The DOI matches its Crossref record; 29 of the 29 references it cites were found in a registry or an index.
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The check wasn’t confident either way, so it gives no verdict — never disputed.
In the citing paper
“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
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Comprehensive Mapping of Long-Range Interactions Reveals Folding Principles of the Human Genome
Lieberman-Aiden, E., van Berkum, N. L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A., Amit, I., Lajoie, B. R., Sabo, P. J., Dorschner, M. O., et al. (2009) · Science · doi:10.1126/science.1181369 · Cited by 8,898
Initial sequencing and comparative analysis of the mouse genome
Mouse Genome Sequencing Consortium (2002) · Nature · doi:10.1038/nature01262 · Cited by 7,187
High-Resolution Profiling of Histone Methylations in the Human Genome
Barski, A., Cuddapah, S., Cui, K., Roh, T.-Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I., & Zhao, K. (2007) · Cell · doi:10.1016/j.cell.2007.05.009 · Cited by 6,845
Topological domains in mammalian genomes identified by analysis of chromatin interactions
Dixon, J. R., Selvaraj, S., Yue, F., Kim, A., Li, Y., Shen, Y., Hu, M., Liu, J. S., & Ren, B. (2012) · Nature · doi:10.1038/nature11082 · Cited by 6,829
Self-citationThe ENCODE Project Consortium (2007) · Nature · doi:10.1038/nature05874 · Cited by 5,223
Histone H3K27ac separates active from poised enhancers and predicts developmental state
Creyghton, M. P., Cheng, A. W., Welstead, G. G., Kooistra, T., Carey, B. W., Steine, E. J., Hanna, J., Lodato, M. A., Frampton, G. M., Sharp, P. A., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1016071107 · Cited by 4,302
Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes
Siepel, A., Bejerano, G., Pedersen, J. S., Hinrichs, A. S., Hou, M., Rosenbloom, K., Clawson, H., Spieth, J., Hillier, L. W., Richards, S., et al. (2005) · Genome Research · doi:10.1101/gr.3715005 · Cited by 3,971
Heintzman, N. D., Stuart, R. K., Hon, G., Fu, Y., Ching, C. W., Hawkins, R. D., Barrera, L. O., Van Calcar, S., Qu, C., Ching, K. A., et al. (2007) · Nature Genetics · doi:10.1038/ng1966 · Cited by 3,398
Self-citationPruitt, K., Tatusova, T., & Maglott, D. (2004) · Nucleic Acids Res. · doi:10.1093/nar/gki025 · Cited by 3,248
Mapping and analysis of chromatin state dynamics in nine human cell types
Ernst, J., Kheradpour, P., Mikkelsen, T. S., Shoresh, N., Ward, L. D., Epstein, C. B., Zhang, X., Wang, L., Issner, R., Coyne, M., et al. (2011) · Nature · doi:10.1038/nature09906 · Cited by 2,898
Flagged first, then by citations
Research works printed but not linked: 2
Cited by
Sorted by citations
Items 701–800 of 1,005
Zouari, Y. B., Molitor, A., Sikorska, N., Pancaldi, V., & Sexton, T. (2018) · Genome Biology · doi:10.1186/s13059-019-1706-3 · Cited by 27
Dynamic Long-Range Chromatin Interaction Controls Expression of IL-21 in CD4+ T Cells
Park, J., Choi, Y., Song, M., Park, K., Lee, J., & Kim, H. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1500636 · Cited by 26
3D genome architecture from populations to single cells
Furlan-Magaril, M., Várnai, C., Nagano, T., & Fraser, P. (2015) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2015.04.004 · Cited by 29
Computational schemes for the prediction and annotation of enhancers from epigenomic assays
Whitaker, J. W., Nguyen, T. T., Zhu, Y., Wildberg, A., & Wang, W. (2014) · Methods · doi:10.1016/j.ymeth.2014.10.008 · Cited by 26
Fine Tuning of Craniofacial Morphology by Distant-Acting Enhancers
Attanasio, C., Nord, A. S., Zhu, Y., Blow, M. J., Li, Z., Liberton, D. K., Morrison, H., Plajzer-Frick, I., Holt, A., Hosseini, R., et al. (2013) · Science · doi:10.1126/science.1241006 · Cited by 244
Self-citationMaternal oxycodone treatment causes pathophysiological changes in the mouse placenta
Green, M. T., Martin, R. E., Kinkade, J. A., Schmidt, R., Bivens, N. J., Tuteja, G., Mao, J., & Rosenfeld, C. S. (2020) · Placenta · doi:10.1016/j.placenta.2020.08.006 · Cited by 34
“We used the mouse ENCODE [42] dataset to carry out the enrichment analysis with default settings.”
