The transcription factor BATF operates as an essential differentiation checkpoint in early effector CD8+ T cells

The transcription factor BATF is required for differentiation of certain helper T cell subsets. Haining and colleagues show that BATF crucially regulates CD8 + effector cells by coordinating a transcription factor network. The transcription factor BATF is required for the differentiation of interleu...

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Veröffentlicht in:	Nature immunology Jg. 15; H. 4; S. 373 - 383
Hauptverfasser:	Kurachi, Makoto, Barnitz, R Anthony, Yosef, Nir, Odorizzi, Pamela M, DiIorio, Michael A, Lemieux, Madeleine E, Yates, Kathleen, Godec, Jernej, Klatt, Martin G, Regev, Aviv, Wherry, E John, Haining, W Nicholas
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	New York Nature Publishing Group US 01.04.2014 Nature Publishing Group
Schlagworte:	13 13/31 38 38/15 38/23 38/77 42/44 631/250/2152/1566/1571 631/250/2152/1566/1618 64/60 Animals Antigens Basic-Leucine Zipper Transcription Factors - genetics Basic-Leucine Zipper Transcription Factors - immunology Basic-Leucine Zipper Transcription Factors - metabolism Biomedicine CD8 antigen CD8-Positive T-Lymphocytes - immunology Cell differentiation Cell Differentiation - genetics Cell Growth Processes - genetics Cells, Cultured Cytokine receptors Down-Regulation Effector cells Granzyme B Granzymes - genetics Granzymes - metabolism Helper cells Immunology Infectious Diseases Inflammation Interferon regulatory factor 4 Interferon Regulatory Factors - metabolism Interferon-gamma - genetics Interferon-gamma - metabolism Interleukin 17 Lymphocyte Activation - genetics Lymphocytes Lymphocytes T Male Mice Mice, Inbred C57BL Mice, Knockout Population growth Positive Regulatory Domain I-Binding Factor 1 Proto-Oncogene Proteins c-jun - metabolism T cell receptors T-Box Domain Proteins - genetics T-Box Domain Proteins - metabolism Th17 Cells - immunology Transcription factors Transcription Factors - genetics Transcription Factors - metabolism Transcriptional Activation - genetics γ-Interferon
ISSN:	1529-2908, 1529-2916, 1529-2916
Online-Zugang:	Volltext
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Abstract	The transcription factor BATF is required for differentiation of certain helper T cell subsets. Haining and colleagues show that BATF crucially regulates CD8 + effector cells by coordinating a transcription factor network. The transcription factor BATF is required for the differentiation of interleukin 17 (IL-17)-producing helper T cells (T H 17 cells) and follicular helper T cells (T FH cells). Here we identified a fundamental role for BATF in regulating the differentiation of effector of CD8 + T cells. BATF-deficient CD8 + T cells showed profound defects in effector population expansion and underwent proliferative and metabolic catastrophe early after encountering antigen. BATF, together with the transcription factors IRF4 and Jun proteins, bound to and promoted early expression of genes encoding lineage-specific transcription-factors (T-bet and Blimp-1) and cytokine receptors while paradoxically repressing genes encoding effector molecules (IFN-γ and granzyme B). Thus, BATF amplifies T cell antigen receptor (TCR)-dependent expression of transcription factors and augments the propagation of inflammatory signals but restrains the expression of genes encoding effector molecules. This checkpoint prevents irreversible commitment to an effector fate until a critical threshold of downstream transcriptional activity has been achieved.
