Hierarchical regulation of the resting and activated T cell epigenome by major transcription factor families

T cell activation, a key early event in the adaptive immune response, is subject to elaborate transcriptional control. In the present study, we examined how the activities of eight major transcription factor (TF) families are integrated to shape the epigenome of naive and activated CD4 and CD8 T cel...

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Published inNature immunology Vol. 23; no. 1; pp. 122 - 134
Main Authors Zhong, Yi, Walker, Sarah K., Pritykin, Yuri, Leslie, Christina S., Rudensky, Alexander Y., van der Veeken, Joris
Format Journal Article
LanguageEnglish
Published New York Nature Publishing Group US 01.01.2022
Nature Publishing Group
Subjects
631/250/2502/2170
631/250/2502/248
Adaptive immunity
Adaptive Immunity - immunology
Animals
Biomedical and Life Sciences
Biomedicine
CD4 antigen
CD4-Positive T-Lymphocytes - immunology
CD8 antigen
CD8-Positive T-Lymphocytes - immunology
Cell activation
Chromatin
Chromatin - immunology
Divergence
Epigenesis, Genetic - immunology
Epigenetics
Epigenome - immunology
ETS protein
Gene expression
Gene Expression Regulation - immunology
Gene regulation
Immune response
Immunology
Infectious Diseases
LEF protein
Lymphocyte Activation - immunology
Lymphocytes
Lymphocytes T
Male
Mice
Resource
Transcription factors
Transcription Factors - immunology
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Abstract T cell activation, a key early event in the adaptive immune response, is subject to elaborate transcriptional control. In the present study, we examined how the activities of eight major transcription factor (TF) families are integrated to shape the epigenome of naive and activated CD4 and CD8 T cells. By leveraging extensive polymorphisms in evolutionarily divergent mice, we identified the ‘heavy lifters’ positively influencing chromatin accessibility. Members of Ets, Runx and TCF/Lef TF families occupied the vast majority of accessible chromatin regions, acting as ‘housekeepers’, ‘universal amplifiers’ and ‘placeholders’, respectively, at sites that maintained or gained accessibility upon T cell activation. In addition, a small subset of strongly induced immune response genes displayed a noncanonical TF recruitment pattern. Our study provides a key resource and foundation for the understanding of transcriptional and epigenetic regulation in T cells and offers a new perspective on the hierarchical interactions between critical TFs. Zhong et al. utilize B6/Cast F1 hybrid mice to examine transcriptional regulation of T cell gene expression upon activation induced by viral challenge. They describe gene accessibility changes that lead to differential gene expression and report a hierarchy of transcription factor families that mediate the chromatin dynamics.
AbstractList T cell activation, a key early event in the adaptive immune response, is subject to elaborate transcriptional control. In the present study, we examined how the activities of eight major transcription factor (TF) families are integrated to shape the epigenome of naive and activated CD4 and CD8 T cells. By leveraging extensive polymorphisms in evolutionarily divergent mice, we identified the 'heavy lifters' positively influencing chromatin accessibility. Members of Ets, Runx and TCF/Lef TF families occupied the vast majority of accessible chromatin regions, acting as 'housekeepers', 'universal amplifiers' and 'placeholders', respectively, at sites that maintained or gained accessibility upon T cell activation. In addition, a small subset of strongly induced immune response genes displayed a noncanonical TF recruitment pattern. Our study provides a key resource and foundation for the understanding of transcriptional and epigenetic regulation in T cells and offers a new perspective on the hierarchical interactions between critical TFs.
T cell activation, a key early event in the adaptive immune response, is subject to elaborate transcriptional control. Here, we examined how the activities of eight major transcription factor (TF) families are integrated to shape the epigenome of naïve and activated CD4 and CD8 T cells. By leveraging extensive polymorphisms in evolutionarily divergent mice, we identified the “heavy lifters” positively influencing chromatin accessibility. Members of Ets, Runx, and TCF/Lef TF families occupied the vast majority of accessible chromatin regions, acting as “housekeepers”, “universal amplifiers”, and “placeholders”, respectively, at sites that maintained or gained accessibility upon T cell activation. Additionally, a small subset of strongly induced immune response genes displayed a non-canonical TF recruitment pattern. Our study provides a key resource and foundation for the understanding of transcriptional and epigenetic regulation in T cells and offers a new perspective on the hierarchical interactions between critical TFs.
T cell activation, a key early event in the adaptive immune response, is subject to elaborate transcriptional control. In the present study, we examined how the activities of eight major transcription factor (TF) families are integrated to shape the epigenome of naive and activated CD4 and CD8 T cells. By leveraging extensive polymorphisms in evolutionarily divergent mice, we identified the ‘heavy lifters’ positively influencing chromatin accessibility. Members of Ets, Runx and TCF/Lef TF families occupied the vast majority of accessible chromatin regions, acting as ‘housekeepers’, ‘universal amplifiers’ and ‘placeholders’, respectively, at sites that maintained or gained accessibility upon T cell activation. In addition, a small subset of strongly induced immune response genes displayed a noncanonical TF recruitment pattern. Our study provides a key resource and foundation for the understanding of transcriptional and epigenetic regulation in T cells and offers a new perspective on the hierarchical interactions between critical TFs. Zhong et al. utilize B6/Cast F1 hybrid mice to examine transcriptional regulation of T cell gene expression upon activation induced by viral challenge. They describe gene accessibility changes that lead to differential gene expression and report a hierarchy of transcription factor families that mediate the chromatin dynamics.
