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A map of the cis-regulatory sequences in the mouse genome
Open accessAbstract
The laboratory mouse is the most widely used mammalian model organism in biomedical research. The 2.6 × 10(9) bases of the mouse genome possess a high degree of conservation with the human genome, so a thorough annotation of the mouse genome will be of significant value to understanding the function of the human genome. So far, most of the functional sequences in the mouse genome have yet to be found, and the cis-regulatory sequences in particular are still poorly annotated. Comparative genomics has been a powerful tool for the discovery of these sequences, but on its own it cannot resolve their temporal and spatial functions. Recently, ChIP-Seq has been developed to identify cis-regulatory elements in the genomes of several organisms including humans, Drosophila melanogaster and Caenorhabditis elegans. Here we apply the same experimental approach to a diverse set of 19 tissues and cell types in the mouse to produce a map of nearly 300,000 murine cis-regulatory sequences. The annotated sequences add up to 11% of the mouse genome, and include more than 70% of conserved non-coding sequences. We define tissue-specific enhancers and identify potential transcription factors regulating gene expression in each tissue or cell type. Finally, we show that much of the mouse genome is organized into domains of coordinately regulated enhancers and promoters. Our results provide a resource for the annotation of functional elements in the mammalian genome and for the study of mechanisms regulating tissue-specific gene expression.
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“Furthermore, an analysis of publically available DNase I hypersensitivity data (Shen et al., 2012) confirmed that >60% of embryonic sites remain accessible in the adult liver (data not shown).”
From Hippo Signaling Influences HNF4A and FOXA2 Enhancer Switching during Hepatocyte Differentiation (2014) · cites this paper as Shen et al., 2012
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“…interactions (topological domains) are a common feature of the mouse and human ES cell genome (Dixon et al., 2012; Nora et al., 2012) and have been proposed to form “enhancer–promoter units,” in which genes and their cell type-specific enhancers are contained (Nora et al., 2012; Shen et al., 2012).”
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The transcriptomic and epigenetic map of vascular quiescence in the continuous lung endothelium
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“(c) The H3K4me1, H3K27ac [31], cohesin, and CTCF [22] ChIP-Seq signals around 97 Bmal1 super-enhancers.”
MethodChoukrallah, M.-A., Song, S., Rolink, A. G., Burger, L., & Matthias, P. (2015) · Nature Communications · doi:10.1038/ncomms9324 · Cited by 54
“The enhancer landscape is largely shaped by the cooperative binding of ubiquitous and cell type-specific TFs 4,27 .”
Jiang, J. (2015) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2015.01.005 · Cited by 57
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“…and CBP/p300 binding are other distinctive features of active enhancers (Kim et al., 2010; Visel et al., 2013) Tissue- and cell typespecific signatures of active enhancers were identified by genomic studies comparing many tissues and cell types (Shen et al., 2012, Thurman et al., 2012).”
BackgroundA WIZ/Cohesin/CTCF Complex Anchors DNA Loops to Define Gene Expression and Cell Identity
Justice, M., Carico, Z. M., Stefan, H. C., & Dowen, J. M. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.03.067 · Cited by 51
“%) across these tissues overlap with conserved CTCF peaks in these tissues (Figure S1F) (Isbel et al., 2016; Shen et al., 2012).”
McEnhancer: predicting gene expression via semi-supervised assignment of enhancers to target genes
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“We focus our efforts on fly embryonic enhancers: The fly genome is compact, such that enhancers are frequently close to multiple genes (e.g., within a few kilobases), and one can therefore not assume that the closest promoter is always the correct one [27, 28].”
BackgroundResultPoterlowicz, K., Yarker, J. L., Malashchuk, I., Lajoie, B. R., Mardaryev, A. N., Gdula, M. R., Sharov, A. A., Kohwi-shigematsu, T., Botchkarev, V. A., & Fessing, M. Y. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006966 · Cited by 48
“ChIP-seq analyses revealed 16 regions in the EDC locus and its neighbouring regions with the high levels of both H3K4me1 and H3K27ac modifications, serving as the signatures of active enhancers [3, 47, 48] (Fig 3C, S11 Table).”
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“In addition, CTCF was observed to localize at tissue-specific enhancer elements [74,75], suggesting a role for CTCF in mediating physical interactions between DNA regulatory elements and in driving the chromosomal conformation that is necessary for cell type specification.”
