An anti-silencer– and SATB1-dependent chromatin hub regulates Rag1 and Rag2 gene expression during thymocyte development

Hao, Bingtao; Naik, Abani Kanta; Watanabe, Akiko; Tanaka, Hirokazu; Chen, Liang; Richards, Hunter W.; Kondo, Motonari; Taniuchi, Ichiro; Kohwi, Yoshinori; Kohwi-Shigematsu, Terumi; Krangel, Michael S.

doi:10.1084/jem.20142207

An anti-silencer– and SATB1-dependent chromatin hub regulates Rag1 and Rag2 gene expression during thymocyte development

Journal Article · Mon Apr 06 00:00:00 EDT 2015 · Journal of Experimental Medicine

DOI:https://doi.org/10.1084/jem.20142207· OSTI ID:1625199

Hao, Bingtao ^[1]; Naik, Abani Kanta ^[2]; Watanabe, Akiko ^[2]; Tanaka, Hirokazu ^[3]; Chen, Liang ^[2]; Richards, Hunter W. ^[4]; Kondo, Motonari ^[2]; Taniuchi, Ichiro ^[3]; Kohwi, Yoshinori ^[4]; Kohwi-Shigematsu, Terumi ^[4]; Krangel, Michael S. ^[2]

Duke University, Durham, NC (United States); DOE/OSTI
Duke University, Durham, NC (United States)
RIKEN Center for Centre for Integrative Medical Sciences, Yokohama (Japan)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Rag1 and Rag2 gene expression in CD4⁺CD8⁺ double-positive (DP) thymocytes depends on the activity of a distant anti-silencer element (ASE) that counteracts the activity of an intergenic silencer. However, the mechanistic basis for ASE activity is unknown. Here, we show that the ASE physically interacts with the distant Rag1 and Rag2 gene promoters in DP thymocytes, bringing the two promoters together to form an active chromatin hub. Moreover, we show that the ASE functions as a classical enhancer that can potently activate these promoters in the absence of the silencer or other locus elements. In thymocytes lacking the chromatin organizer SATB1, we identified a partial defect in Tcra gene rearrangement that was associated with reduced expression of Rag1 and Rag2 at the DP stage. SATB1 binds to the ASE and Rag promoters, facilitating inclusion of Rag2 in the chromatin hub and the loading of RNA polymerase II to both the Rag1 and Rag2 promoters. Our results provide a novel framework for understanding ASE function and demonstrate a novel role for SATB1 as a regulator of Rag locus organization and gene expression in DP thymocytes.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: Japan Society for the Promotion of Science (JSPS); Leukemia and Lymphoma Society Scholar Award; National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1625199

Journal Information:: Journal of Experimental Medicine, Journal Name: Journal of Experimental Medicine Journal Issue: 5 Vol. 212; ISSN 0022-1007

Publisher:: Rockefeller University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (66)