T cell activation, a key early event in the adaptive immune response, is subject to elaborate transcriptional control. In the present study, we examined how the activities of eight major transcription factor (TF) families are integrated to shape the epigenome of naive and activated CD4 and CD8 T cells. By leveraging extensive polymorphisms in evolutionarily divergent mice, we identified the ‘heavy lifters’ positively influencing chromatin accessibility. Members of Ets, Runx and TCF/Lef TF families occupied the vast majority of accessible chromatin regions, acting as ‘housekeepers’, ‘universal amplifiers’ and ‘placeholders’, respectively, at sites that maintained or gained accessibility upon T cell activation. In addition, a small subset of strongly induced immune response genes displayed a noncanonical TF recruitment pattern. Our study provides a key resource and foundation for the understanding of transcriptional and epigenetic regulation in T cells and offers a new perspective on the hierarchical interactions between critical TFs.Zhong et al. utilize B6/Cast F1 hybrid mice to examine transcriptional regulation of T cell gene expression upon activation induced by viral challenge. They describe gene accessibility changes that lead to differential gene expression and report a hierarchy of transcription factor families that mediate the chromatin dynamics.
T cell activation, a key early event in the adaptive immune response, is subject to elaborate transcriptional control. In the present study, we examined how the activities of eight major transcription factor (TF) families are integrated to shape the epigenome of naive and activated CD4 and CD8 T cells. By leveraging extensive polymorphisms in evolutionarily divergent mice, we identified the 'heavy lifters' positively influencing chromatin accessibility. Members of Ets, Runx and TCF/Lef TF families occupied the vast majority of accessible chromatin regions, acting as 'housekeepers', 'universal amplifiers' and 'placeholders', respectively, at sites that maintained or gained accessibility upon T cell activation. In addition, a small subset of strongly induced immune response genes displayed a noncanonical TF recruitment pattern. Our study provides a key resource and foundation for the understanding of transcriptional and epigenetic regulation in T cells and offers a new perspective on the hierarchical interactions between critical TFs.T cell activation, a key early event in the adaptive immune response, is subject to elaborate transcriptional control. In the present study, we examined how the activities of eight major transcription factor (TF) families are integrated to shape the epigenome of naive and activated CD4 and CD8 T cells. By leveraging extensive polymorphisms in evolutionarily divergent mice, we identified the 'heavy lifters' positively influencing chromatin accessibility. Members of Ets, Runx and TCF/Lef TF families occupied the vast majority of accessible chromatin regions, acting as 'housekeepers', 'universal amplifiers' and 'placeholders', respectively, at sites that maintained or gained accessibility upon T cell activation. In addition, a small subset of strongly induced immune response genes displayed a noncanonical TF recruitment pattern. Our study provides a key resource and foundation for the understanding of transcriptional and epigenetic regulation in T cells and offers a new perspective on the hierarchical interactions between critical TFs.
Author Walker, Sarah K.
Pritykin, Yuri
Rudensky, Alexander Y.
van der Veeken, Joris
Leslie, Christina S.
Zhong, Yi
AuthorAffiliation 4 Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ
1 Howard Hughes Medical Institute and Immunology Program, Sloan Kettering Institute, and Ludwig Center at Memorial Sloan Kettering Cancer Center, New York, NY
6 Department of Computer Science, Princeton University, Princeton NJ
3 Shanghai Immune Therapy Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China
5 Quantitative and Computational Biology Graduate Program, Princeton University, Princeton, NJ
7 Research Institute of Molecular Pathology (IMP), Vienna Biocenter (VBC), Vienna, Austria
2 Computational and Systems Biology Program, Memorial Sloan Kettering Cancer Center, New York, NY
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Cites_doi 10.1016/j.cell.2018.03.016
10.1126/science.1162327
10.1126/science.1104935
10.1016/j.it.2016.11.004
10.1016/S0092-8674(02)01111-X
10.1016/j.immuni.2018.10.012
10.1084/jem.175.5.1391
10.1038/s41467-017-01020-6
10.1084/jem.20070133
10.1093/nar/gky491
10.1016/j.cell.2012.12.009
10.1038/nature11245
10.1038/nrg2538
10.1038/377635a0
10.1101/gad.9.8.995
10.1038/377639a0
10.1101/gad.14.3.366
10.1016/j.coi.2018.03.017
10.1016/j.cell.2013.02.014
10.1038/nrg3207
10.1242/dev.128892
10.1038/ni.3031
10.1146/annurev-immunol-041015-055318
10.1016/j.immuni.2019.03.031
10.1128/MCB.16.6.2708
10.1038/ni.1730
10.1038/ni.1663
10.1007/s00109-010-0642-1
10.1093/emboj/18.6.1609
10.1038/ni.1969
10.1038/s41588-021-00790-6
10.1126/science.1151844
10.1038/nmeth.2688
10.1016/j.cell.2014.08.009
10.1016/S0021-9258(18)46906-2
10.4049/jimmunol.1701700
10.1186/gb-2008-9-9-r137
10.1242/dev.126.14.3131
10.1002/j.1460-2075.1988.tb02904.x
10.1073/pnas.95.20.11590
10.1038/nature08750
10.1093/nar/gky955
10.1016/j.immuni.2020.10.010
10.1371/journal.pgen.1000778
10.1146/annurev.biochem.79.081507.103945
10.1038/nature10413
10.1128/MCB.24.24.10954-10964.2004
10.1101/gad.1561707
10.1093/bioinformatics/btr064
10.1038/nri3307
10.1016/1074-7613(95)90092-6
10.1016/j.immuni.2018.01.012
10.1073/pnas.2019655118
10.7554/eLife.21856
10.1146/annurev-immunol-030409-101212
10.1038/s41577-020-00426-6
10.1093/bioinformatics/bts635
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AUTHOR CONTRIBUTIONS
J.v.d.V. and A.Y.R. designed the study. J.v.d.V. performed experiments and analyzed data. Y.Z. and C.S.L. designed allele-specific analysis pipeline. Y.Z. performed computational analysis of sequencing data. S.K.W. and Y.P. analyzed single cell ATAC-seq data. J.v.d.V. and A.Y.R. wrote the manuscript with input from all authors.