BackgroundRegulation and Function of the Peg3 Imprinted Domain
He, H., & Kim, J. (2014) · Genomics & Informatics · doi:10.5808/gi.2014.12.3.105 · Cited by 49
“This prediction has been recently confirmed through the epigenomic results in which the majority of these ECRs is associated with two histone modifications, H3K4me1 and H3K27ac (monomethylation of lysine 4 and acetylation of lysine 27, respectively, of histone 3) [16], which are closely associated with enhancers [17].”
BackgroundHNF4A modulates glucocorticoid action in the liver
Hunter, A. L., Poolman, T. M., Kim, D., Gonzalez, F. J., Bechtold, D. A., Loudon, A. S. I., Iqbal, M., & Ray, D. W. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110697 · Cited by 49
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Reorganized 3D Genome Structures Support Transcriptional Regulation in Mouse Spermatogenesis
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“To test the functional roles of the most abundant loops formed in SZ, we used ChIP-seq data of histone marks and RNA Pol II binding in testis from previous reports (Shen et al., 2012) to annotate potential enhancers.”
MethodMechanism governing a stem cell-generating cis -regulatory element
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“LZK is normally expressed in the CNS of embryonic and adult mice based on mouse transcriptomic data (Shen et al., 2012).”
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“The distribution of CTCF (p-value 1 }10−5) in untreated CTCF-AID cells resembles that of normal ES cells (Shen et al., 2012), indicating that AID fusion does not affect its DNA binding (Figure S1C).”
BackgroundSelf-citationEvolution of mammalian sound localization circuits: A developmental perspective
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“RELATED INFORMATION ChIP-Seq has been used extensively to study genome-wide histone modification profiles and transcription factor occupancy in cultured human and murine cells (Neph et al. 2012; Thurman et al. 2012; Shen et al. 2012).”
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Identical cells with different 3D genomes; cause and consequences?
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Transcriptional regulatory network controlling the ontogeny of hematopoietic stem cellsPreprint
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“enhancers from 19 non-hematopoietic cell lines reported by the ENCODE project (Shen et al., 2012) (brown adipose tissue, brain (E14.”
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HiPiler: Visual Exploration of Large Genome Interaction Matrices with Interactive Small Multiples
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Enhancers reside in a unique epigenetic environment during early zebrafish development
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A discrete chromatin loop in the murine Tcra-Tcrd locus shapes the TCRδ and TCRα repertoires
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Grabbing the genome by the NADs
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Hi-C Chromatin Interaction Networks Predict Co-expression in the Mouse Cortex
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“So, the resulting genome-wide interactions are averaged across the cells and are not exactly the same in any given cell [8, 26].”
BackgroundMethodInfluentialEndoplasmic reticulum stress actively suppresses hepatic molecular identity in damaged liver
Dubois, V., Gheeraert, C., Vankrunkelsven, W., Dubois‐Chevalier, J., Dehondt, H., Bobowski‐Gerard, M., Vinod, M., Zummo, F. P., Güiza, F., Ploton, M., et al. (2020) · Molecular Systems Biology · doi:10.15252/msb.20199156 · Cited by 46
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“Notably, comparison with those from a panel of tissues ( n = 94) from ENCODE 30 showed oocytes possessed a large fraction of unique enhancers ( n = 31,838, 47.7%), in contrast to pre-implantation embryos ( n = 6,581, 9.7”
InfluentialTranscriptional mechanisms of pancreatic β-cell maturation and functional adaptation
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Spectacle: fast chromatin state annotation using spectral learning
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“Several computational methods have been developed to annotate chromatin states from epigenomic data, not only in the human genome but also in the Drosophila, mouse, yeast and Arabidopsis thaliana genomes [15-27].”
MethodA mechanistic link between gene regulation and genome architecture in mammalian development
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“To explore whether the poised KO-H3K4me1 sites seen to partially overlap with enhancers present in brain tissue could indeed switch to an active enhancer state on neuronal differentiation in vitro, we examined the acquisition of H3K27ac, which is considered indicative for functionally active enhancers (20).”
BackgroundMethodInfluentialSnapATAC: A Comprehensive Analysis Package for Single Cell ATAC-seqPreprint
Fang, R.-X., Preissl, S., Li, Y., Hou, X.-M., Lucero, J., Wang, X.-X., Motamedi, A., Shiau, A., Zhou, X.-Z., Xie, F.-M., et al. (2019) · bioRxiv · doi:10.1101/615179 · Cited by 44
“Specifically, we monitor the running time for 1) TF1216 IDF transformation and Singular Value Decomposition (SVD) for LSA, 2) function 1217 “runModels” with topics = c(2, 5, 10, 15, 20, 25, 30, 35, 40) and “selectModel” function in 1218 cisTopic.”