MethodTissières, V., Geier, F. M., Keßler, B., Wolf, E., Zeller, R., & López-Rı́os, J. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.03.054 · Cited by 27
“Genome-wide functional genomics approaches allow for systematic cataloging of cis-regulatory elements (CREs) that interact and are regulated by transcriptional regulators that are ultimately responsible for wiring these GRNs (Osterwalder et al., 2014; Shen et al., 2012; Yue et al., 2014).”
BackgroundFunctional genomic approaches to elucidate the role of enhancers during development
Ryan, G. E., & Farley, E. K. (2019) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1467 · Cited by 22
“Together, H3K4me1 and H3K27ac are widely used to predict active enhancers (Bonn et al., 2012; Kharchenko et al., 2011; Rada-Iglesias et al., 2011; Shen et al., 2012; Wamstad et al., 2012).”
BackgroundAn enhancer cluster controls gene activity and topology of the SCN5A-SCN10A locus in vivo
Man, J. C. K., Mohan, R. A., van den Boogaard, M., Hilvering, C. R. E., Jenkins, C., Wakker, V., Bianchi, V., de Laat, W. L., Barnett, P., Boukens, B. J., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12856-5 · Cited by 43
Vojnits, K., Mahammad, S., Collins, T. J., & Bhatia, M. (2019) · Stem Cells Translational Medicine · doi:10.1002/sctm.19-0054 · Cited by 29
Gene expression dysregulation domains are not a specific feature of Down syndrome
Ahlfors, H., Anyanwu, N., Pakanavicius, E., Dinischiotu, N., Lana‐Elola, E., Watson-Scales, S., Tosh, J., Wiseman, F. K., Briscoe, J., Page, K. M., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-10129-9 · Cited by 26
Barnea, O. Y., Valensisi, C., Jayavelu, N. D., Kishore, K., Andrus, C. R., Koffler-Brill, T., Ushakov, K., Perl, K., Noy, Y., Bhonker, Y., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-35587-x · Cited by 29
Ye, Y., Gao, L., & Zhang, S. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz201 · Cited by 27
“edu/ENCODE/), including the architectural protein CTCF, seven histone modifications (H3K4me3, H3K9ac, H3K36me3, H3K4me1, H3K27ac, H3K27me3, H3K9me3), RNA Polymerase II, EP300, DNase-seq and RNA-seq data from (23).”
BackgroundPegolo, S., Dadousis, C., Mach, N., Ramayo‐Caldas, Y., Mele, M. L., Conte, G., Schiavon, S., Bittante, G., & Cecchinato, A. (2017) · Scientific Reports · doi:10.1038/s41598-017-17434-7 · Cited by 38
Anil, A., Spalinskas, R., Åkerborg, Ö., & Sahlén, P. (2017) · Bioinformatics · doi:10.1093/bioinformatics/btx625 · Cited by 27
“Promoters play a pivotal role in regulating expression levels of the corresponding genes (Smale and Kadonaga, 2003).”
BackgroundAlternative SET/TAFI Promoters Regulate Embryonic Stem Cell Differentiation
Edupuganti, R. R., Harikumar, A., Aaronson, Y., Biran, A., Sailaja, B. S., Nissim‐Rafinia, M., Azad, G. K., Cohen, M. A., Park, J. E., Shivalila, C., et al. (2017) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.08.021 · Cited by 25
“Finally, RNA sequencing (RNA-seq) tracks from ESCs and mouse embryonic fibroblasts (MEFs) from different sources (Shen et al., 2012; Yue et al., 2014) provided further support for the SETa/SETb isoform switch between ESCs and MEFs at the RNA level (Figure 1H).”
Nuclease Footprints in Sperm Project Past and Future Chromatin Regulatory Events
Johnson, G. D., Jodar, M., Piqué-Regi, R., & Krawetz, S. A. (2016) · Scientific Reports · doi:10.1038/srep25864 · Cited by 35
Moisan, S., Berlivet, S., Ka, C., Gac, G. L., Dostie, J., & Férec, C. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1300 · Cited by 26
Thiaville, M. M., Kim, H., Frey, W. D., & Kim, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0075417 · Cited by 26
Statistical analysis of ChIP-seq data with MOSAiCS.