Identification of genes involved in the initiation of human Th1 or Th2 cell commitment Lund, Riikka; Ahlfors, Helena; Kainonen, Essi European Journal of Immunology, Vol. 35, Issue 11 https://doi.org/10.1002/eji.200526079	journal	November 2005
Transgenic mice with hematopoietic and lymphoid specific expression of Cre de Boer, Jasper; Williams, Adam; Skavdis, George European Journal of Immunology, Vol. 33, Issue 2 https://doi.org/10.1002/immu.200310005	journal	February 2003
Generation of an Improved Luciferase Reporter Gene Plasmid That Employs a Novel Mechanism for High-Copy Replication Bert, Andrew G.; Burrows, Joanna; Osborne, Cameron S. Plasmid, Vol. 44, Issue 2 https://doi.org/10.1006/plas.2000.1474	journal	September 2000
Functional and Mechanistic Diversity of Distal Transcription Enhancers Bulger, Michael; Groudine, Mark Cell, Vol. 144, Issue 5 https://doi.org/10.1016/j.cell.2011.02.026	journal	March 2011
CTCF and Cohesin: Linking Gene Regulatory Elements with Their Targets Merkenschlager, Matthias; Odom, Duncan T. Cell, Vol. 152, Issue 6 https://doi.org/10.1016/j.cell.2013.02.029	journal	March 2013
Mechanisms controlling expression of the RAG locus during lymphocyte development Kuo, Tracy C.; Schlissel, Mark S. Current Opinion in Immunology, Vol. 21, Issue 2 https://doi.org/10.1016/j.coi.2009.03.008	journal	April 2009
Mechanics of T cell receptor gene rearrangement Krangel, Michael S. Current Opinion in Immunology, Vol. 21, Issue 2 https://doi.org/10.1016/j.coi.2009.03.009	journal	April 2009
The Satb1 Protein Directs Hematopoietic Stem Cell Differentiation toward Lymphoid Lineages Satoh, Yusuke; Yokota, Takafumi; Sudo, Takao Immunity, Vol. 38, Issue 6 https://doi.org/10.1016/j.immuni.2013.05.014	journal	June 2013
Phosphorylation of SATB1, a Global Gene Regulator, Acts as a Molecular Switch Regulating Its Transcriptional Activity In Vivo Pavan Kumar, P.; Purbey, Prabhat Kumar; Sinha, Chandan Kumar Molecular Cell, Vol. 22, Issue 2 https://doi.org/10.1016/j.molcel.2006.03.010	journal	April 2006
Modification of Enhancer Chromatin: What, How, and Why? Calo, Eliezer; Wysocka, Joanna Molecular Cell, Vol. 49, Issue 5 https://doi.org/10.1016/j.molcel.2013.01.038	journal	March 2013
The Hierarchy of the 3D Genome Gibcus, Johan H.; Dekker, Job Molecular Cell, Vol. 49, Issue 5 https://doi.org/10.1016/j.molcel.2013.02.011	journal	March 2013
Essential Role of LAT in T Cell Development Zhang, Weiguo; Sommers, Connie L.; Burshtyn, Deborah N. Immunity, Vol. 10, Issue 3 https://doi.org/10.1016/s1074-7613(00)80032-1	journal	March 1999
A Conserved Transcriptional Enhancer Regulates RAG Gene Expression in Developing B Cells Hsu, Lih-Yun; Lauring, Josh; Liang, Hong-Erh Immunity, Vol. 19, Issue 1 https://doi.org/10.1016/s1074-7613(03)00181-x	journal	July 2003
Chromatin Architecture and the Generation of Antigen Receptor Diversity Jhunjhunwala, Suchit; van Zelm, Menno C.; Peak, Mandy M. Journal of End-to-End-testing, Vol. 138, Issue 33 https://doi.org/10.1016/s9999-9994(09)20447-8	journal	August 2009
SATB1 targets chromatin remodelling to regulate genes over long distances Yasui, Dag; Miyano, Masaru; Cai, Shutao Nature, Vol. 419, Issue 6907 https://doi.org/10.1038/nature01084	journal	October 2002
SATB1 reprogrammes gene expression to promote breast tumour growth and metastasis Han, Hye-Jung; Russo, Jose; Kohwi, Yoshinori Nature, Vol. 452, Issue 7184 https://doi.org/10.1038/nature06781	journal	March 2008
Widespread transcription at neuronal activity-regulated enhancers Kim, Tae-Kyung; Hemberg, Martin; Gray, Jesse M. Nature, Vol. 465, Issue 7295 https://doi.org/10.1038/nature09033	journal	April 2010
Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation Li, Wenbo; Notani, Dimple; Ma, Qi Nature, Vol. 498, Issue 7455 https://doi.org/10.1038/nature12210	journal	June 2013
Required enhancer–matrin-3 network interactions for a homeodomain transcription program Skowronska-Krawczyk, Dorota; Ma, Qi; Schwartz, Michal Nature, Vol. 514, Issue 7521 https://doi.org/10.1038/nature13573	journal	August 2014
Functional interaction between PML and SATB1 regulates chromatin-loop architecture and transcription of the MHC class I locus P., Pavan Kumar; Bischof, Oliver; Purbey, Prabhat Kumar Nature Cell Biology, Vol. 9, Issue 1 https://doi.org/10.1038/ncb1516	journal	December 2006
Tissue-specific nuclear architecture and gene expession regulated by SATB1 Cai, Shutao; Han, Hye-Jung; Kohwi-Shigematsu, Terumi Nature Genetics, Vol. 34, Issue 1 https://doi.org/10.1038/ng1146	journal	April 2003
Repression of the genome organizer SATB1 in regulatory T cells is required for suppressive function and inhibition of effector differentiation Beyer, Marc; Thabet, Yasser; Müller, Roman-Ulrich Nature Immunology, Vol. 12, Issue 9 https://doi.org/10.1038/ni.2084	journal	August 2011
A cis element in the recombination activating gene locus regulates gene expression by counteracting a distant silencer Yannoutsos, Nikos; Barreto, Vasco; Misulovin, Ziva Nature Immunology, Vol. 5, Issue 4 https://doi.org/10.1038/ni1053	journal	March 2004
