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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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Changes in Gene Expression and Estrogen Receptor Cistrome in Mouse Liver Upon Acute E2 Treatment
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“org/finder/) (44, 45): Foxa1 (GSM427090; 46), Cebp (GSM548908) (47), Cebp (GSM427088) (46), Ppar (GSM864671) (48), Rxr (GSM864674) (48), GR (common peaks from replicates GSM1122512 and GSM1122515) (49), Esrr (GSM1067408) (50), NR1D1 (GSM647029) (51), NR1D2 (GSM840529) (52), HDAC3 (common peaks from replicates GSM64702…”
Deep conservation of cis -regulatory elements in metazoans
Maeso, I., Irimia, M., Tena, J. J., Casares, F., & Gómez-Skármeta, J. L. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0020 · Cited by 35
Nucleosome fibre topology guides transcription factor binding to enhancers
O’Dwyer, M. R., Azagury, M., Furlong, K., Alsheikh, A., Hall-Ponselé, E., Pinto, H. B., Fyodorov, D. V., Jaber, M., Papachristoforou, E., Benchetrit, H., et al. (2024) · Nature · doi:10.1038/s41586-024-08333-9 · Cited by 32
Myod1 and GR coordinate myofiber-specific transcriptional enhancers
Rovito, D., Rerra, A.-I., Ueberschlag-Pitiot, V., Joshi, S., Karasu, N., Dacleu-Siewe, V., Rayana, K. B., Ghaibour, K. C., Parisotto, M., Ferry, A., et al. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab226 · Cited by 30
“Conversely to the GR and Myod1 common locations at enhancers, Ctcf binding sites were not localized at active enhancers, in contrast with previous studies (78,79), but at H3K4me1-rich regions localized between genes.”
ResultRELACS nuclei barcoding enables high-throughput ChIP-seq
Arrigoni, L., Al-Hasani, H., Ramírez, F., Panzeri, I., Ryan, D. P., Santacruz, D., Kress, N., Pospisilik, J. A., Bönisch, U., & Manke, T. (2018) · Communications Biology · doi:10.1038/s42003-018-0219-z · Cited by 41
Genome-wide Identification and Characterization of Enhancers Across 10 Human Tissues
Xiong, L., Kang, R., Ding, R., Kang, W., Zhang, Y., Liu, W., Huang, Q., Meng, J., & Guo, Z. (2018) · International Journal of Biological Sciences · doi:10.7150/ijbs.26605 · Cited by 41
Genome-wide profiling of transcribed enhancers during macrophage activation
Denisenko, E., Guler, R., Mhlanga, M. M., Suzuki, H., Brombacher, F., & Schmeier, S. (2017) · Epigenetics & Chromatin · doi:10.1186/s13072-017-0158-9 · Cited by 29
“Among 8,667 active enhancers, 54.7% were deemed macrophage-specific (Materials and Methods), in agreement with known tissue-specificity of enhancers 23,42,43 .”
InfluentialEl‐Kasti, M. M., Wells, T., & Carter, D. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds389 · Cited by 29
Transcriptional Enhancers: Bridging the Genome and PhenomePreprint
Ren, B., & Yue, F. (2015) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2015.80.027219 · Cited by 34
“This DNA hypomethylation at enhancers likely involves oxidization of methylcytosine that is subsequently converted to unmethylated cytosine in a Tet-dependent process (Yu et al. 2012; Shen et al. 2013; Song et al. 2013; Hon et al. 2014).”
BackgroundSelf-citationPutative Causal Variants Are Enriched in Annotated Functional Regions From Six Bovine Tissues
Prowse-Wilkins, C., Wang, J., Xiang, R., Garner, J. B., Goddard, M. E., & Chamberlain, A. J. (2021) · Frontiers in Genetics · doi:10.3389/fgene.2021.664379 · Cited by 29
KDM1A maintains genome-wide homeostasis of transcriptional enhancersPreprint
Agarwal, S., Bonefas, K. M., Garay, P. M., Brookes, E., Murata-Nakamura, Y., Porter, R. S., Macfarlan, T. S., Ren, B., & Iwase, S. (2021) · Genome Research · doi:10.1101/gr.234559.118 · Cited by 32
“Loss of KDM1A but not KDM5C results in aberrant activation of transcriptional enhancers in mESCs KDM5C appears to reside in the same complex as KDM1A and suppresses the overactivation of active enhancers in breast cancer cells (Shen et al. 2016).”