AbstractList	The transcription factor BATF is required for the differentiation of interleukin 17 (IL-17)-producing helper T cells (TH17 cells) and follicular helper T cells (TFH cells). Here we identified a fundamental role for BATF in regulating the differentiation of effector of CD8(+) T cells. BATF-deficient CD8(+) T cells showed profound defects in effector population expansion and underwent proliferative and metabolic catastrophe early after encountering antigen. BATF, together with the transcription factors IRF4 and Jun proteins, bound to and promoted early expression of genes encoding lineage-specific transcription-factors (T-bet and Blimp-1) and cytokine receptors while paradoxically repressing genes encoding effector molecules (IFN-γ and granzyme B). Thus, BATF amplifies T cell antigen receptor (TCR)-dependent expression of transcription factors and augments the propagation of inflammatory signals but restrains the expression of genes encoding effector molecules. This checkpoint prevents irreversible commitment to an effector fate until a critical threshold of downstream transcriptional activity has been achieved. The transcription factor BATF is required for interleukin 17 (IL-17)-producing helper T cell (TH17) and follicular helper T cell (TFH) differentiation. Here, we show that BATF also has a fundamental role in regulating effector CD8+ T cell differentiation. BATF-deficient CD8+ T cells show profound defects in effector expansion and undergo proliferative and metabolic catastrophe early after antigen encounter. BATF, together with IRF4 and Jun proteins, binds to and promotes early expression of genes encoding lineage-specific transcription-factors (T-bet and Blimp-1) and cytokine receptors, while paradoxically repressing genes encoding effector molecules (IFN-γ and granzyme B). Thus, BATF amplifies TCR-dependent transcription factor expression and augments inflammatory signal propagation but restrains effector gene expression. This checkpoint prevents irreversible commitment to an effector fate until a critical threshold of downstream transcriptional activity has been achieved. The transcription factor BATF is required for differentiation of certain helper T cell subsets. Haining and colleagues show that BATF crucially regulates CD8+ effector cells by coordinating a transcription factor network.The transcription factor BATF is required for the differentiation of interleukin 17 (IL-17)-producing helper T cells (TH17 cells) and follicular helper T cells (TFH cells). Here we identified a fundamental role for BATF in regulating the differentiation of effector of CD8+ T cells. BATF-deficient CD8+ T cells showed profound defects in effector population expansion and underwent proliferative and metabolic catastrophe early after encountering antigen. BATF, together with the transcription factors IRF4 and Jun proteins, bound to and promoted early expression of genes encoding lineage-specific transcription-factors (T-bet and Blimp-1) and cytokine receptors while paradoxically repressing genes encoding effector molecules (IFN-γ and granzyme B). Thus, BATF amplifies T cell antigen receptor (TCR)-dependent expression of transcription factors and augments the propagation of inflammatory signals but restrains the expression of genes encoding effector molecules. This checkpoint prevents irreversible commitment to an effector fate until a critical threshold of downstream transcriptional activity has been achieved. The transcription factor BATF is required for the differentiation of interleukin 17 (IL-17)-producing helper T cells (TH17 cells) and follicular helper T cells (TFH cells). Here we identified a fundamental role for BATF in regulating the differentiation of effector of CD8(+) T cells. BATF-deficient CD8(+) T cells showed profound defects in effector population expansion and underwent proliferative and metabolic catastrophe early after encountering antigen. BATF, together with the transcription factors IRF4 and Jun proteins, bound to and promoted early expression of genes encoding lineage-specific transcription-factors (T-bet and Blimp-1) and cytokine receptors while paradoxically repressing genes encoding effector molecules (IFN-γ and granzyme B). Thus, BATF amplifies T cell antigen receptor (TCR)-dependent expression of transcription factors and augments the propagation of inflammatory signals but restrains the expression of genes encoding effector molecules. This checkpoint prevents irreversible commitment to an effector fate until a critical threshold of downstream transcriptional