Regulation of T cell receptor α gene assembly by a complex hierarchy of germline Jα promoters Hawwari, Abbas; Bock, Cheryl; Krangel, Michael S. Nature Immunology, Vol. 6, Issue 5 https://doi.org/10.1038/ni1189	journal	April 2005
Regulation of the TCRα repertoire by the survival window of CD4+CD8+ thymocytes Guo, Jian; Hawwari, Abbas; Li, Hong Nature Immunology, Vol. 3, Issue 5 https://doi.org/10.1038/ni791	journal	April 2002
Transcription initiation platforms and GTF recruitment at tissue-specific enhancers and promoters Koch, Frederic; Fenouil, Romain; Gut, Marta Nature Structural & Molecular Biology, Vol. 18, Issue 8 https://doi.org/10.1038/nsmb.2085	journal	July 2011
CTCF-mediated chromatin looping in EGR2 regulation and SUZ12 recruitment critical for peripheral myelination and repair Wang, Jincheng; Wang, Jiajia; Yang, Lijun Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-17955-2	journal	August 2020
p63 regulates Satb1 to control tissue-specific chromatin remodeling during development of the epidermis Fessing, Michael Y.; Mardaryev, Andrei N.; Gdula, Michal R. Journal of Cell Biology, Vol. 194, Issue 6 https://doi.org/10.1083/jcb.201101148	journal	September 2011
The Role of Recombination Activating Gene (RAG) Reinduction in Thymocyte Development in Vivo Yannoutsos, Nikos; Wilson, Patrick; Yu, Wong Journal of Experimental Medicine, Vol. 194, Issue 4 https://doi.org/10.1084/jem.194.4.471	journal	August 2001
ENCODE Data in the UCSC Genome Browser: year 5 update Rosenbloom, Kate R.; Sloan, Cricket A.; Malladi, Venkat S. Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1172	journal	November 2012
In vivo live imaging of RNA polymerase II transcription factories in primary cells Ghamari, A.; van de Corput, M. P. C.; Thongjuea, S. Genes & Development, Vol. 27, Issue 7 https://doi.org/10.1101/gad.216200.113	journal	April 2013
FAIRE (Formaldehyde-Assisted Isolation of Regulatory Elements) isolates active regulatory elements from human chromatin Giresi, P. G.; Kim, J.; McDaniell, R. M. Genome Research, Vol. 17, Issue 6 https://doi.org/10.1101/gr.5533506	journal	June 2007
Real-Time Dynamics of RNA Polymerase II Clustering in Live Human Cells Cisse, I. I.; Izeddin, I.; Causse, S. Z. Science, Vol. 341, Issue 6146 https://doi.org/10.1126/science.1239053	journal	July 2013
The Organization of Replication and Transcription Cook, P. R. Science, Vol. 284, Issue 5421 https://doi.org/10.1126/science.284.5421.1790	journal	June 1999
Coordinate Regulation of RAG1 and RAG2 by Cell Type-Specific DNA Elements 5' of RAG2 Yu, W. Science, Vol. 285, Issue 5430 https://doi.org/10.1126/science.285.5430.1080	journal	August 1999
Satb1 Ablation Alters Temporal Expression of Immediate Early Genes and Reduces Dendritic Spine Density during Postnatal Brain Development Balamotis, M. A.; Tamberg, N.; Woo, Y. J. Molecular and Cellular Biology, Vol. 32, Issue 2 https://doi.org/10.1128/mcb.05917-11	journal	November 2011
Enhancer control of local accessibility to V(D)J recombinase. McMurry, M. T.; Hernandez-Munain, C.; Lauzurica, P. Molecular and Cellular Biology, Vol. 17, Issue 8 https://doi.org/10.1128/mcb.17.8.4553	journal	August 1997
V(D)J Recombination: Mechanisms of Initiation Schatz, David G.; Swanson, Patrick C. Annual Review of Genetics, Vol. 45, Issue 1 https://doi.org/10.1146/annurev-genet-110410-132552	journal	December 2011
Noncoding Transcription at Enhancers: General Principles and Functional Models Natoli, Gioacchino; Andrau, Jean-Christophe Annual Review of Genetics, Vol. 46, Issue 1 https://doi.org/10.1146/annurev-genet-110711-155459	journal	December 2012
SATB1 dictates expression of multiple genes including IL-5 involved in human T helper cell differentiation Ahlfors, Helena; Limaye, Amita; Elo, Laura L. Blood, Vol. 116, Issue 9 https://doi.org/10.1182/blood-2009-11-252205	journal	September 2010
An encyclopedia of mouse DNA elements (Mouse ENCODE) Stamatoyannopoulos, John A.; Snyder, Michael; Hardison, Ross Genome Biology, Vol. 13, Issue 8 https://doi.org/10.1186/gb-2012-13-8-418	journal	January 2012
Global Regulator SATB1 Recruits β-Catenin and Regulates TH2 Differentiation in Wnt-Dependent Manner Notani, Dimple; Gottimukkala, Kamalvishnu P.; Jayani, Ranveer S. PLoS Biology, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pbio.1000296	journal	January 2010
Long-Distance Regulation of Fetal V _δ Gene Segment TRDV4 by the Tcrd Enhancer Hao, Bingtao; Krangel, Michael S. The Journal of Immunology, Vol. 187, Issue 5 https://doi.org/10.4049/jimmunol.1100468	journal	July 2011
Chromatin Architecture, CCCTC-Binding Factor, and V(D)J Recombination: Managing Long-Distance Relationships at Antigen Receptor Loci Shih, Han-Yu; Krangel, Michael S. The Journal of Immunology, Vol. 190, Issue 10 https://doi.org/10.4049/jimmunol.1300218	journal	May 2013