These authors jointly supervised this work
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  text: 2022-01-01
  day: 01
PublicationDecade 2020
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PublicationTitle Nature immunology
PublicationTitleAbbrev Nat Immunol
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Publisher Nature Publishing Group US
Nature Publishing Group
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References Egawa, Tillman, Naoe, Taniuchi, Littman (CR46) 2007; 204
van der Veeken (CR16) 2019; 50
Thompson (CR35) 1992; 12
Keane (CR53) 2011; 477
McLane, Abdel-Hakeem, Wherry (CR3) 2019; 37
Polansky (CR18) 2010; 88
Granja (CR61) 2021; 53
van der Veeken (CR15) 2020; 53
Jolma (CR9) 2013; 152
Bassuk, Leiden (CR22) 1995; 3
Dobin (CR54) 2013; 29
Kim (CR20) 1999; 18
Mélet, Motro, Rossi, Zhang, Bernstein (CR29) 1996; 16
Yamada, Park, Mamonkin, Lacorazza (CR32) 2009; 10
Grant, Bailey, Noble (CR58) 2011; 27
Rabault, Ghysdael (CR24) 1994; 269
Wotton, Ghysdael, Wang, Speck, Owen (CR19) 1994; 14
Wang (CR21) 1994; 14
Spitz, Furlong (CR12) 2012; 13
Gray (CR7) 2004; 306
Liu (CR52) 2018; 173
Lee, Young (CR11) 2013; 152
CR2
Anderson, Hernandez-Hoyos, Diamond, Rothenberg (CR31) 1999; 126
Levanon (CR47) 1998; 95
Milner, Goldrath (CR5) 2018; 51
Pognonec, Boulukos, Gesquière, Stéhelin, Ghysdael (CR23) 1988; 7
Muthusamy, Barton, Leiden (CR28) 1995; 377
Hollenhorst, McIntosh, Graves (CR34) 2011; 80
Wang, Petryniak, Ho, Thompson, Leiden (CR36) 1992; 175
Luo (CR33) 2017; 8
Setoguchi (CR48) 2008; 319
Frankish (CR60) 2019; 47
CR44
Cowley, Graves (CR25) 2000; 14
Badis (CR8) 2009; 324
Hollenhorst, Shah, Hopkins, Graves (CR37) 2007; 21
Zheng (CR43) 2010; 463
Weirauch (CR57) 2014; 158
Zhang (CR55) 2008; 9
CR14
Gerstein (CR10) 2012; 489
CR51
Giese, Kingsley, Kirshner, Grosschedl (CR39) 1995; 9
Lazarevic (CR41) 2011; 12
Johnson (CR49) 2018; 48
Li, Brown, Huang, Bickel (CR56) 2011; 5
Link, Romanoski, Metzler, Glass (CR59) 2018; 46
Verbaro, Sakurai, Kim, Shinkai, Egawa (CR40) 2018; 200
Mackay, Kallies (CR4) 2017; 38
Kaech, Cui (CR1) 2012; 12
Kim (CR30) 2018; 49
Zhang, Meng, Strober (CR42) 2008; 9
Buenrostro, Giresi, Zaba, Chang, Greenleaf (CR50) 2013; 10
Bories (CR27) 1995; 377
Chang, Wherry, Goldrath (CR13) 2014; 15
Hollenhorst (CR38) 2009; 5
Hota, Bruneau (CR17) 2016; 143
Foulds, Nelson, Blaszczak, Graves (CR26) 2004; 24
Vaquerizas, Kummerfeld, Teichmann, Luscombe (CR6) 2009; 10
Taniuchi (CR45) 2002; 111
PC Hollenhorst (1086_CR38) 2009; 5
T Egawa (1086_CR46) 2007; 204
VM Link (1086_CR59) 2018; 46
MT Weirauch (1086_CR57) 2014; 158
J van der Veeken (1086_CR15) 2020; 53
PC Hollenhorst (1086_CR37) 2007; 21
LK Mackay (1086_CR4) 2017; 38
PA Gray (1086_CR7) 2004; 306
Q Li (1086_CR56) 2011; 5
JT Chang (1086_CR13) 2014; 15
JC Bories (1086_CR27) 1995; 377
J van der Veeken (1086_CR16) 2019; 50
JM Granja (1086_CR61) 2021; 53
JL Johnson (1086_CR49) 2018; 48
D Wotton (1086_CR19) 1994; 14
TM Keane (1086_CR53) 2011; 477
TI Lee (1086_CR11) 2013; 152
JJ Milner (1086_CR5) 2018; 51
PC Hollenhorst (1086_CR34) 2011; 80
CE Foulds (1086_CR26) 2004; 24
Y Zheng (1086_CR43) 2010; 463
F Zhang (1086_CR42) 2008; 9
1086_CR2
AG Bassuk (1086_CR22) 1995; 3
T Yamada (1086_CR32) 2009; 10
CT Luo (1086_CR33) 2017; 8
CE Grant (1086_CR58) 2011; 27
MK Anderson (1086_CR31) 1999; 126
DJ Verbaro (1086_CR40) 2018; 200
JK Polansky (1086_CR18) 2010; 88
G Badis (1086_CR8) 2009; 324
P Pognonec (1086_CR23) 1988; 7
1086_CR51
V Lazarevic (1086_CR41) 2011; 12
Y Zhang (1086_CR55) 2008; 9
CB Thompson (1086_CR35) 1992; 12
A Frankish (1086_CR60) 2019; 47
CY Wang (1086_CR21) 1994; 14
CY Wang (1086_CR36) 1992; 175
A Dobin (1086_CR54) 2013; 29
R Setoguchi (1086_CR48) 2008; 319
1086_CR14
F Spitz (1086_CR12) 2012; 13
DO Cowley (1086_CR25) 2000; 14
MB Gerstein (1086_CR10) 2012; 489
F Mélet (1086_CR29) 1996; 16
CJ Kim (1086_CR30) 2018; 49
WY Kim (1086_CR20) 1999; 18
A Jolma (1086_CR9) 2013; 152
N Liu (1086_CR52) 2018; 173
D Levanon (1086_CR47) 1998; 95
N Muthusamy (1086_CR28) 1995; 377
JM Vaquerizas (1086_CR6) 2009; 10
SM Kaech (1086_CR1) 2012; 12
