort="Zimmermann, Valerie" uniqKey="Zimmermann V" first="Valérie" last="Zimmermann">Valérie Zimmermann</name>
<affiliation wicri:level="1"><nlm:affiliation>Institut de Génétique Moléculaire de Montpellier, CNRS, UMR 5535, Université de Montpellier, F-34293 Montpellier, France.</nlm:affiliation>
<country xml:lang="fr">France</country>
<wicri:regionArea>Institut de Génétique Moléculaire de Montpellier, CNRS, UMR 5535, Université de Montpellier, F-34293 Montpellier</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Kinet, Sandrina" sort="Kinet, Sandrina" uniqKey="Kinet S" first="Sandrina" last="Kinet">Sandrina Kinet</name>
<affiliation wicri:level="1"><nlm:affiliation>Institut de Génétique Moléculaire de Montpellier, CNRS, UMR 5535, Université de Montpellier, F-34293 Montpellier, France.</nlm:affiliation>
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<series><title level="j">Science signaling</title>
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<term>Cell Differentiation (immunology)</term>
<term>Glutamine (immunology)</term>
<term>Glutamine (metabolism)</term>
<term>Ketoglutaric Acids (immunology)</term>
<term>Ketoglutaric Acids (metabolism)</term>
<term>Mice</term>
<term>Multiprotein Complexes (immunology)</term>
<term>Multiprotein Complexes (metabolism)</term>
<term>T-Lymphocytes, Regulatory (immunology)</term>
<term>T-Lymphocytes, Regulatory (metabolism)</term>
<term>TOR Serine-Threonine Kinases (immunology)</term>
<term>TOR Serine-Threonine Kinases (metabolism)</term>
<term>Th1 Cells (immunology)</term>
<term>Th1 Cells (metabolism)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>Acides cétoglutariques (immunologie)</term>
<term>Acides cétoglutariques (métabolisme)</term>
<term>Animaux</term>
<term>Complexes multiprotéiques (immunologie)</term>
<term>Complexes multiprotéiques (métabolisme)</term>
<term>Différenciation cellulaire (immunologie)</term>
<term>Glutamine (immunologie)</term>
<term>Glutamine (métabolisme)</term>
<term>Lymphocytes T régulateurs (immunologie)</term>
<term>Lymphocytes T régulateurs (métabolisme)</term>
<term>Lymphocytes auxiliaires Th1 (immunologie)</term>
<term>Lymphocytes auxiliaires Th1 (métabolisme)</term>
<term>Souris</term>
<term>Sérine-thréonine kinases TOR (immunologie)</term>
<term>Sérine-thréonine kinases TOR (métabolisme)</term>
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<term>Ketoglutaric Acids</term>
<term>Multiprotein Complexes</term>
<term>TOR Serine-Threonine Kinases</term>
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<term>Complexes multiprotéiques</term>
<term>Différenciation cellulaire</term>
<term>Glutamine</term>
<term>Lymphocytes T régulateurs</term>
<term>Lymphocytes auxiliaires Th1</term>
<term>Sérine-thréonine kinases TOR</term>
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<keywords scheme="MESH" qualifier="immunology" xml:lang="en"><term>Cell Differentiation</term>
<term>T-Lymphocytes, Regulatory</term>
<term>Th1 Cells</term>
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<front><div type="abstract" xml:lang="en">T cell activation requires that the cell meet increased energetic and biosynthetic demands. We showed that exogenous nutrient availability regulated the differentiation of naïve CD4(+) T cells into distinct subsets. Activation of naïve CD4(+) T cells under conditions of glutamine deprivation resulted in their differentiation into Foxp3(+) (forkhead box P3-positive) regulatory T (Treg) cells, which had suppressor function in vivo. Moreover, glutamine-deprived CD4(+) T cells that were activated in the presence of cytokines that normally induce the generation of T helper 1 (TH1) cells instead differentiated into Foxp3(+) Treg cells. We found that α-ketoglutarate (αKG), the glutamine-derived metabolite that enters into the mitochondrial citric acid cycle, acted as a metabolic regulator of CD4(+) T cell differentiation. Activation of glutamine-deprived naïve CD4(+) T cells in the presence of a cell-permeable αKG analog increased the expression of the gene encoding the TH1 cell-associated transcription factor Tbet and resulted in their differentiation into TH1 cells, concomitant with stimulation of mammalian target of rapamycin complex 1 (mTORC1) signaling. Together, these data suggest that a decrease in the intracellular amount of αKG, caused by the limited availability of extracellular glutamine, shifts the balance between the generation of TH1 and Treg cells toward that of a Treg phenotype.</div>
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<Month>09</Month>
<Day>30</Day>
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<DateCompleted><Year>2016</Year>
<Month>07</Month>
<Day>12</Day>
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<DateRevised><Year>2017</Year>
<Month>11</Month>
<Day>16</Day>
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<JournalIssue CitedMedium="Internet"><Volume>8</Volume>
<Issue>396</Issue>
<PubDate><Year>2015</Year>
<Month>Sep</Month>
<Day>29</Day>
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<Title>Science signaling</Title>
<ISOAbbreviation>Sci Signal</ISOAbbreviation>
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<ArticleTitle>Glutamine-dependent α-ketoglutarate production regulates the balance between T helper 1 cell and regulatory T cell generation.</ArticleTitle>