Sun, G., Chung, D., Liang, K., & Keleş, S. (2013) · Methods in molecular biology · doi:10.1007/978-1-62703-514-9_12 · Cited by 26
Matsuwaka, M., Kumon, M., & Inoue, A. (2024) · Nature Cell Biology · doi:10.1038/s41556-024-01553-1 · Cited by 25
Zhu, X., 中国农业大学生物学院农业生物技术国家重点实验室, 北. 1., Wang, Y., Li, C., Wu, H., Zhang, R., Hu, X., & 中国农业大学模式动物表型与遗传研究国家重大科技基础设施, 北. 1. (2022) · 动物学研究 · doi:10.24272/j.issn.2095-8137.2022.228 · Cited by 29
“…(Shen et al., 2012), tissue specificity indices for each peak were calculated (Schug et al., 2005; Shen et al., 2012), with entropy values closer to zero indicating higher tissue specificity of the peak,…”
InfluentialCTCF blocks antisense transcription initiation at divergent promoters
Luan, J. Y., Vermunt, M. W., Syrett, C. M., Coté, A., Tome, J. M., Zhang, H., Huang, A., Luppino, J. M., Keller, C. A., Giardine, B. M., et al. (2022) · Nature Structural & Molecular Biology · doi:10.1038/s41594-022-00855-y · Cited by 29
3D genome organization links non-coding disease-associated variants to genes
Orozco, G., Schoenfelder, S., Walker, N. J., Eyre, S., & Fraser, P. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.995388 · Cited by 30
“The human genome is thought to contain around one million enhancers (ENCODE project Consortum, 2012; Shen et al., 2012), greatly exceeding the number of protein-coding genes.”
BackgroundMany facades of CTCF unified by its coding for three-dimensional genome architecture
Wu, Q., Liu, P., & Wang, L. (2020) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2020.06.008 · Cited by 26
Mice deficient in UXT exhibit retinitis pigmentosa-like features via aberrant autophagy activation
Pan, M., Yin, Y., Wang, X., Wang, Q., Zhang, L., Hu, H., & Wang, C. (2020) · Autophagy · doi:10.1080/15548627.2020.1796015 · Cited by 28
“[53] and GSE101986 from GEO [54], which covered 9 mouse tissues, including bone marrow, cerebellum, cortex, heart, liver, retina, lung, spleen and kidney.”
BackgroundDifferential 3D chromatin organization and gene activity in genomic imprinting.
Noordermeer, D., & Feil, R. (2020) · Current Opinion in Genetics and Development · doi:10.1016/j.gde.2020.03.004 · Cited by 25
“Within 110 TADs, genes and their associated regulatory elements cluster, whereas CTCF binding is 111 strongly enriched at their boundaries [32,35].”
BackgroundRepressive histone methylation: A case study in deterministic versus stochastic gene regulation
Lyons, D. B., & Lomvardas, S. (2014) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2014.05.010 · Cited by 23
H3K4me3 epigenomic landscape derived from ChIP-Seq of 1 000 mouse early embryonic cells
Shen, J., Jiang, D., Fu, Y., Wu, X.-L., Guo, H.-S., Feng, B., Pang, Y.-H., Streets, A. M., Tang, F.-C., & Huang, Y.-Y. (2014) · Cell Research · doi:10.1038/cr.2014.119 · Cited by 25
Choreography of lamina‐associated domains: structure meets dynamics
Alagna, N. S., Thomas, T. I., Wilson, K. L., & Reddy, K. L. (2023) · FEBS Letters · doi:10.1002/1873-3468.14771 · Cited by 31
“The robust overlap between LADs and (inactive) TAD regions, as defined by Hi-C, highlights the link between overall genome organization and LAD organization [101,115 – 117].”
BackgroundUniversal chromatin state annotation of the mouse genome
Vu, H., & Ernst, J. (2023) · Genome biology · doi:10.1186/s13059-023-02994-x · Cited by 26
“[29] (http:// chrom osome. sdsc. edu/ mouse/ downl oad/ 19-tissu es-expr. zip).”