I Taniuchi (1086_CR45) 2002; 111
LM McLane (1086_CR3) 2019; 37
JD Buenrostro (1086_CR50) 2013; 10
B Rabault (1086_CR24) 1994; 269
K Giese (1086_CR39) 1995; 9
SK Hota (1086_CR17) 2016; 143
1086_CR44
34937931 - Nat Immunol. 2022 Jan;23(1):3-4. doi: 10.1038/s41590-021-01075-0.
References_xml – volume: 173
  start-page: 430
  year: 2018
  end-page: 442.e417
  ident: CR52
  article-title: Direct promoter repression by BCL11A controls the fetal to adult hemoglobin switch
  publication-title: Cell
  doi: 10.1016/j.cell.2018.03.016
– volume: 324
  start-page: 1720
  year: 2009
  end-page: 1723
  ident: CR8
  article-title: Diversity and complexity in DNA recognition by transcription factors
  publication-title: Science
  doi: 10.1126/science.1162327
– ident: CR51
– volume: 306
  start-page: 2255
  year: 2004
  end-page: 2257
  ident: CR7
  article-title: Mouse brain organization revealed through direct genome-scale TF expression analysis
  publication-title: Science
  doi: 10.1126/science.1104935
– volume: 38
  start-page: 94
  year: 2017
  end-page: 103
  ident: CR4
  article-title: Transcriptional regulation of tissue-resident lymphocytes
  publication-title: Trends Immunol.
  doi: 10.1016/j.it.2016.11.004
– volume: 111
  start-page: 621
  year: 2002
  end-page: 633
  ident: CR45
  article-title: Differential requirements for Runx proteins in CD4 repression and epigenetic silencing during T lymphocyte development
  publication-title: Cell
  doi: 10.1016/S0092-8674(02)01111-X
– volume: 49
  start-page: 1034
  year: 2018
  end-page: 1048.e1038
  ident: CR30
  article-title: The transcription factor Ets1 suppresses T follicular helper type 2 cell differentiation to halt the onset of systemic lupus erythematosus
  publication-title: Immunity
  doi: 10.1016/j.immuni.2018.10.012
– volume: 175
  start-page: 1391
  year: 1992
  end-page: 1399
  ident: CR36
  article-title: Evolutionarily conserved Ets family members display distinct DNA binding specificities
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.175.5.1391
– volume: 8
  year: 2017
  ident: CR33
  article-title: Ets transcription factor GABP controls T cell homeostasis and immunity
  publication-title: Nat. Commun.
  doi: 10.1038/s41467-017-01020-6
– volume: 204
  start-page: 1945
  year: 2007
  end-page: 1957
  ident: CR46
  article-title: The role of the Runx transcription factors in thymocyte differentiation and in homeostasis of naive T cells
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.20070133
– volume: 29
  start-page: 15
  year: 2013
  end-page: 21
  ident: CR54
  article-title: STAR: ultrafast universal RNA-seq aligner
  publication-title: Bioinformatics
– volume: 46
  start-page: 7006
  year: 2018
  end-page: 7021
  ident: CR59
  article-title: MMARGE: motif mutation analysis for regulatory genomic elements
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gky491
– volume: 152
  start-page: 327
  year: 2013
  end-page: 339
  ident: CR9
  article-title: DNA-binding specificities of human transcription factors
  publication-title: Cell
  doi: 10.1016/j.cell.2012.12.009
– volume: 489
  start-page: 91
  year: 2012
  end-page: 100
  ident: CR10
  article-title: Architecture of the human regulatory network derived from ENCODE data
  publication-title: Nature
  doi: 10.1038/nature11245
– volume: 10
  start-page: 252
  year: 2009
  end-page: 263
  ident: CR6
  article-title: A census of human transcription factors: function, expression and evolution
  publication-title: Nat. Rev. Genet.
  doi: 10.1038/nrg2538
– volume: 377
  start-page: 635
  year: 1995
  end-page: 638
  ident: CR27
  article-title: Increased T-cell apoptosis and terminal B-cell differentiation induced by inactivation of the Ets-1 proto-oncogene
  publication-title: Nature
  doi: 10.1038/377635a0
– volume: 9
  start-page: 995
  year: 1995
  end-page: 1008
  ident: CR39
  article-title: Assembly and function of a TCR alpha enhancer complex is dependent on LEF-1-induced DNA bending and multiple protein–protein interactions
  publication-title: Genes Dev.