MethodSelf-citationRepression and 3D-restructuring resolves regulatory conflicts in evolutionarily rearranged genomes
Ringel, A. R., Szabo, Q., Chiariello, A. M., Chudzik, K., Schöpflin, R., Rothe, P., Mattei, A. L., Zehnder, T., Harnett, D., Laupert, V., et al. (2022) · Cell · doi:10.1016/j.cell.2022.09.006 · Cited by 50
Global Analysis of Enhancer Targets Reveals Convergent Enhancer-Driven Regulatory Modules
Xie, S., Armendariz, D. A., Zhou, P., Duan, J., & Hon, G. C. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.10.073 · Cited by 46
“…the direct target genes of enhancers, using methods including computational correlation of epigenetic modifications (Andersson et al., 2014; Shen et al., 2012), three-dimensional chromatin looping (Fang et al., 2016; Mumbach et al., 2016), and high-throughput perturbation of enhancers…”
MethodEpigenetic memory: A macrophage perspective
Logie, C., & Stunnenberg, H. G. (2016) · Seminars in Immunology · doi:10.1016/j.smim.2016.06.003 · Cited by 44
“‘enhancers’ modulate the activity of the promoters [12,13].”
The nuclear periphery is a scaffold for tissue-specific enhancers
Smith, C. L., Poleshko, A., & Epstein, J. A. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab392 · Cited by 44
Decoding enhancer complexity with machine learning and high-throughput discovery
Smith, G. D., Ching, W. H., Cornejo‐Páramo, P., & Wong, E. S. W. (2023) · Genome biology · doi:10.1186/s13059-023-02955-4 · Cited by 48
“This “enhancer real estate” is significantly larger than the 2% of the genome that comprises of protein-coding genes [9–15] (Fig.”
BackgroundMarino, M. M., Rega, C., Russo, R., Valletta, M., Gentile, M. T., Esposito, S., Baglivo, I., Feis, I. D., Angelini, C., Xiao, T., et al. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.004882 · Cited by 50
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Meis1 coordinates a network of genes implicated in eye development and microphthalmia
Marcos, S., González‐Lázaro, M., Beccari, L., Carramolino, L., Martín-Bermejo, M. J., Amarie, O., Martín, D. M.-S., Torroja, C., Bogdanović, O., Doohan, R., et al. (2015) · Development · doi:10.1242/dev.122176 · Cited by 43
Tissue-specific targeting of cell fate regulatory genes by E2f factors
Julian, L. M., Liu, Y., Pakenham, C. A., Dugal-Tessier, D., Ruzhynsky, V., Bae, S., Tsai, S.-Y., Leone, G. W., Slack, R. S., & Blais, A. (2015) · Cell Death and Differentiation · doi:10.1038/cdd.2015.36 · Cited by 46
“Importantly, we have previously demonstrated that loss of either E2f3 isoform in NPCs does not result in altered expression or a perceivable change in DNA-binding capacity of the other isoform, nor of other E2f factors.8 We identified 3144 enriched peaks (2979 genes) in E2f3a-deficient cells, indicating that E2f3b is…”
BackgroundMethodInfluentialHEB associates with PRC2 and SMAD2/3 to regulate developmental fates
Yoon, S.-J., Foley, J. W., & Baker, J. (2015) · Nature Communications · doi:10.1038/ncomms7546 · Cited by 43
“All rights reserved. members of the Hox (38) and Fox (19) gene families, which are not found in the gene set marked by PRC2 alone (Fig.”
BackgroundInfluentialThe 3D enhancer network of the developing T cell genome is shaped by SATB1
Ζελένκα, Τ., Klonizakis, A., Tsoukatou, D., Papamatheakis, D.-A., Franzenburg, S., Tzerpos, P., Tzonevrakis, I.-R., Papadogkonas, G., Kapsetaki, M., Nikolaou, C., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-34345-y · Cited by 50
Evolution of mouse circadian enhancers from transposable elements
Judd, J., Sanderson, H., & Feschotte, C. (2021) · Genome biology · doi:10.1186/s13059-021-02409-9 · Cited by 40
The Role of Insulation in Patterning Gene Expression
Özdemir, I., & Gambetta, M. C. (2019) · Genes · doi:10.3390/genes10100767 · Cited by 50
“The gene regulatory functions of mammalian TADs are discussed in Section 4, but they are generally viewed as basic structural and functional units in which genes are coordinately regulated [64,80].”