Ranking reprogramming factors for cell differentiation
Hammelman, J., Patel, T., Closser, M., Wichterle, H., & Gifford, D. K. (2022) · Nature Methods · doi:10.1038/s41592-022-01522-2 · Cited by 34
Molecular dissection of segment formation in the developing hindbrain
Labalette, C., Wassef, M. A., Dinh, C. D., Bouchoucha, Y. X., Men, J. L., Charnay, P., & Gilardi‐Hebenstreit, P. (2014) · Development · doi:10.1242/dev.109652 · Cited by 22
Yukawa, M., Akiyama, T., Franke, V., Mise, N., Isagawa, T., Suzuki, Y., Suzuki, M. G., Vlahoviček, K., Abe, K., Aburatani, H., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092689 · Cited by 35
Colaneri, A., Wang, T., Pagadala, V., Kittur, J., Staffa, N. G., Peddada, S. D., ISGANAITIS, E. M., Patti, M., & Birnbaumer, L. (2013) · PLoS ONE · doi:10.1371/journal.pone.0072670 · Cited by 21
Ching, S., Infante, C., Du, W., Sharir, A., Park, S., Menke, D. B., & Klein, O. (2018) · Human Molecular Genetics · doi:10.1093/hmg/ddx388 · Cited by 24
“Mouse H3K27ac ChIP-Seq alignments for two replicates each of 16 adult and embryonic tissues were downloaded from the ENCODE project website (73).”
MethodKinkade, J. A., Seetharam, A. S., Sachdev, S., Bivens, N. J., Phinney, B. S., Grigorean, G., Roberts, R. M., Tuteja, G., & Rosenfeld, C. S. (2023) · Biology of Reproduction · doi:10.1093/biolre/ioad146 · Cited by 26
“The differentially expressed proteins were used for enrichment analyses, with TissueEnrich (v 1.16.0) and the Mouse ENCODE [57] reference set [58].”
MethodInfluentialIdentification of an intronic enhancer regulating RANKL expression in osteocytic cells
Yan, M., Tsukasaki, M., Muro, R., Ando, Y., Nakamura, K., Komatsu, N., Nitta, T., Okamura, T., Okamoto, K., & Takayanagi, H. (2023) · Bone Research · doi:10.1038/s41413-023-00277-6 · Cited by 26
“23,35 However, the RANKL intronic enhancer sequence is highly conserved (nearly 90”
BackgroundSon, K., Aldonza, M. B., Nam, A.-R., Lee, K.-H., Lee, J.-W., Shin, K.-J., Kang, K., & Cho, J.-Y. (2022) · bioRxiv · doi:10.1101/2022.07.22.501075 · Cited by 23
“For analysis, the algorithm described by the Human Protein Atlas (HPA) [95], as adapted by mouse ENCODE [96] and GTEx [97], was used using teGeneRetrieval function of TissueEnrich [98] v1.”
ΔNp63 regulates a common landscape of enhancer associated genes in non-small cell lung cancer
Napoli, M., Wu, S. J., Gore, B. L., Abbas, H. A., Lee, K., Checker, R., Dhar, S. S., Rajapakshe, K., Tan, A. C., Lee, M. G., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-28202-1 · Cited by 23
Inducible CRISPRa screen identifies putative enhancers
Dai, Z., Li, R., Hou, Y., Li, Q., Zhao, K., Li, T., Li, M. J., & Wu, X. (2021) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2021.06.012 · Cited by 25
Enhancer transcription identifies cis -regulatory elements for photoreceptor cell types
Nadadur, R. D., Perez-Cervantes, C., Lonfat, N., Smith, L. A., Hughes, A. E. O., Wang, S., Corbo, J. C., Cepko, C. L., & Moskowitz, I. P. G. (2020) · Development · doi:10.1242/dev.184432 · Cited by 18
Assessment and site-specific manipulation of DNA (hydroxy-)methylation during mouse corticogenesis
Noack, F., Pataskar, A., Schneider, M., Buchholz, F., Tiwari, V. K., & Calegari, F. (2019) · Life Science Alliance · doi:10.26508/lsa.201900331 · Cited by 29
“5 mouse cortex were taken from the ENCODE project (Shen et al, 2012).”
