The transcription factor IRF4 is essential for TCR affinity–mediated metabolic programming and clonal expansion of T cells
Clonal expansion of cytotoxic T lymphocytes entails profound energetic demands. Kallies and colleagues show that the transcription factor IRF4 is critical for the metabolic reprogramming, survival and effector function of these cells during clonal expansion. During immune responses, T cells are subj...
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| Published in | Nature immunology Vol. 14; no. 11; pp. 1155 - 1165 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.11.2013
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Clonal expansion of cytotoxic T lymphocytes entails profound energetic demands. Kallies and colleagues show that the transcription factor IRF4 is critical for the metabolic reprogramming, survival and effector function of these cells during clonal expansion.
During immune responses, T cells are subject to clonal competition, which leads to the predominant expansion of high-affinity clones; however, there is little understanding of how this process is controlled. We found here that the transcription factor IRF4 was induced in a manner dependent on affinity for the T cell antigen receptor (TCR) and acted as a dose-dependent regulator of the metabolic function of activated T cells. IRF4 regulated the expression of key molecules required for the aerobic glycolysis of effector T cells and was essential for the clonal expansion and maintenance of effector function of antigen-specific CD8
+
T cells. Thus, IRF4 is an indispensable molecular 'rheostat' that 'translates' TCR affinity into the appropriate transcriptional programs that link metabolic function with the clonal selection and effector differentiation of T cells. |
|---|---|
| AbstractList | During immune responses, T cells are subject to clonal competition, which leads to the predominant expansion of high-affinity clones; however, there is little understanding of how this process is controlled. We found here that the transcription factor IRF4 was induced in a manner dependent on affinity for the T cell antigen receptor (TCR) and acted as a dose-dependent regulator of the metabolic function of activated T cells. IRF4 regulated the expression of key molecules required for the aerobic glycolysis of effector T cells and was essential for the clonal expansion and maintenance of effector function of antigen-specific CD8(+) T cells. Thus, IRF4 is an indispensable molecular 'rheostat' that 'translates' TCR affinity into the appropriate transcriptional programs that link metabolic function with the clonal selection and effector differentiation of T cells.During immune responses, T cells are subject to clonal competition, which leads to the predominant expansion of high-affinity clones; however, there is little understanding of how this process is controlled. We found here that the transcription factor IRF4 was induced in a manner dependent on affinity for the T cell antigen receptor (TCR) and acted as a dose-dependent regulator of the metabolic function of activated T cells. IRF4 regulated the expression of key molecules required for the aerobic glycolysis of effector T cells and was essential for the clonal expansion and maintenance of effector function of antigen-specific CD8(+) T cells. Thus, IRF4 is an indispensable molecular 'rheostat' that 'translates' TCR affinity into the appropriate transcriptional programs that link metabolic function with the clonal selection and effector differentiation of T cells. Clonal expansion of cytotoxic T lymphocytes entails profound energetic demands. Kallies and colleagues show that the transcription factor IRF4 is critical for the metabolic reprogramming, survival and effector function of these cells during clonal expansion. During immune responses, T cells are subject to clonal competition, which leads to the predominant expansion of high-affinity clones; however, there is little understanding of how this process is controlled. We found here that the transcription factor IRF4 was induced in a manner dependent on affinity for the T cell antigen receptor (TCR) and acted as a dose-dependent regulator of the metabolic function of activated T cells. IRF4 regulated the expression of key molecules required for the aerobic glycolysis of effector T cells and was essential for the clonal expansion and maintenance of effector function of antigen-specific CD8 + T cells. Thus, IRF4 is an indispensable molecular 'rheostat' that 'translates' TCR affinity into the appropriate transcriptional programs that link metabolic function with the clonal selection and effector differentiation of T cells. During immune responses, T cells are subject to clonal competition, which leads to the predominant expansion of high-affinity clones; however, there is little understanding of how this process is controlled. We found here that the transcription factor IRF4 was induced in a manner dependent on affinity for the T cell antigen receptor (TCR) and acted as a dose-dependent regulator of the metabolic function of activated T cells. IRF4 regulated the expression of key molecules required for the aerobic glycolysis of effector T cells and was essential for the clonal expansion and maintenance of effector function of antigen-specific CD8 super(+) T cells. Thus, IRF4 is an indispensable molecular 'rheostat' that 'translates' TCR affinity into the appropriate transcriptional programs that link metabolic function with the clonal selection and effector differentiation of T cells. During immune responses, T cells are subject to clonal competition, which leads to the predominant expansion of high-affinity clones; however, there is little understanding of how this process is controlled. We found here that the transcription factor IRF4 was induced in a manner dependent on affinity for the T cell antigen receptor (TCR) and acted as a dose-dependent regulator of the metabolic