  doi: 10.1101/gad.9.8.995
– volume: 377
  start-page: 639
  year: 1995
  end-page: 642
  ident: CR28
  article-title: Defective activation and survival of T cells lacking the Ets-1 transcription factor
  publication-title: Nature
  doi: 10.1038/377639a0
– volume: 14
  start-page: 366
  year: 2000
  end-page: 376
  ident: CR25
  article-title: Phosphorylation represses Ets-1 DNA binding by reinforcing autoinhibition
  publication-title: Genes Dev.
  doi: 10.1101/gad.14.3.366
– volume: 51
  start-page: 162
  year: 2018
  end-page: CD169
  ident: CR5
  article-title: Transcriptional programming of tissue-resident memory CD8
  publication-title: Curr. Opin. Immunol.
  doi: 10.1016/j.coi.2018.03.017
– volume: 152
  start-page: 1237
  year: 2013
  end-page: 1251
  ident: CR11
  article-title: Transcriptional regulation and its misregulation in disease
  publication-title: Cell
  doi: 10.1016/j.cell.2013.02.014
– volume: 14
  start-page: 840
  year: 1994
  end-page: 850
  ident: CR19
  article-title: Cooperative binding of Ets-1 and core binding factor to DNA
  publication-title: Mol. Cell Biol.
– volume: 13
  start-page: 613
  year: 2012
  end-page: 626
  ident: CR12
  article-title: Transcription factors: from enhancer binding to developmental control
  publication-title: Nat. Rev. Genet.
  doi: 10.1038/nrg3207
– volume: 143
  start-page: 2882
  year: 2016
  end-page: 2897
  ident: CR17
  article-title: ATP-dependent chromatin remodeling during mammalian development
  publication-title: Development
  doi: 10.1242/dev.128892
– volume: 12
  start-page: 1043
  year: 1992
  end-page: 1053
  ident: CR35
  article-title: -acting sequences required for inducible interleukin-2 enhancer function bind a novel Ets-related protein, Elf-1
  publication-title: Mol. Cell Biol.
– volume: 15
  start-page: 1104
  year: 2014
  end-page: 1115
  ident: CR13
  article-title: Molecular regulation of effector and memory T cell differentiation
  publication-title: Nat. Immunol.
  doi: 10.1038/ni.3031
– volume: 37
  start-page: 457
  year: 2019
  end-page: 495
  ident: CR3
  article-title: CD8 T cell exhaustion during chronic viral infection and cancer
  publication-title: Annu. Rev. Immunol.
  doi: 10.1146/annurev-immunol-041015-055318
– volume: 50
  start-page: 1202
  year: 2019
  end-page: 1217.e1207
  ident: CR16
  article-title: Natural genetic variation reveals key features of epigenetic and transcriptional memory in virus-specific CD8 T cells
  publication-title: Immunity
  doi: 10.1016/j.immuni.2019.03.031
– volume: 16
  start-page: 2708
  year: 1996
  end-page: 2718
  ident: CR29
  article-title: Generation of a novel Fli-1 protein by gene targeting leads to a defect in thymus development and a delay in Friend virus-induced erythroleukemia
  publication-title: Mol. Cell Biol.
  doi: 10.1128/MCB.16.6.2708
– volume: 14
  start-page: 1153
  year: 1994
  end-page: 1159
  ident: CR21
  article-title: Activation of the granulocyte–macrophage colony-stimulating factor promoter in T cells requires cooperative binding of Elf-1 and AP-1 transcription factors
  publication-title: Mol. Cell Biol.
– volume: 10
  start-page: 618
  year: 2009
  end-page: 626
  ident: CR32
  article-title: Transcription factor ELF4 controls the proliferation and homing of CD8 T cells via the Krüppel-like factors KLF4 and KLF2
  publication-title: Nat. Immunol.
  doi: 10.1038/ni.1730
– ident: CR14
– ident: CR2
– volume: 9
  start-page: 1297
  year: 2008
  end-page: 1306
  ident: CR42
  article-title: Interactions among the transcription factors Runx1, RORgammat and Foxp3 regulate the differentiation of interleukin 17-producing T cells
  publication-title: Nat. Immunol.
  doi: 10.1038/ni.1663
– volume: 88
  start-page: 1029
  year: 2010
  end-page: 1040
  ident: CR18
  article-title: Methylation matters: binding of Ets-1 to the demethylated Foxp3 gene contributes to the stabilization of Foxp3 expression in regulatory T cells
  publication-title: J. Mol. Med.
  doi: 10.1007/s00109-010-0642-1
– volume: 18
  start-page: 1609
  year: 1999
  end-page: 1620
  ident: CR20
  article-title: Mutual activation of Ets-1 and AML1 DNA binding by direct interaction of their autoinhibitory domains
  publication-title: EMBO J.
  doi: 10.1093/emboj/18.6.1609
– volume: 12
  start-page: 96
  year: 2011
  end-page: 104
  ident: CR41
  article-title: T-bet represses T 17 differentiation by preventing Runx1-mediated activation of the gene encoding RORγt
  publication-title: Nat. Immunol.
  doi: 10.1038/ni.1969
– volume: 53
  start-page: 403
  year: 2021
  end-page: 411
  ident: CR61
  article-title: ArchR is a scalable software package for integrative single-cell chromatin accessibility analysis
  publication-title: Nat. Genet.