InfluentialThe effect of Jun dimerization on neurite outgrowth and motif binding
Danzi, M. C., Mehta, S. T., Dulla, K., Zunino, G., Cooper, D. J., Bixby, J. L., & Lemmon, V. (2018) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2018.08.001 · Cited by 36
Mi, W., Uebbing, S., & Ellegren, H. (2017) · Genome Biology and Evolution · doi:10.1093/gbe/evx080 · Cited by 28
Effect of Interaction between Chromatin Loops on Cell-to-Cell Variability in Gene Expression
Liu, T., Zhang, J., & Zhou, T. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004917 · Cited by 27
Bilaterian-like promoters in the highly compact Amphimedon queenslandica genome
Fernández-Valverde, S. L., & Degnan, B. M. (2016) · Scientific Reports · doi:10.1038/srep22496 · Cited by 27
Rich chromatin structure prediction from Hi-C data
Malik, L., & Patro, R. (2015) · bioRxiv · doi:10.1145/3107411.3107448 · Cited by 23
Heterogeneous Tempo and Mode of Conserved Noncoding Sequence Evolution among Four Mammalian Orders
Babarinde, I. A., & Saitou, N. (2013) · Genome Biology and Evolution · doi:10.1093/gbe/evt177 · Cited by 30
“The genomic distribution of CNSs is dynamic with higher proportions of rodent and primate CNSs located in the introns compared with carnivores and cetartiodactyls.”
BackgroundComputational Identification of Active Enhancers in Model Organisms
Wang, C. C. Q., Zhang, M. Q., & Zhang, Z. (2013) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2013.04.002 · Cited by 21
“By comparing predicted enhancers with 726 experimentally validated enhancers, they found that 82% of predicted enhancers were correctly identified [62].”
BackgroundSTYXL1 regulates CCT complex assembly and flagellar tubulin folding in sperm formation
Chen, Y., Luo, M., Tu, H.-X., Qi, Y.-L., Guo, Y.-S., Zhang, X.-Z., Cui, Y., Gao, M.-M., Zhou, X., Zhu, T., et al. (2024) · Nature Communications · doi:10.1038/s41467-023-44337-1 · Cited by 22
“Among 233 phosphatases 28 23 were testis-enriched 29,30 (Fig.”
Bedi, Y. S., Wang, H., Thomas, K. N., Basel, A., Prunier, J., Robert, C., & Golding, M. C. (2022) · Scientific Reports · doi:10.1038/s41598-022-12188-3 · Cited by 35
Bengtsen, M., Winje, I. M., Eftestøl, E., Landskron, J., Sun, C., Nygård, K., Domańska, D., Millay, D. P., Meza‐Zepeda, L. A., & Gundersen, K. (2021) · PLoS Genetics · doi:10.1371/journal.pgen.1009907 · Cited by 26
Dysregulated H3K27 Acetylation Is Implicated in Fatty Liver Hemorrhagic Syndrome in Chickens
Zhu, Y., Zeng, Q., Li, F., Fang, H., Zhou, Z., Jiang, T., Yin, C., Wei, Q., Wang, Y., Ruan, J., et al. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2020.574167 · Cited by 26
Three-dimensional chromatin organization in cardiac development and disease
Bertero, A., & Rosa‐Garrido, M. (2020) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2020.11.008 · Cited by 32
Khilji, S., Hamed, M., Chen, J., & Li, Q. (2018) · Epigenetics · doi:10.1080/15592294.2018.1489659 · Cited by 23
Li, I. M. H., Liu, K., Neal, A., Clegg, P., Val, S. D., & Bou–Gharios, G. (2018) · Scientific Reports · doi:10.1038/s41598-018-19186-4 · Cited by 24
Struebing, F. L., Wang, J., Li, Y., King, R., Mistretta, O. C., ENGLISH, A. W., & Geisert, E. E. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00354 · Cited by 21
“While peripheral and central neurons share about 90% of expressed genes, specific molecules are selectively expressed in both transcriptomes (Smith et al., 2011).”