Allele-Specific Regulation of TCRβ Variable Gene Segment Chromatin Structure Jackson, Annette M.; Krangel, Michael S. The Journal of Immunology, Vol. 175, Issue 8 https://doi.org/10.4049/jimmunol.175.8.5186	journal	October 2005
A tissue-specific MAR/SAR DNA-binding protein with unusual binding site recognition Dickinson, L. Cell, Vol. 70, Issue 4 https://doi.org/10.1016/0092-8674(92)90432-C	journal	August 1992
Essential Role of LAT in T Cell Development Zhang, Weiguo; Sommers, Connie L.; Burshtyn, Deborah N. Immunity, Vol. 10, Issue 3 https://doi.org/10.1016/S1074-7613(00)80032-1	journal	March 1999
A Conserved Transcriptional Enhancer Regulates RAG Gene Expression in Developing B Cells Hsu, Lih-Yun; Lauring, Josh; Liang, Hong-Erh Immunity, Vol. 19, Issue 1 https://doi.org/10.1016/S1074-7613(03)00181-X	journal	July 2003
Chromatin Architecture and the Generation of Antigen Receptor Diversity Jhunjhunwala, Suchit; van Zelm, Menno C.; Peak, Mandy M. Cell, Vol. 138, Issue 3 https://doi.org/10.1016/j.cell.2009.07.016	journal	August 2009
Functional and Mechanistic Diversity of Distal Transcription Enhancers Bulger, Michael; Groudine, Mark Cell, Vol. 144, Issue 3 https://doi.org/10.1016/j.cell.2011.01.024	journal	February 2011
Genome organizing function of SATB1 in tumor progression Kohwi-Shigematsu, Terumi; Poterlowicz, Krzysztof; Ordinario, Ellen Seminars in Cancer Biology, Vol. 23, Issue 2 https://doi.org/10.1016/j.semcancer.2012.06.009	journal	April 2013
Chromatin Architecture and the Generation of Antigen Receptor Diversity Jhunjhunwala, Suchit; van Zelm, Menno C.; Peak, Mandy M. Journal of End-to-End-testing, Vol. 138, Issue 3 https://doi.org/10.1016/s9999-9994(09)20396-5	journal	August 2009
A role for cohesin in T-cell-receptor rearrangement and thymocyte differentiation Seitan, Vlad C.; Hao, Bingtao; Tachibana-Konwalski, Kikuë Nature, Vol. 476, Issue 7361 https://doi.org/10.1038/nature10312	journal	August 2011
SATB1 packages densely looped, transcriptionally active chromatin for coordinated expression of cytokine genes Cai, Shutao; Lee, Charles C.; Kohwi-Shigematsu, Terumi Nature Genetics, Vol. 38, Issue 11 https://doi.org/10.1038/ng1913	journal	October 2006
Satb1 regulates the self-renewal of hematopoietic stem cells by promoting quiescence and repressing differentiation commitment Will, Britta; Vogler, Thomas O.; Bartholdy, Boris Nature Immunology, Vol. 14, Issue 5 https://doi.org/10.1038/ni.2572	journal	April 2013
Regulation of T cell receptor β allelic exclusion at a level beyond accessibility Jackson, Annette; Kondilis, Hrisavgi D.; Khor, Bernard Nature Immunology, Vol. 6, Issue 2 https://doi.org/10.1038/ni1157	journal	January 2005
Quantitative analysis of chromosome conformation capture assays (3C-qPCR) Hagège, Hélène; Klous, Petra; Braem, Caroline Nature Protocols, Vol. 2, Issue 7 https://doi.org/10.1038/nprot.2007.243	journal	July 2007
RAG2 is regulated differentially in B and T cells by elements 5' of the promoter Monroe, R. J.; Chen, F.; Ferrini, R. Proceedings of the National Academy of Sciences, Vol. 96, Issue 22 https://doi.org/10.1073/pnas.96.22.12713	journal	October 1999
The MAR-binding protein SATB1 orchestrates temporal and spatial expression of multiple genes during T-cell development Alvarez, John D.; Yasui, Dag H.; Niida, Hiroyuki Genes & Development, Vol. 14, Issue 5 https://doi.org/10.1101/gad.14.5.521	journal	March 2000
Satb1 and Satb2 regulate embryonic stem cell differentiation and Nanog expression Savarese, Fabio; Dávila, Amparo; Nechanitzky, Robert Genes & Development, Vol. 23, Issue 22 https://doi.org/10.1101/gad.1815709	journal	November 2009
Capturing Chromosome Conformation Dekker, J. Science, Vol. 295, Issue 5558 https://doi.org/10.1126/science.1067799	journal	February 2002
Satb1 Ablation Alters Temporal Expression of Immediate Early Genes and Reduces Dendritic Spine Density during Postnatal Brain Development Balamotis, M. A.; Tamberg, N.; Woo, Y. J. Molecular and Cellular Biology, Vol. 32, Issue 2 https://doi.org/10.1128/MCB.05917-11	journal	November 2011
Enhancer control of local accessibility to V(D)J recombinase. McMurry, M. T.; Hernandez-Munain, C.; Lauzurica, P. Molecular and Cellular Biology, Vol. 17, Issue 8 https://doi.org/10.1128/MCB.17.8.4553	journal	August 1997
Systemic Overexpression of BCL-2 in the Hematopoietic System Protects Transgenic Mice From the Consequences of Lethal Irradiation Domen, Jos; Gandy, Kimberly L.; Weissman, Irving L. Blood, Vol. 91, Issue 7 https://doi.org/10.1182/blood.V91.7.2272	journal	April 1998
Systemic Overexpression of BCL-2 in the Hematopoietic System Protects Transgenic Mice From the Consequences of Lethal Irradiation Domen, Jos; Gandy, Kimberly L.; Weissman, Irving L. Blood, Vol. 91, Issue 7 https://doi.org/10.1182/blood.v91.7.2272.2272_2272_2282	journal	April 1998
FAIRE (Formaldehyde-Assisted Isolation of Regulatory Elements) isolates active regulatory elements from human chromatin G., Giresi, P.; R., Iyer, V.; J., Kim, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/8cez-3e87	text	January 2007