  doi: 10.1038/s41588-021-00790-6
– volume: 319
  start-page: 822
  year: 2008
  end-page: 825
  ident: CR48
  article-title: Repression of the transcription factor Th-POK by Runx complexes in cytotoxic T cell development
  publication-title: Science
  doi: 10.1126/science.1151844
– volume: 10
  start-page: 1213
  year: 2013
  end-page: 1218
  ident: CR50
  article-title: Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position
  publication-title: Nat. Methods
  doi: 10.1038/nmeth.2688
– volume: 158
  start-page: 1431
  year: 2014
  end-page: 1443
  ident: CR57
  article-title: Determination and inference of eukaryotic transcription factor sequence specificity
  publication-title: Cell
  doi: 10.1016/j.cell.2014.08.009
– volume: 269
  start-page: 28143
  year: 1994
  end-page: 28151
  ident: CR24
  article-title: Calcium-induced phosphorylation of ETS1 inhibits its specific DNA binding activity
  publication-title: J. Biol. Chem.
  doi: 10.1016/S0021-9258(18)46906-2
– volume: 200
  start-page: 3891
  year: 2018
  end-page: 3896
  ident: CR40
  article-title: Cutting edge: the histone methyltransferase G9a is required for silencing of helper T lineage-associated genes in proliferating CD8 T cells
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.1701700
– volume: 9
  year: 2008
  ident: CR55
  article-title: Model-based analysis of ChIP-Seq (MACS)
  publication-title: Genome Biol.
  doi: 10.1186/gb-2008-9-9-r137
– volume: 126
  start-page: 3131
  year: 1999
  end-page: 3148
  ident: CR31
  article-title: Precise developmental regulation of Ets family transcription factors during specification and commitment to the T cell lineage
  publication-title: Development
  doi: 10.1242/dev.126.14.3131
– ident: CR44
– volume: 7
  start-page: 977
  year: 1988
  end-page: 983
  ident: CR23
  article-title: Mitogenic stimulation of thymocytes results in the calcium-dependent phosphorylation of c-ets-1 proteins
  publication-title: EMBO J.
  doi: 10.1002/j.1460-2075.1988.tb02904.x
– volume: 95
  start-page: 11590
  year: 1998
  end-page: 11595
  ident: CR47
  article-title: Transcriptional repression by AML1 and LEF-1 is mediated by the TLE/Groucho corepressors
  publication-title: Proc. Natl Acad. Sci. USA
  doi: 10.1073/pnas.95.20.11590
– volume: 5
  start-page: 1752
  year: 2011
  end-page: 1779
  ident: CR56
  article-title: Measuring reproducibility of high-throughput experiments
  publication-title: Ann. Appl. Stat.
– volume: 463
  start-page: 808
  year: 2010
  end-page: 812
  ident: CR43
  article-title: Role of conserved non-coding DNA elements in the Foxp3 gene in regulatory T-cell fate
  publication-title: Nature
  doi: 10.1038/nature08750
– volume: 47
  start-page: D766
  year: 2019
  end-page: D773
  ident: CR60
  article-title: GENCODE reference annotation for the human and mouse genomes
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gky955
– volume: 53
  start-page: 971
  year: 2020
  end-page: 984.e975
  ident: CR15
  article-title: The transcription factor Foxp3 shapes regulatory T cell identity by tuning the activity of -acting intermediaries
  publication-title: Immunity
  doi: 10.1016/j.immuni.2020.10.010
– volume: 5
  start-page: e1000778
  year: 2009
  ident: CR38
  article-title: DNA specificity determinants associate with distinct transcription factor functions
  publication-title: PLoS Genet.
  doi: 10.1371/journal.pgen.1000778
– volume: 80
  start-page: 437
  year: 2011
  end-page: 471
  ident: CR34
  article-title: Genomic and biochemical insights into the specificity of ETS transcription factors
  publication-title: Annu. Rev. Biochem.
  doi: 10.1146/annurev.biochem.79.081507.103945
– volume: 477
  start-page: 289
  year: 2011
  end-page: 294
  ident: CR53
  article-title: Mouse genomic variation and its effect on phenotypes and gene regulation
  publication-title: Nature
  doi: 10.1038/nature10413
– volume: 24
  start-page: 10954
  year: 2004
  end-page: 10964
  ident: CR26
  article-title: Ras/mitogen-activated protein kinase signaling activates Ets-1 and Ets-2 by CBP/p300 recruitment
  publication-title: Mol. Cell Biol.
  doi: 10.1128/MCB.24.24.10954-10964.2004
– volume: 21
  start-page: 1882
  year: 2007
  end-page: 1894
  ident: CR37
  article-title: Genome-wide analyses reveal properties of redundant and specific promoter occupancy within the ETS gene family
  publication-title: Genes Dev.
  doi: 10.1101/gad.1561707
– volume: 27
  start-page: 1017
  year: 2011
  end-page: 1018
  ident: CR58
  article-title: FIMO: scanning for occurrences of a given motif
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btr064
– volume: 12
  start-page: 749
  year: 2012
  end-page: 761
  ident: CR1
  article-title: Transcriptional control of effector and memory CD8 T cell differentiation
  publication-title: Nat. Rev. Immunol.