function of activated T cells. IRF4 regulated the expression of key molecules required for the aerobic glycolysis of effector T cells and was essential for the clonal expansion and maintenance of effector function of antigen-specific CD8(+) T cells. Thus, IRF4 is an indispensable molecular 'rheostat' that 'translates' TCR affinity into the appropriate transcriptional programs that link metabolic function with the clonal selection and effector differentiation of T cells. During immune responses, T cells are subject to clonal competition, which leads to the predominant expansion of high- affinity clones; however, there is little understanding of how this process is controlled. We found here that the transcription factor IRF4 was induced in a manner dependent on affinity for the T cell antigen receptor (TCR) and acted as a dose-dependent regulator of the metabolic function of activated T cells. IRF4 regulated the expression of key molecules required for the aerobic glycolysis of effector T cells and was essential for the clonal expansion and maintenance of effector function of antigen-specific [CD8.sup.+] T cells. Thus, IRF4 is an indispensable molecular 'rheostat' that 'translates' TCR affinity into the appropriate transcriptional programs that link metabolic function with the clonal selection and effector differentiation of T cells. |
| Audience | Academic |
| Author | Preston, Simon Shi, Wei Smyth, Gordon K Nutt, Stephen L Belz, Gabrielle T Kallies, Axel Man, Kevin Miasari, Maria Pellegrini, Marc Febbraio, Mark A Xin, Annie Henstridge, Darren C |
| Author_xml | – sequence: 1 givenname: Kevin surname: Man fullname: Man, Kevin organization: The Walter and Eliza Hall Institute of Medical Research, The Department of Medical Biology, University of Melbourne – sequence: 2 givenname: Maria surname: Miasari fullname: Miasari, Maria organization: The Walter and Eliza Hall Institute of Medical Research, The Department of Medical Biology, University of Melbourne – sequence: 3 givenname: Wei surname: Shi fullname: Shi, Wei organization: The Walter and Eliza Hall Institute of Medical Research, The Department of Computing and Information Systems, University of Melbourne – sequence: 4 givenname: Annie surname: Xin fullname: Xin, Annie organization: The Walter and Eliza Hall Institute of Medical Research, The Department of Medical Biology, University of Melbourne – sequence: 5 givenname: Darren C surname: Henstridge fullname: Henstridge, Darren C organization: Cellular and Molecular Metabolism Laboratory, Baker IDI Heart and Diabetes Institute – sequence: 6 givenname: Simon surname: Preston fullname: Preston, Simon organization: The Walter and Eliza Hall Institute of Medical Research, The Department of Medical Biology, University of Melbourne – sequence: 7 givenname: Marc surname: Pellegrini fullname: Pellegrini, Marc organization: The Walter and Eliza Hall Institute of Medical Research, The Department of Medical Biology, University of Melbourne – sequence: 8 givenname: Gabrielle T surname: Belz fullname: Belz, Gabrielle T organization: The Walter and Eliza Hall Institute of Medical Research, The Department of Medical Biology, University of Melbourne – sequence: 9 givenname: Gordon K surname: Smyth fullname: Smyth, Gordon K organization: The Walter and Eliza Hall Institute of Medical Research, The Department of Mathematics and Statistics, University of Melbourne – sequence: 10 givenname: Mark A surname: Febbraio fullname: Febbraio, Mark A organization: Cellular and Molecular Metabolism Laboratory, Baker IDI Heart and Diabetes Institute – sequence: 11 givenname: Stephen L surname: Nutt fullname: Nutt, Stephen L organization: The Walter and Eliza Hall Institute of Medical Research, The Department of Medical Biology, University of Melbourne – sequence: 12 givenname: Axel surname: Kallies fullname: Kallies, Axel email: kallies@wehi.edu.au organization: The Walter and Eliza Hall Institute of Medical Research, The Department of Medical Biology, University of Melbourne |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24056747$$D View this record in MEDLINE/PubMed |
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| Snippet | Clonal expansion of cytotoxic T lymphocytes entails profound energetic demands. Kallies and colleagues show that the transcription factor IRF4 is critical for... During immune responses, T cells are subject to clonal competition, which leads to the predominant expansion of high-affinity clones; however, there is little... During immune responses, T cells are subject to clonal competition, which leads to the predominant expansion of high- affinity clones; however, there is little... |
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| SubjectTerms | 631/250/248 631/250/2502/248 Animals Biomedicine CD4-Positive T-Lymphocytes - immunology CD4-Positive T-Lymphocytes - metabolism CD4-Positive T-Lymphocytes - virology CD8-Positive T-Lymphocytes - immunology CD8-Positive T-Lymphocytes - metabolism CD8-Positive T-Lymphocytes - virology Cell Differentiation Cell Proliferation Clone Cells Gene Expression Regulation Genetic aspects Glucose metabolism Humans Immunology Infectious Diseases Influenza A Virus, H3N2 Subtype - immunology Interferon Regulatory Factors - genetics Interferon Regulatory Factors - immunology Interferon Regulatory Factors - metabolism Mice Mice, Transgenic Orthomyxoviridae Infections - immunology Orthomyxoviridae Infections - metabolism Orthomyxoviridae Infections - virology Physiological aspects Receptors, Antigen, T-Cell - genetics Receptors, Antigen, T-Cell - immunology Receptors, Antigen, T-Cell - metabolism T cells T-Lymphocyte Subsets - immunology T-Lymphocyte Subsets - metabolism T-Lymphocyte Subsets - virology Transcription factors Transcription, Genetic |
| Title | The transcription factor IRF4 is essential for TCR affinity–mediated metabolic programming and clonal expansion of T cells |
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