BackgroundCis-Regulatory Code for Predicting Plant Cell-Type Transcriptional Response to High Salinity
Uygun, S., Azodi, C. B. D., & Shiu, S. (2019) · PLANT PHYSIOLOGY · doi:10.1104/pp.19.00653 · Cited by 42
Martinez, M. E., Duarte, C. W., Stohn, J. P., Karaczyn, A. A., Wu, Z.-F., Demambro, V. E., & Hernandez, A. (2018) · Molecular Psychiatry · doi:10.1038/s41380-018-0281-4 · Cited by 42
Lsh/HELLS regulates self-renewal/proliferation of neural stem/progenitor cells
Han, Y., Ren, J., Lee, E. Y., Xu, X., Yu, W., & Muegge, K. (2017) · Scientific Reports · doi:10.1038/s41598-017-00804-6 · Cited by 38
Simultaneous mapping of active DNA demethylation and sister chromatid exchange in single cellsPreprint
Wu, X., Inoue, A., Suzuki, T., & Zhang, Y. (2017) · Genes & Development · doi:10.1101/gad.294843.116 · Cited by 49
“…Supplemental Figures S1 and S2, we used the following published data sets of mouse ES cells: H3K4me1 (Meissner et al. 2008), H3K27ac (Creyghton et al. 2010), mouse ES cell enhancers (Shen et al. 2012), 5hmC DIP (Wu et al. 2011), 5fC DIP, 5caC DIP (Shen et al. 2013), and WGMAB-seq (Wu et al. 2014).”
MethodHematopoietic Signaling Mechanism Revealed from a Stem/Progenitor Cell Cistrome
Hewitt, K. J., Kim, D. H., Devadas, P., Prathibha, R., Zuo, C., Sanalkumar, R., Johnson, K. D., Kang, Y.-A., Kim, J., Dewey, C. N., et al. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.05.020 · Cited by 42
“, 2012), as well as 76 histonemodification and 38 chromatin occupancy datasets (Shen et al., 2012b).”
Birnbaum, R. Y., Patwardhan, R. P., Kim, M. J., Findlay, G. M., Martin, B., Zhao, J., Bell, R. J. A., Smith, R. P., Ku, A. A., Shendure, J., et al. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004592 · Cited by 40
Luyten, A., Zang, C., Liu, X. S., & Shivdasani, R. A. (2014) · Genes & Development · doi:10.1101/gad.240101.114 · Cited by 45
“Lineage-specific gene activity in vivo requires ciselements that lie far from transcription start sites (TSSs) (Heintzman et al. 2007) and show dynamic changes in nuclease sensitivity (Stergachis et al. 2013), histone modification (Shen et al. 2012; Zhu et al. 2013), and TF binding.”
BackgroundWijetunga, N. A., Delahaye, F., Zhao, Y. M., Golden, A., Mar, J. C., Einstein, F. H., & Greally, J. M. (2014) · Nature Communications · doi:10.1038/ncomms6195 · Cited by 39
Bhatia, S., & Kleinjan, D. A. (2014) · Human Genetics · doi:10.1007/s00439-014-1424-6 · Cited by 42
A novel regulatory element for Shh expression in the lung and gut of mouse embryos
Tsukiji, N., Amano, T., & Shiroishi, T. (2013) · Mechanisms of Development · doi:10.1016/j.mod.2013.09.003 · Cited by 38
“Histone H3 mono-methylation at lysine 4 (H3K4me1) indicate active enhancers (Heintzman et al., 2009; Hon et al., 2009; Shen et al., 2012).”
Enhancer turnover and conserved regulatory function in vertebrate evolution
Domené, S., Bumaschny, V. F., de Souza, F. S. J., Franchini, L. F., Nasif, S., Low, M. J., & Rubinstein, M. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0027 · Cited by 45
Shih, H., & Krangel, M. S. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1300218 · Cited by 42
Readout of histone methylation by Trim24 locally restricts chromatin opening by p53
Isbel, L., Iskar, M., Durdu, S., Weiss, J., Grand, R. S., Hietter-Pfeiffer, E., Kozicka, Z., Michael, A. K., Burger, L., Thomä, N. H., et al. (2023) · Nature Structural & Molecular Biology · doi:10.1038/s41594-023-01021-8 · Cited by 41
Long genes linked to autism spectrum disorders harbor broad enhancer-like chromatin domainsPreprint
Zhao, Y.-T., Kwon, D. Y., Johnson, B. S., Fasolino, M., Lamonica, J. M., Kim, Y. J., Zhao, B. S., He, C., Vahedi, G., Kim, T. H., et al. (2018) · Genome Research · doi:10.1101/gr.233775.117 · Cited by 36
“by Hi-C profiling in the cortex of 8-wk-old male mice (Shen et al. 2012).”