  doi: 10.1038/nri3307
– volume: 3
  start-page: 223
  year: 1995
  end-page: 237
  ident: CR22
  article-title: A direct physical association between ETS and AP-1 transcription factors in normal human T cells
  publication-title: Immunity
  doi: 10.1016/1074-7613(95)90092-6
– volume: 48
  start-page: 243
  year: 2018
  end-page: 257.e210
  ident: CR49
  article-title: Lineage-determining transcription factor TCF-1 initiates the epigenetic identity of T cells
  publication-title: Immunity
  doi: 10.1016/j.immuni.2018.01.012
– volume: 50
  start-page: 1202
  year: 2019
  ident: 1086_CR16
  publication-title: Immunity
  doi: 10.1016/j.immuni.2019.03.031
– volume: 111
  start-page: 621
  year: 2002
  ident: 1086_CR45
  publication-title: Cell
  doi: 10.1016/S0092-8674(02)01111-X
– volume: 80
  start-page: 437
  year: 2011
  ident: 1086_CR34
  publication-title: Annu. Rev. Biochem.
  doi: 10.1146/annurev.biochem.79.081507.103945
– volume: 21
  start-page: 1882
  year: 2007
  ident: 1086_CR37
  publication-title: Genes Dev.
  doi: 10.1101/gad.1561707
– volume: 143
  start-page: 2882
  year: 2016
  ident: 1086_CR17
  publication-title: Development
  doi: 10.1242/dev.128892
– ident: 1086_CR44
  doi: 10.1073/pnas.2019655118
– volume: 48
  start-page: 243
  year: 2018
  ident: 1086_CR49
  publication-title: Immunity
  doi: 10.1016/j.immuni.2018.01.012
– volume: 477
  start-page: 289
  year: 2011
  ident: 1086_CR53
  publication-title: Nature
  doi: 10.1038/nature10413
– volume: 27
  start-page: 1017
  year: 2011
  ident: 1086_CR58
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btr064
– volume: 306
  start-page: 2255
  year: 2004
  ident: 1086_CR7
  publication-title: Science
  doi: 10.1126/science.1104935
– volume: 10
  start-page: 1213
  year: 2013
  ident: 1086_CR50
  publication-title: Nat. Methods
  doi: 10.1038/nmeth.2688
– volume: 51
  start-page: 162
  year: 2018
  ident: 1086_CR5
  publication-title: Curr. Opin. Immunol.
  doi: 10.1016/j.coi.2018.03.017
– volume: 13
  start-page: 613
  year: 2012
  ident: 1086_CR12
  publication-title: Nat. Rev. Genet.
  doi: 10.1038/nrg3207
– volume: 10
  start-page: 618
  year: 2009
  ident: 1086_CR32
  publication-title: Nat. Immunol.
  doi: 10.1038/ni.1730
– volume: 46
  start-page: 7006
  year: 2018
  ident: 1086_CR59
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gky491
– ident: 1086_CR51
  doi: 10.7554/eLife.21856
– volume: 377
  start-page: 639
  year: 1995
  ident: 1086_CR28
  publication-title: Nature
  doi: 10.1038/377639a0
– volume: 9
  year: 2008
  ident: 1086_CR55
  publication-title: Genome Biol.
  doi: 10.1186/gb-2008-9-9-r137
– volume: 489
  start-page: 91
  year: 2012
  ident: 1086_CR10
  publication-title: Nature
  doi: 10.1038/nature11245
– volume: 12
  start-page: 749
  year: 2012
  ident: 1086_CR1
  publication-title: Nat. Rev. Immunol.
  doi: 10.1038/nri3307
– volume: 15
  start-page: 1104
  year: 2014
  ident: 1086_CR13
  publication-title: Nat. Immunol.
  doi: 10.1038/ni.3031
– volume: 126
  start-page: 3131
  year: 1999
  ident: 1086_CR31
  publication-title: Development
  doi: 10.1242/dev.126.14.3131
– volume: 9
  start-page: 995
  year: 1995
  ident: 1086_CR39
  publication-title: Genes Dev.
  doi: 10.1101/gad.9.8.995
– volume: 8
  year: 2017
  ident: 1086_CR33
  publication-title: Nat. Commun.
  doi: 10.1038/s41467-017-01020-6
– volume: 53
  start-page: 403
  year: 2021
  ident: 1086_CR61
  publication-title: Nat. Genet.
  doi: 10.1038/s41588-021-00790-6
– volume: 12
  start-page: 1043
  year: 1992
  ident: 1086_CR35
  publication-title: Mol. Cell Biol.
– volume: 14
  start-page: 1153
  year: 1994
  ident: 1086_CR21
  publication-title: Mol. Cell Biol.
– volume: 152
  start-page: 1237
  year: 2013
  ident: 1086_CR11
  publication-title: Cell
  doi: 10.1016/j.cell.2013.02.014
– volume: 175
  start-page: 1391
  year: 1992
  ident: 1086_CR36
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.175.5.1391
– volume: 5
  start-page: e1000778
  year: 2009
  ident: 1086_CR38
  publication-title: PLoS Genet.
  doi: 10.1371/journal.pgen.1000778
– volume: 9
  start-page: 1297
  year: 2008
  ident: 1086_CR42
  publication-title: Nat. Immunol.
  doi: 10.1038/ni.1663
– volume: 200
  start-page: 3891
  year: 2018
  ident: 1086_CR40
  publication-title: J. Immunol.
  doi: 10.4049/jimmunol.1701700
– ident: 1086_CR2
  doi: 10.1146/annurev-immunol-030409-101212
– volume: 95
  start-page: 11590
  year: 1998
  ident: 1086_CR47
  publication-title: Proc. Natl Acad. Sci. USA
  doi: 10.1073/pnas.95.20.11590
– volume: 173
  start-page: 430
  year: 2018
  ident: 1086_CR52
  publication-title: Cell
  doi: 10.1016/j.cell.2018.03.016
– volume: 14
  start-page: 366
  year: 2000
  ident: 1086_CR25
  publication-title: Genes Dev.
  doi: 10.1101/gad.14.3.366
– volume: 88
  start-page: 1029
  year: 2010
  ident: 1086_CR18
  publication-title: J. Mol. Med.
  doi: 10.1007/s00109-010-0642-1
– volume: 14
  start-page: 840
  year: 1994
  ident: 1086_CR19
  publication-title: Mol. Cell Biol.