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<Abstract><AbstractText>T cell activation requires that the cell meet increased energetic and biosynthetic demands. We showed that exogenous nutrient availability regulated the differentiation of naïve CD4(+) T cells into distinct subsets. Activation of naïve CD4(+) T cells under conditions of glutamine deprivation resulted in their differentiation into Foxp3(+) (forkhead box P3-positive) regulatory T (Treg) cells, which had suppressor function in vivo. Moreover, glutamine-deprived CD4(+) T cells that were activated in the presence of cytokines that normally induce the generation of T helper 1 (TH1) cells instead differentiated into Foxp3(+) Treg cells. We found that α-ketoglutarate (αKG), the glutamine-derived metabolite that enters into the mitochondrial citric acid cycle, acted as a metabolic regulator of CD4(+) T cell differentiation. Activation of glutamine-deprived naïve CD4(+) T cells in the presence of a cell-permeable αKG analog increased the expression of the gene encoding the TH1 cell-associated transcription factor Tbet and resulted in their differentiation into TH1 cells, concomitant with stimulation of mammalian target of rapamycin complex 1 (mTORC1) signaling. Together, these data suggest that a decrease in the intracellular amount of αKG, caused by the limited availability of extracellular glutamine, shifts the balance between the generation of TH1 and Treg cells toward that of a Treg phenotype.</AbstractText>
<CopyrightInformation>Copyright © 2015, American Association for the Advancement of Science.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Klysz</LastName>
<ForeName>Dorota</ForeName>
<Initials>D</Initials>
<AffiliationInfo><Affiliation>Institut de Génétique Moléculaire de Montpellier, CNRS, UMR 5535, Université de Montpellier, F-34293 Montpellier, France.</Affiliation>
</AffiliationInfo>
</Author>
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<Initials>X</Initials>
<AffiliationInfo><Affiliation>Experimental Immunology Branch, National Cancer Institute, Bethesda, MD 20892, USA.</Affiliation>
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<ForeName>Philippe A</ForeName>
<Initials>PA</Initials>
<AffiliationInfo><Affiliation>Institut de Génétique Moléculaire de Montpellier, CNRS, UMR 5535, Université de Montpellier, F-34293 Montpellier, France. Department of Systems Immunology, Braunschweig Integrated Centre of Systems Biology, 38124 Braunschweig, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Craveiro</LastName>
<ForeName>Marco</ForeName>
<Initials>M</Initials>
<AffiliationInfo><Affiliation>Institut de Génétique Moléculaire de Montpellier, CNRS, UMR 5535, Université de Montpellier, F-34293 Montpellier, France.</Affiliation>
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</AffiliationInfo>
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</Author>
<Author ValidYN="Y"><LastName>Floess</LastName>
<ForeName>Stefan</ForeName>
<Initials>S</Initials>
<AffiliationInfo><Affiliation>Department of Experimental Immunology, Helmholtz Centre for Infection Research, 38124 Braunschweig, Germany.</Affiliation>
</AffiliationInfo>
</Author>
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<ForeName>Vanessa</ForeName>
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</AffiliationInfo>
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<ForeName>Maria I</ForeName>
<Initials>MI</Initials>
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</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Yong</LastName>
<ForeName>Carmen</ForeName>
<Initials>C</Initials>
<AffiliationInfo><Affiliation>Institut de Génétique Moléculaire de Montpellier, CNRS, UMR 5535, Université de Montpellier, F-34293 Montpellier, France. Cancer Immunology Research Program, Sir Peter MacCallum Department of Oncology, University of Melbourne, Parkville, Victoria 3010, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Surh</LastName>
<ForeName>Natalie</ForeName>
<Initials>N</Initials>
<AffiliationInfo><Affiliation>Institut de Génétique Moléculaire de Montpellier, CNRS, UMR 5535, Université de Montpellier, F-34293 Montpellier, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Marie</LastName>
<ForeName>Julien C</ForeName>
<Initials>JC</Initials>
<AffiliationInfo><Affiliation>Cancer Research Center of Lyon, INSERM U1052, CNRS 5286, Université Lyon 1, 69373 Lyon cedex 03, France. DKFZ German Cancer Research Center, 69121 Heidelberg, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Huehn</LastName>
<ForeName>Jochen</ForeName>
<Initials>J</Initials>
<AffiliationInfo><Affiliation>Department of Experimental Immunology, Helmholtz Centre for Infection Research, 38124 Braunschweig, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Zimmermann</LastName>
<ForeName>Valérie</ForeName>
<Initials>V</Initials>
<AffiliationInfo><Affiliation>Institut de Génétique Moléculaire de Montpellier, CNRS, UMR 5535, Université de Montpellier, F-34293 Montpellier, France.</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y"><LastName>Kinet</LastName>
<ForeName>Sandrina</ForeName>
<Initials>S</Initials>
<AffiliationInfo><Affiliation>Institut de Génétique Moléculaire de Montpellier, CNRS, UMR 5535, Université de Montpellier, F-34293 Montpellier, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Dardalhon</LastName>
<ForeName>Valérie</ForeName>
<Initials>V</Initials>
<AffiliationInfo><Affiliation>Institut de Génétique Moléculaire de Montpellier, CNRS, UMR 5535, Université de Montpellier, F-34293 Montpellier, France. valerie.dardalhon@igmm.cnrs.fr taylor@igmm.cnrs.fr.</Affiliation>
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<Author ValidYN="Y"><LastName>Taylor</LastName>
<ForeName>Naomi</ForeName>
<Initials>N</Initials>
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Glutamine-dependent α-ketoglutarate production regulates the balance between T helper 1 cell and regulatory T cell generation.

Glutamine-dependent α-ketoglutarate production regulates the balance between T helper 1 cell and regulatory T cell generation.

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