Cited By (10)

Runx-mediated regulation of CCL5 via antagonizing two enhancers influences immune cell function and anti-tumor immunity Seo, Wooseok; Shimizu, Kanako; Kojo, Satoshi Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-15375-w	journal	March 2020
Hierarchical assembly and disassembly of a transcriptionally active RAG locus in CD4+CD8+ thymocytes Naik, Abani Kanta; Byrd, Aaron T.; Lucander, Aaron C. K. Journal of Experimental Medicine, Vol. 216, Issue 1 https://doi.org/10.1084/jem.20181402	journal	December 2018
Developmental conservation of microRNA gene localization at the nuclear periphery Salataj, Eralda; Stathopoulou, Chrysoula; Hafþórsson, Róbert A. PLOS ONE, Vol. 14, Issue 11 https://doi.org/10.1371/journal.pone.0223759	journal	November 2019
Transcription-coupled genetic instability marks acute lymphoblastic leukemia structural variation hotspots Heinäniemi, Merja; Vuorenmaa, Tapio; Teppo, Susanna eLife, Vol. 5 https://doi.org/10.7554/elife.13087	journal	July 2016
Core pluripotency factors promote glycolysis of human embryonic stem cells by activating GLUT1 enhancer Yu, Lili; Ji, Kai-yuan; Zhang, Jian Protein & Cell, Vol. 10, Issue 9 https://doi.org/10.1007/s13238-019-0637-9	journal	May 2019
Guidance of regulatory T cell development by Satb1-dependent super-enhancer establishment Kitagawa, Yohko; Ohkura, Naganari; Kidani, Yujiro Nature Immunology, Vol. 18, Issue 2 https://doi.org/10.1038/ni.3646	journal	December 2016
SATB family chromatin organizers as master regulators of tumor progression Naik, Rutika; Galande, Sanjeev Oncogene, Vol. 38, Issue 12 https://doi.org/10.1038/s41388-018-0541-4	journal	November 2018
SATB1 establishes ameloblast cell polarity and regulates directional amelogenin secretion for enamel formation Zhang, Yan; Zheng, Liwei; Le, Michael BMC Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s12915-019-0722-9	journal	December 2019
SATB1 Plays a Critical Role in Establishment of Immune Tolerance Kondo, Motonari; Tanaka, Yuriko; Kuwabara, Taku The Journal of Immunology, Vol. 196, Issue 2 https://doi.org/10.4049/jimmunol.1501429	journal	December 2015
Transcription-coupled genetic instability marks acute lymphoblastic leukemia structural variation hotspots Heinäniemi, Merja; Vuorenmaa, Tapio; Teppo, Susanna eLife, Vol. 5 https://doi.org/10.7554/eLife.13087	journal	July 2016