– volume: 38
  start-page: 94
  year: 2017
  ident: 1086_CR4
  publication-title: Trends Immunol.
  doi: 10.1016/j.it.2016.11.004
– volume: 16
  start-page: 2708
  year: 1996
  ident: 1086_CR29
  publication-title: Mol. Cell Biol.
  doi: 10.1128/MCB.16.6.2708
– volume: 377
  start-page: 635
  year: 1995
  ident: 1086_CR27
  publication-title: Nature
  doi: 10.1038/377635a0
– volume: 49
  start-page: 1034
  year: 2018
  ident: 1086_CR30
  publication-title: Immunity
  doi: 10.1016/j.immuni.2018.10.012
– volume: 319
  start-page: 822
  year: 2008
  ident: 1086_CR48
  publication-title: Science
  doi: 10.1126/science.1151844
– ident: 1086_CR14
  doi: 10.1038/s41577-020-00426-6
– volume: 158
  start-page: 1431
  year: 2014
  ident: 1086_CR57
  publication-title: Cell
  doi: 10.1016/j.cell.2014.08.009
– volume: 10
  start-page: 252
  year: 2009
  ident: 1086_CR6
  publication-title: Nat. Rev. Genet.
  doi: 10.1038/nrg2538
– volume: 3
  start-page: 223
  year: 1995
  ident: 1086_CR22
  publication-title: Immunity
  doi: 10.1016/1074-7613(95)90092-6
– volume: 324
  start-page: 1720
  year: 2009
  ident: 1086_CR8
  publication-title: Science
  doi: 10.1126/science.1162327
– volume: 24
  start-page: 10954
  year: 2004
  ident: 1086_CR26
  publication-title: Mol. Cell Biol.
  doi: 10.1128/MCB.24.24.10954-10964.2004
– volume: 29
  start-page: 15
  year: 2013
  ident: 1086_CR54
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/bts635
– volume: 463
  start-page: 808
  year: 2010
  ident: 1086_CR43
  publication-title: Nature
  doi: 10.1038/nature08750
– volume: 53
  start-page: 971
  year: 2020
  ident: 1086_CR15
  publication-title: Immunity
  doi: 10.1016/j.immuni.2020.10.010
– volume: 7
  start-page: 977
  year: 1988
  ident: 1086_CR23
  publication-title: EMBO J.
  doi: 10.1002/j.1460-2075.1988.tb02904.x
– volume: 18
  start-page: 1609
  year: 1999
  ident: 1086_CR20
  publication-title: EMBO J.
  doi: 10.1093/emboj/18.6.1609
– volume: 37
  start-page: 457
  year: 2019
  ident: 1086_CR3
  publication-title: Annu. Rev. Immunol.
  doi: 10.1146/annurev-immunol-041015-055318
– volume: 47
  start-page: D766
  year: 2019
  ident: 1086_CR60
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gky955
– volume: 204
  start-page: 1945
  year: 2007
  ident: 1086_CR46
  publication-title: J. Exp. Med.
  doi: 10.1084/jem.20070133
– volume: 152
  start-page: 327
  year: 2013
  ident: 1086_CR9
  publication-title: Cell
  doi: 10.1016/j.cell.2012.12.009
– volume: 12
  start-page: 96
  year: 2011
  ident: 1086_CR41
  publication-title: Nat. Immunol.
  doi: 10.1038/ni.1969
– volume: 269
  start-page: 28143
  year: 1994
  ident: 1086_CR24
  publication-title: J. Biol. Chem.
  doi: 10.1016/S0021-9258(18)46906-2
– volume: 5
  start-page: 1752
  year: 2011
  ident: 1086_CR56
  publication-title: Ann. Appl. Stat.
– reference: 34937931 - Nat Immunol. 2022 Jan;23(1):3-4. doi: 10.1038/s41590-021-01075-0.
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Snippet T cell activation, a key early event in the adaptive immune response, is subject to elaborate transcriptional control. In the present study, we examined how...
T cell activation, a key early event in the adaptive immune response, is subject to elaborate transcriptional control. Here, we examined how the activities of...
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StartPage 122
SubjectTerms 631/250/2502/2170
631/250/2502/248
Adaptive immunity
Adaptive Immunity - immunology
Animals
Biomedical and Life Sciences
Biomedicine
CD4 antigen
CD4-Positive T-Lymphocytes - immunology
CD8 antigen
CD8-Positive T-Lymphocytes - immunology
Cell activation
Chromatin
Chromatin - immunology
Divergence
Epigenesis, Genetic - immunology
Epigenetics
Epigenome - immunology
ETS protein
Gene expression
Gene Expression Regulation - immunology
Gene regulation
Immune response
Immunology
Infectious Diseases
LEF protein
Lymphocyte Activation - immunology
Lymphocytes
Lymphocytes T
Male
Mice
Resource
Transcription factors
Transcription Factors - immunology
Title Hierarchical regulation of the resting and activated T cell epigenome by major transcription factor families
URI https://link.springer.com/article/10.1038/s41590-021-01086-x
https://www.ncbi.nlm.nih.gov/pubmed/34937932
https://www.proquest.com/docview/2613412031
https://www.proquest.com/docview/2613289979
https://pubmed.ncbi.nlm.nih.gov/PMC8712421
Volume 23
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