BackgroundKrox20 hindbrain regulation incorporates multiple modes of cooperation between cis-acting elements
Thierion, E., Men, J. L., Collombet, S., Hernandez, C., Coulpier, F., Torbey, P., Thomas‐Chollier, M., Noordermeer, D., Charnay, P., & Gilardi‐Hebenstreit, P. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006903 · Cited by 24
PAX6 MiniPromoters drive restricted expression from rAAV in the adult mouse retina
Hickmott, J. W., Chen, C., Arenillas, D. J., Korecki, A. J., Lam, S. L., Molday, L. L., Bonaguro, R. J., Zhou, M., Chou, A., Mathelier, A., et al. (2016) · Molecular Therapy — Methods & Clinical Development · doi:10.1038/mtm.2016.51 · Cited by 23
Zhou, J., & Troyanskaya, O. G. (2016) · Nature Communications · doi:10.1038/ncomms10528 · Cited by 17
A Variably Occupied CTCF Binding Site in the Ultrabithorax Gene in the Drosophila Bithorax Complex
Magbanua, J. P., Rünneburger, E., Russell, S. R. H., & White, R. A. (2014) · Molecular and Cellular Biology · doi:10.1128/mcb.01061-14 · Cited by 18
Sokol, M., Wabl, M. R., Ruiz, I. R., & Pedersen, F. S. (2014) · Retrovirology · doi:10.1186/1742-4690-11-36 · Cited by 25
“Abbreviations MLV: Murine leukemia virus; IM: Insertional mutagenesis; LTR: Long terminal repeat; CIS: Common integration site; RNA-seq: RNA sequencing; ChIP-seq: Chromatin Immunoprecipitation with sequencing; EPU: Enhancer and promoter unit; TSS: Transcriptional start site; RTCGD: Retrovirus and Transposon tagged Can…”
BackgroundMethodInfluentialCoregulation of genetic programs by the transcription factors NFIB and STAT5.
Robinson, G., Kang, K., Yoo, K., Tang, Y., Zhu, B., Yamaji, D., Colditz, V., Jang, S.-J., Gronostajski, R., & Hennighausen, L. (2014) · Molecular Endocrinology · doi:10.1210/me.2012-1387 · Cited by 22
Evidence for Local Regulatory Control of Escape from Imprinted X Chromosome Inactivation
Mugford, J. W., Starmer, J., Williams, R. L., Calabrese, J. M., Mieczkowski, P. A., Yee, D., & Magnuson, T. (2014) · Genetics · doi:10.1534/genetics.114.162800 · Cited by 22
“…that escaper interaction profiles were generally enriched for genomic features Local Regulation of Escape from XCI 719 associated with enhancer elements (H3K4me1, H3K27Ac, and DNAse) (Ernst et al. 2011; Shen et al. 2012) or formation of chromatin loops (CCCT-binding factor) (Dixon et al. 2012).”
BackgroundVertebrate Paralogous Conserved Noncoding Sequences May Be Related to Gene Expressions in Brain
Matsunami, M., & Saitou, N. (2012) · Genome Biology and Evolution · doi:10.1093/gbe/evs128 · Cited by 22
CTCF: A misguided jack-of-all-trades in cancer cells
Segueni, J., & Noordermeer, D. (2022) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2022.05.044 · Cited by 31
Nuclease deficiencies alter plasma cell-free DNA methylation profiles
Han, D. S. C., Ni, M., Chan, R. W., Wong, D. K. L., Hiraki, L. T., Volpi, S., Jiang, P., Lui, K. O., Chan, K., Chiu, R. W. K., et al. (2021) · Genome Research · doi:10.1101/gr.275426.121 · Cited by 21
“The loss of DNA self-tolerance with DNASE1L3 deletion is presumably related to the disrupted clearance of nucleosomes by DNASE1L3 (Napirei et al. 2000; Sisirak et al. 2016).”
BackgroundThe Role of Bone Morphogenetic Protein 9 in Nonalcoholic Fatty Liver Disease in Mice
Sun, Q., Cai, L.-Y., Jian, J., Cui, Y., Huang, C., Liu, S., Lu, J., Wang, W., Zeng, X., & Zhong, L. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.605967 · Cited by 21
“The accessibility of chromatin is important for modulating gene expression during normal development (Stergachis et al., 2013; Wu et al., 2016) and results in distinct cellular phenotypes (Shen et al., 2012).”