BackgroundMethodInfluentialMylonas, C., & Tessarz, P. (2018) · Life Science Alliance · doi:10.26508/lsa.201800085 · Cited by 43
Phf8 loss confers resistance to depression-like and anxiety-like behaviors in mice
Walsh, R. M., Shen, E., Bagot, R. C., Anselmo, A. N., Jiang, Y., Javidfar, B., Wojtkiewicz, G. R., Cloutier, J. K., Chen, J. W., Sadreyev, R. I., et al. (2017) · Nature Communications · doi:10.1038/ncomms15142 · Cited by 46
Maury, E., & Hashizume, R. (2017) · Epigenetics · doi:10.1080/15592294.2016.1278095 · Cited by 50
“signals at enhancers can regulate tissue-specific expression patterns during development.(18) Some of these marks have been identified as a chromatin signature linked to transcriptional”
BackgroundGenome-wide identification of regulatory elements in Sertoli cells
Maatouk, D. M., Natarajan, A., Shibata, Y., Song, L., Crawford, G. E., Ohler, U., & Capel, B. (2017) · Development · doi:10.1242/dev.142554 · Cited by 45
“CTCF overlap We used previously published CTCF ChIP-seq datasets (Shen et al., 2012) and compared these against Sertoli-unique, Sertoli-specific and Sertolicommon DHSs using BedTools.”
BackgroundMethodResultInfluentialEtiology and pathogenesis of the cohesinopathies
Zakari, M., Yuen, K. C. Y., & Gerton, J. L. (2015) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.190 · Cited by 41
Eukaryotic enhancers: common features, regulation, and participation in diseases
Erokhin, M., Vassetzky, Y. S., Georgiev, P. G., & Chetverina, D. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-1871-9 · Cited by 54
“Indeed, the DNA sequences predicted as enhancers by enrichment of H3K4me1 and p300 and depletion of H3K4me3 gives over 75 % of positives in a functional test [62, 101].”
BackgroundFunctional Interactions between NURF and Ctcf Regulate Gene Expression
Qiu, Z., Song, C., Malakouti, N., Murray, D. T., Hariz, A., Zimmerman, M., Gygax, D. M., Alhazmi, A., & Landry, J. W. (2014) · Molecular and Cellular Biology · doi:10.1128/mcb.00553-14 · Cited by 33
Epigenetic Mechanisms in Heart Failure Pathogenesis
Salvo, T. G. D., & Haldar, S. M. (2014) · Circulation Heart Failure · doi:10.1161/circheartfailure.114.001193 · Cited by 38
Bunina, D., Abazova, N., Diaz, N. S., Noh, K., Krijgsveld, J., & Zaugg, J. B. (2020) · Cell Systems · doi:10.1016/j.cels.2020.05.003 · Cited by 39
“5 brain data from Shen et al., 2012).”
BackgroundInfluentialMechanistic insights into acephalic spermatozoa syndrome–associated mutations in the human SUN5 gene
Shang, Y.-L., Yan, J., Tang, W.-H., Liu, C., Xiao, S., Guo, Y.-S., Yuan, L., Chen, L., Jiang, H., Guo, X.-J., et al. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra117.000861 · Cited by 40
“Testis-specific gene annotation was from previous published data (24).”