activity has been achieved.The transcription factor BATF is required for the differentiation of interleukin 17 (IL-17)-producing helper T cells (TH17 cells) and follicular helper T cells (TFH cells). Here we identified a fundamental role for BATF in regulating the differentiation of effector of CD8(+) T cells. BATF-deficient CD8(+) T cells showed profound defects in effector population expansion and underwent proliferative and metabolic catastrophe early after encountering antigen. BATF, together with the transcription factors IRF4 and Jun proteins, bound to and promoted early expression of genes encoding lineage-specific transcription-factors (T-bet and Blimp-1) and cytokine receptors while paradoxically repressing genes encoding effector molecules (IFN-γ and granzyme B). Thus, BATF amplifies T cell antigen receptor (TCR)-dependent expression of transcription factors and augments the propagation of inflammatory signals but restrains the expression of genes encoding effector molecules. This checkpoint prevents irreversible commitment to an effector fate until a critical threshold of downstream transcriptional activity has been achieved. The transcription factor BATF is required for differentiation of certain helper T cell subsets. Haining and colleagues show that BATF crucially regulates CD8 + effector cells by coordinating a transcription factor network. The transcription factor BATF is required for the differentiation of interleukin 17 (IL-17)-producing helper T cells (T H 17 cells) and follicular helper T cells (T FH cells). Here we identified a fundamental role for BATF in regulating the differentiation of effector of CD8 + T cells. BATF-deficient CD8 + T cells showed profound defects in effector population expansion and underwent proliferative and metabolic catastrophe early after encountering antigen. BATF, together with the transcription factors IRF4 and Jun proteins, bound to and promoted early expression of genes encoding lineage-specific transcription-factors (T-bet and Blimp-1) and cytokine receptors while paradoxically repressing genes encoding effector molecules (IFN-γ and granzyme B). Thus, BATF amplifies T cell antigen receptor (TCR)-dependent expression of transcription factors and augments the propagation of inflammatory signals but restrains the expression of genes encoding effector molecules. This checkpoint prevents irreversible commitment to an effector fate until a critical threshold of downstream transcriptional activity has been achieved.
Author	Godec, Jernej Barnitz, R Anthony DiIorio, Michael A Lemieux, Madeleine E Haining, W Nicholas Yates, Kathleen Klatt, Martin G Regev, Aviv Odorizzi, Pamela M Wherry, E John Kurachi, Makoto Yosef, Nir
AuthorAffiliation	6 Bioinfo, Plantagenet, Ontario, Canada 4 Division of Hematology/Oncology, Children’s Hospital, Harvard Medical School, Boston, MA, USA 2 Institute for Immunology, University of Pennsylvania Perelman School Medicine, Philadelphia, PA, USA 3 Department of Pediatric Oncology, Dana-Farber Cancer Institute Children’s Hospital, Harvard Medical School, Boston, MA, USA 7 Howard Hughes Medical Institute, Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA 1 Department of Microbiology University of Pennsylvania Perelman School Medicine, Philadelphia, PA, USA 5 Broad Institute of MIT and Harvard, 7 Cambridge Center, Cambridge, MA, USA
AuthorAffiliation_xml	– name: 3 Department of Pediatric Oncology, Dana-Farber Cancer Institute Children’s Hospital, Harvard Medical School, Boston, MA, USA – name: 7 Howard Hughes Medical Institute, Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA – name: 6 Bioinfo, Plantagenet, Ontario, Canada – name: 1 Department of Microbiology University of Pennsylvania Perelman School Medicine, Philadelphia, PA, USA – name: 4 Division of Hematology/Oncology, Children’s Hospital, Harvard Medical School, Boston, MA, USA – name: 2 Institute for Immunology, University of Pennsylvania Perelman School Medicine, Philadelphia, PA, USA – name: 5 Broad Institute of MIT and Harvard, 7 Cambridge Center, Cambridge, MA, USA