BackgroundHuang, Y., Feulner, P. G. D., Eizaguirre, C., Lenz, T. L., Bornberg‐Bauer, E., Milinski, M., Reusch, T. B. H., & Chain, F. J. J. (2019) · Genome Biology and Evolution · doi:10.1093/gbe/evz148 · Cited by 25
EnDisease: a manually curated database for enhancer-disease associations
Zeng, W., Xu, M., & Jiang, R. (2019) · Database · doi:10.1093/database/baz020 · Cited by 21
Nanog Expression in Embryonic Stem Cells – An Ideal Model System to Dissect Enhancer Function
Blinka, S. M., & Rao, S. (2017) · BioEssays · doi:10.1002/bies.201700086 · Cited by 24
Dissecting the brown adipogenic regulatory network using integrative genomics
Pradhan, R., Bues, J., Gardeux, V., Schwalie, P. C., Alpern, D., Chen, W., Russeil, J., Raghav, S., & Deplancke, B. (2017) · Scientific Reports · doi:10.1038/srep42130 · Cited by 21
“Further, upon evaluating the mean gene expression levels (across mice and across human cell lines, respectively) of each of these regulators and their correlation with Ucp1 levels, we identified a core group of factors that exhibited both, expression in mouse and human BAT as well as a strong positive correlation with…”
InfluentialKranzhöfer, D., Gilsbach, R., Grüning, B. A., Backofen, R., Nührenberg, T. G., & Hein, L. (2016) · PLoS ONE · doi:10.1371/journal.pone.0166575 · Cited by 17
Zhang, H., Li, F., Jia, Y., Xu, B., Zhang, Y., Li, X., & Zhang, Z. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx885 · Cited by 18
“However, because most cis-regulatory sequences are in the size range of hundreds of base-pairs and may be closely clustered (24), precise definition of individual enhancer-promoter interactions on a genome-wide scale remains beyond the capacity of current Hi-C methodology.”
BackgroundPriest, D. G., Kumar, S., Yan, Y., Dunlap, D. D., Dodd, I. B., & Shearwin, K. E. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1410764111 · Cited by 23
“Chromatin capture studies show that enhancers and promoters are connected in highly complex condition-dependent patterns (6, 15, 17).”
BackgroundAn integrated transcription factor framework for Treg identity and diversity
Chowdhary, K., Léon, J., Ramanan, D., Mathis, D., & Benoist, C. O. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2411301121 · Cited by 31
Merging short and stranded long reads improves transcript assembly
Kainth, A. S., Haddad, G. A., Hall, J. M., & Ruthenburg, A. J. (2023) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1011576 · Cited by 21
“Pol II occupancy at cheRNA Fastq files for RNA Pol II ChIP-seq for HAP1 cells (SRR2301045) [90] and eight-week old mouse heart (RNA Pol II IP: SRR489670; Input: SRR489681) [95] were downloaded from the GEO database.”
MicroRNA changes in the mouse placenta due to bisphenol A exposure.
Mao, J.-D., Kinkade, J. A., Bivens, N., & Rosenfeld, C. (2021) · Epigenomics · doi:10.2217/epi-2021-0339 · Cited by 20
Ghavi-Helm, Y. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.09.010 · Cited by 20
Kirsanova, E., Heringstad, B., Lewandowska-Sabat, A., & Olsaker, I. (2019) · Animal Genetics · doi:10.1111/age.12886 · Cited by 20
Ctcf haploinsufficiency mediates intron retention in a tissue-specific manner
Alharbi, A. B., Schmitz, U., Marshall, A. D., Vanichkina, D., Nagarajah, R., Vellozzi, M., Wong, J. J. L., Bailey, C. G., & Rasko, J. E. J. (2020) · RNA Biology · doi:10.1080/15476286.2020.1796052 · Cited by 23
“Given that CTCF expression and DNA occupancy are variable between tissues [2-5,8,9], these differences may govern how CTCF specifically regulates the transcriptome and AS in tissues.”
BackgroundMeasuring significant changes in chromatin conformation with ACCOST
Cook, K. B., Hristov, B., Roch, K. L. L., Vert, J.-P., & Noble, W. S. (2019) · bioRxiv · doi:10.1101/727768 · Cited by 20
“The first data set is derived from mouse embryonic stem cells (mESCs) (25), and the second is from mouse cortex (26).”
BackgroundDynamic chromatin organization in the cell
Prieto, E., & Maeshima, K. (2019) · Essays in Biochemistry · doi:10.1042/ebc20180054 · Cited by 26
Epigenetic Regulation of IL-17-Induced Chemokines in Lung Epithelial Cells
Luo, J., An, X., Yao, Y., Erb, C., Ferguson, A. A., Kolls, J. K., Fan, S., & Chen, K. (2019) · Mediators of Inflammation · doi:10.1155/2019/9050965 · Cited by 24
“For example, trimethylated histone H3K4 is enriched at promoters [30], while monomethylated H3K4 and acetylated H3Lys27 (H3K27ac) are enriched at active enhancers [31, 32].”