BackgroundIncorporation of histone H3.1 suppresses the lineage potential of skeletal muscle
Harada, A., Maehara, K., Sato, Y., Konno, D., Tachibana, T., Kimurâ, H., & Ohkawa, Y. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku1346 · Cited by 49
Ito, S., Magalska, A., Alcaraz-Iborra, M., López-Atalaya, J., Rovira, V., Contreras-Moreira, B., Lipiński, M., Olivares, R., Martínez-Hernández, J., Ruszczycki, B., et al. (2014) · Nature Communications · doi:10.1038/ncomms5450 · Cited by 40
Epigenetic-based therapies for Friedreich ataxia
Sandi, C., Sandi, M., Virmouni, S. A., Al-Mahdawi, S., & Pook, M. A. (2014) · Frontiers in Genetics · doi:10.3389/fgene.2014.00165 · Cited by 42
The HASTER lncRNA promoter is a cis-acting transcriptional stabilizer of HNF1A
Beucher, A., Miguel-Escalada, I., Balboa, D., Vas, M. G. D., Maestro, M. A., García-Hurtado, J., Bernal, A., Gonzalez-Franco, R., Vargiu, P., Heyn, H., et al. (2022) · Nature Cell Biology · doi:10.1038/s41556-022-00996-8 · Cited by 42
Transcriptional Regulation and Implications for Controlling Hox Gene Expression
Afzal, Z., & Krumlauf, R. K. (2022) · Journal of Developmental Biology · doi:10.3390/jdb10010004 · Cited by 51
“Since then, a variety of analyses have revealed that animal genomes contain a large number of putative enhancers, out numbering coding genes [51,52].”
BackgroundChen, L., Toke, N. H., Luo, S., Vasoya, R. P., Aita, R., Parthasarathy, A., Tsai, Y.-H., Spence, J. R., & Verzi, M. P. (2019) · Development · doi:10.1242/dev.179432 · Cited by 50
Holo-Seq: single-cell sequencing of holo-transcriptome
Xiao, Z., Cheng, G., Yang, J., Pan, C., Li, R., Jia, D., Zhu, J., Wu, C., Zheng, M., & Jia, J. (2018) · Genome biology · doi:10.1186/s13059-018-1553-7 · Cited by 46
“gov/sra under accession numbers SRP006786 [55], SRP000712 [56], SRP026197 [18], SRP028301 [6], SRP071245 [23], SRP034543 [22], and SRP074776 [29].”
Two independent modes of chromosome organization are revealed by cohesin removalPreprint
Schwarzer, W., Abdennur, N., Goloborodko, A., Pękowska, A., Fudenberg, G., Loe-Mie, Y., Fonseca, N. A., Huber, W., Haering, C., Mirny, L., et al. (2016) · bioRxiv · doi:10.1101/094185 · Cited by 39
Vitamin D-dependent chromatin association of CTCF in human monocytes
Neme, A., Seuter, S., & Carlberg, C. (2016) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2016.08.008 · Cited by 46
The role of loops on the order of eukaryotes and prokaryotes
Hofmann, A., & Heermann, D. W. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.04.021 · Cited by 35
Battistelli, C., Busanello, A., & Maione, R. (2014) · Journal of Cell Science · doi:10.1242/jcs.149427 · Cited by 39
“CTCF is a ubiquitously expressed factor and binds genomewide in a conserved fashion in different cell types (Barski et al., 2007; Kim et al., 2007; Shen et al., 2012).”
Background
Metadata
- Authors
- Shen, Y., Yue, F., McCleary, D. F., Ye, Z., Edsall, L., Kuan, S., Wagner, U., Dixon, J., Lee, L., Lobanenkov, V. V., & Ren, B.
- Affiliations
- Ludwig Cancer Research (US)
- University of California San Diego (US)
- National Institutes of Health (US)
- Corresponding author
- Ren, Bing
- ORCID
- Venue
- Nature
- Published
- 2012-07-01
- Volume
- 488
- Issue
- 7409
- Pages
- 116-120
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4041622
- OpenAlex
- W2042930277
- Cited by
- 1,361
- References
- 29
- Citations by year
- 2026: 12 · 2025: 24 · 2024: 51 · 2023: 75 · 2022: 88 · 2021: 119 · 2020: 90 · 2019: 107 · 2018: 97 · 2017: 110 · 2016: 125 · 2015: 137 · 2014: 167 · 2013: 132 · 2012: 26
- FWCI
- 59.44
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Human Genome Research Institute (R01HG003991)
- National Institute of General Medical Sciences (T32GM007198)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- cis-regulatory sequences, mouse genome, enhancers, promoter, CTCF binding sites, tissue-specific gene expression, transcription factor binding, conserved non-coding elements, genome annotation, ChIP-seq
- MeSH terms
- Acetylation, Animals, Chromatin, Enhancer Elements, Genetic, Gene Expression Regulation, Male, Methylation, Mice, Inbred C57BL, Organ Specificity, Promoter Regions, Genetic, Regulatory Sequences, Nucleic Acid, Transcription Factors, Genome, Conserved Sequence, Sequence Analysis, DNA, Evolution, Molecular, Physical Chromosome Mapping, Chromatin Immunoprecipitation, Mice, Molecular Sequence Annotation, Nucleotide Motifs
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