Author_xml	– sequence: 1 givenname: Makoto surname: Kurachi fullname: Kurachi, Makoto organization: Department of Microbiology, University of Pennsylvania Perelman School of Medicine, Institute for Immunology, University of Pennsylvania Perelman School of Medicine – sequence: 2 givenname: R Anthony surname: Barnitz fullname: Barnitz, R Anthony organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Harvard Medical School – sequence: 3 givenname: Nir surname: Yosef fullname: Yosef, Nir organization: Broad Institute of MIT and Harvard – sequence: 4 givenname: Pamela M surname: Odorizzi fullname: Odorizzi, Pamela M organization: Department of Microbiology, University of Pennsylvania Perelman School of Medicine, Institute for Immunology, University of Pennsylvania Perelman School of Medicine – sequence: 5 givenname: Michael A surname: DiIorio fullname: DiIorio, Michael A organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Harvard Medical School – sequence: 6 givenname: Madeleine E surname: Lemieux fullname: Lemieux, Madeleine E organization: Bioinfo – sequence: 7 givenname: Kathleen surname: Yates fullname: Yates, Kathleen organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Harvard Medical School – sequence: 8 givenname: Jernej surname: Godec fullname: Godec, Jernej organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Harvard Medical School – sequence: 9 givenname: Martin G surname: Klatt fullname: Klatt, Martin G organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Harvard Medical School – sequence: 10 givenname: Aviv surname: Regev fullname: Regev, Aviv organization: Bioinfo, Department of Biology, Howard Hughes Medical Institute, Massachusetts Institute of Technology – sequence: 11 givenname: E John surname: Wherry fullname: Wherry, E John email: wherry@mail.med.upenn.edu organization: Department of Microbiology, University of Pennsylvania Perelman School of Medicine, Institute for Immunology, University of Pennsylvania Perelman School of Medicine – sequence: 12 givenname: W Nicholas surname: Haining fullname: Haining, W Nicholas email: nicholas_haining@dfci.harvard.edu organization: Department of Pediatric Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Broad Institute of MIT and Harvard, Division of Hematology/Oncology, Children's Hospital, Harvard Medical School
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/24584090$$D View this record in MEDLINE/PubMed
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 These authors contributed equally. M.K. and P.O. performed the experiments in the animal models; R.A.B, M.A.D., K.Y., J. G. and M.G.K. performed the gene expression and ChIP experiments; N.Y. and M.E.L. designed and performed analytic experiments; A.R., W.N.H. and E.J.W. designed the analytic experiments; W.N.H and E.J.W conceived the project; M.K., R.A.B., E.J.W. and W.N.H. wrote the paper. Author contributions
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Snippet	The transcription factor BATF is required for differentiation of certain helper T cell subsets. Haining and colleagues show that BATF crucially regulates CD8 +... The transcription factor BATF is required for the differentiation of interleukin 17 (IL-17)-producing helper T cells (TH17 cells) and follicular helper T cells... The transcription factor BATF is required for differentiation of certain helper T cell subsets. Haining and colleagues show that BATF crucially regulates CD8+... The transcription factor BATF is required for interleukin 17 (IL-17)-producing helper T cell (TH17) and follicular helper T cell (TFH) differentiation. Here,...
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SubjectTerms	13 13/31 38 38/15 38/23 38/77 42/44 631/250/2152/1566/1571 631/250/2152/1566/1618 64/60 Animals Antigens Basic-Leucine Zipper Transcription Factors - genetics Basic-Leucine Zipper Transcription Factors - immunology Basic-Leucine Zipper Transcription Factors - metabolism Biomedicine CD8 antigen CD8-Positive T-Lymphocytes - immunology Cell differentiation Cell Differentiation - genetics Cell Growth Processes - genetics Cells, Cultured Cytokine receptors Down-Regulation Effector cells Granzyme B Granzymes - genetics Granzymes - metabolism Helper cells Immunology Infectious Diseases Inflammation Interferon regulatory factor 4 Interferon Regulatory Factors - metabolism Interferon-gamma - genetics Interferon-gamma - metabolism Interleukin 17 Lymphocyte Activation - genetics Lymphocytes Lymphocytes T Male Mice Mice, Inbred C57BL Mice, Knockout Population growth Positive Regulatory Domain I-Binding Factor 1 Proto-Oncogene Proteins c-jun - metabolism T cell receptors T-Box Domain Proteins - genetics T-Box Domain Proteins - metabolism Th17 Cells - immunology Transcription factors Transcription Factors - genetics Transcription Factors - metabolism Transcriptional Activation - genetics γ-Interferon
Title	The transcription factor BATF operates as an essential differentiation checkpoint in early effector CD8+ T cells
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