Similar Records

Crystal structure of the V(D)J recombinase RAG1–RAG2

Journal Article · Tue Feb 17 19:00:00 EST 2015 · Nature (London) · OSTI ID:1247328

The MAR-binding protein SATB1 orchestrates temporal and spatial expression of multiple genes during T-cell development

Journal Article · Wed Feb 23 23:00:00 EST 2000 · Genes & Development · OSTI ID:771795

Regulation of early T cell development by the PHD finger of histone lysine methyltransferase ASH1

Journal Article · Thu Jan 17 23:00:00 EST 2008 · Biochemical and Biophysical Research Communications · OSTI ID:21043580

Related Subjects

histone H3 lysine 27 trimethylation
variable, diversity, and joining gene segment
60 APPLIED LIFE SCIENCES
ChIP-sequencing
RNA polymerase II
anti-silencer element
bacterial artificial chromosome
chromatin immunoprecipitation
chromosome conformation capture
double positive
formaldehyde-assisted isolation of regulatory elements
histone H3 lysine 27 acetylation
histone H3 lysine 4 monomethylation
histone H3 lysine 4 trimethylation
recombination activating gene
recombination signal sequence
single positive
special AT-rich binding protein 1

An anti-silencer– and SATB1-dependent chromatin hub regulates Rag1 and Rag2 gene expression during thymocyte development

Citation Formats

References (66)

Cited By (10)

Similar Records

Related Subjects