BackgroundThe genome-wide transcriptional regulatory landscape of ecdysone in the silkworm
Cheng, D., Cheng, T., Yang, X., Zhang, Q., Fu, J., Feng, T., Gong, J., & Xia, Q. (2018) · Epigenetics & Chromatin · doi:10.1186/s13072-018-0216-y · Cited by 22
Zhang, P., Rhodes, J. S., Garland, T., Perez, S. D., Southey, B. R., & Rodriguez‐Zas, S. L. (2018) · PLoS ONE · doi:10.1371/journal.pone.0201773 · Cited by 21
“The comparison of brain regions also offers evidence of the statistical power of the experimental design used to detect genes known to be differentially expressed between brain regions based on the mouse ENCODE transcriptome database [96].”
BackgroundBinding of high mobility group A proteins to the mammalian genome occurs as a function of AT-content
Colombo, D., Burger, L., Baubec, T., & Schübeler, D. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1007102 · Cited by 32
Rosario, B. C. D., Rosario, A. M. D., Anselmo, A., Wang, P. I., Sadreyev, R. I., & Lee, J. T. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.09.027 · Cited by 20
“RNA-seq data generated from three murine ES cell lines confirmed that, while ES cells do not express the HH ligands, they express components of the HH signaling pathway (Figures S1A and S1B) (Marks et al., 2012; Shen et al., 2012; Kung et al., 2015).”
BackgroundA unique stylopod patterning mechanism by Shox2 controlled osteogenesis
Ye, W., Song, Y., Huang, Z. J., Osterwalder, M., Ljubojevic, A., Xu, J., Bobick, B. E., Abassah‐Oppong, S., Ruan, N., Shamby, R., et al. (2016) · Development · doi:10.1242/dev.138750 · Cited by 24
Distinct mechanisms regulate Cdx2 expression in the blastocyst and in trophoblast stem cells
Rayon, T., Menchero, S., Rollan, I., Ors, I., Helness, A., Crespo, M., Nieto, A., Azuara, V., Rossant, J., & Manzanares, M. (2016) · Scientific Reports · doi:10.1038/srep27139 · Cited by 20
Remission for Loss of Odontogenic Potential in a New Micromilieu In Vitro
Zheng, Y.-F., Cai, J.-L., Hutchins, A., Jia, L.-N., Liu, P.-F., Yang, D.-D., Chen, S.-B., Ge, L., Pei, D., & Wei, S.-C. (2016) · PLoS ONE · doi:10.1371/journal.pone.0152893 · Cited by 20
Moorthy, S. D., & Mitchell, J. A. (2016) · Journal of Visualized Experiments · doi:10.3791/53552 · Cited by 24
Harten, S. K., Oey, H., Bourke, L. M., Bharti, V., Isbel, L., Daxinger, L., Faou, P., Robertson, N. O., Matthews, J. M., & Whitelaw, E. (2015) · BMC Biology · doi:10.1186/s12915-015-0128-2 · Cited by 20
“To calculate enrichment of histones at Rlf-DMRs the ENCODE sequencing reads [31] for both biological replicates, and for the input, for each tissue and histone modification considered in this manuscript (E14.”
MethodPluripotency in 3D: genome organization in pluripotent cells
Denholtz, M., & Plath, K. (2012) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2012.11.001 · Cited by 21
Zhu, Y., Shang, L., Tang, Y., Li, Q., Ding, L., Wang, Y., Zhang, T., Xie, B., Ma, J., Li, X., et al. (2024) · Advanced Science · doi:10.1002/advs.202404224 · Cited by 11
Lyu, P., Settlage, R. E., & Jiang, H. (2021) · BMC Genomics · doi:10.1186/s12864-021-08224-7 · Cited by 25
Moon, S., & Zhao, Y.-T. (2021) · Glycobiology · doi:10.1093/glycob/cwab054 · Cited by 19
Chromatin architecture reveals cell type-specific target genes for kidney disease risk variants
Duan, A., Wang, H., Zhu, Y., Wang, Q., Zhang, J., Hou, Q., Xing, Y., Shi, J., Hou, J., Qin, Z. S., et al. (2021) · BMC Biology · doi:10.1186/s12915-021-00977-7 · Cited by 26
“Furthermore, histone modifications have been linked to specific functional annotation of non-coding regions [9].”
BackgroundMishra, M. K., Liang, E. Y., Geurts, A. M., Auer, P. L., Liu, P., Rao, S., Greene, A. S., Liang, M., & Liu, Y. U. (2020) · Hypertension · doi:10.1161/hypertensionaha.119.14109 · Cited by 24
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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