Self-citationNeuronal activity-induced BRG1 phosphorylation regulates enhancer activation
Kim, B., Luo, Y., Zhan, X., Zhang, Z., Shi, X., Yi, J., Xuan, Z., & Wu, J. I. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109357 · Cited by 28
CRUP: a comprehensive framework to predict condition-specific regulatory units
Ramisch, A., Heinrich, V., Glaser, L. V., Fuchs, A., Yang, X., Benner, P., Schöpflin, R., Li, N., Kinkley, S., Römer-Hillmann, A., et al. (2019) · Genome biology · doi:10.1186/s13059-019-1860-7 · Cited by 29
Vicente‐García, C., Villarejo-Balcells, B., Irastorza-Azcárate, I., Naranjo, S., Acemel, R. D., Tena, J. J., Rigby, P. W. J., Devos, D. P., Gómez-Skármeta, J. L., & Carvajal, J. J. (2017) · Genome biology · doi:10.1186/s13059-017-1225-z · Cited by 30
“These are large genome intervals defined by an increased number of long-range chromatin interactions between the loci contained in the same chromosomal domain and a decreased number of interactions with loci in neighbouring domains [5].”
BackgroundMethodDynamic cohesin‐mediated chromatin architecture controls epithelial–mesenchymal plasticity in cancer
Yun, J., Song, S., Kim, H., Han, S., Yi, E. C., & Kim, T. (2016) · EMBO Reports · doi:10.15252/embr.201541852 · Cited by 35
“We postulated that there might be unknown non-coding RNA or cis-regulatory sequences in these cells [67].”
Sequence signatures extracted from proximal promoters can be used to predict distal enhancers
Taher, L., Smith, R. P., Kim, M. J., Ahituv, N., & Ovcharenko, I. (2013) · Genome biology · doi:10.1186/gb-2013-14-10-r117 · Cited by 32
“Although most promoters drive basal levels of transcription ubiquitously, some promoters are capable of controlling transcription in a tissue- and/or temporal-specific manner [26-29].”
BackgroundEun, B., Sampley, M. L., Good, A. L., Gebert, C. M., & Pfeifer, K. E. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks1182 · Cited by 31
Accelerated evolution of enhancer hotspots in the mammal ancestor
Holloway, A. K., Bruneau, B. G., Sukonnik, T., Rubenstein, J. L., & Pollard, K. S. (2016) · Molecular Biology and Evolution · doi:10.1093/molbev/msv344 · Cited by 27
“5 brain (Shen et al. 2012).”
BackgroundInfluentialAn Atlas of Gene Regulatory Elements in Adult Mouse Cerebrum
Li, Y. E., Preissl, S., Hou, X., Zhang, Z., Zhang, K., Fang, R., Qiu, Y., Poirion, O., Li, B., Liu, H., et al. (2020) · doi:10.1101/2020.05.10.087585 · Cited by 187
Self-citationTröndle, K., Rizzo, L., Pichler, R., Koch, F., Itani, A., Zengerle, R., Lienkamp, S. S., Koltay, P., & Zimmermann, S. (2021) · Biofabrication · doi:10.1088/1758-5090/abe185 · Cited by 36
“When referring to kidney specificity, gene expression in mouse kidney with respect to the median of the other mouse tissues were compared, according to the RNA sequencing based expression analysis from [35].”
MethodRosario, B. C. D., Kriz, A. J., Rosario, A. M. D., Anselmo, A. N., Fry, C. J., White, F. M., Sadreyev, R. I., & Lee, J. T. (2019) · eLife · doi:10.7554/elife.42341 · Cited by 30
Loguercio, S., Barajas-Mora, E. M., Shih, H., Krangel, M. S., & Feeney, A. J. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.00425 · Cited by 32
Tordini, F., Aldinucci, M., Milanesi, L., Lió, P., & Merelli, I. (2016) · Frontiers in Genetics · doi:10.3389/fgene.2016.00194 · Cited by 32
“…cellular functions are continuously emerging (Lieberman-Aiden et al., 2009; Dong et al., 2010; Schoenfelder et al., 2010; Gerstein et al., 2012; Kalhor et al., 2012; Lan et al., 2012; Shen et al., 2012; Homouz and Kudlicki, 2013; Jin et al., 2013; Papantonis and Cook, 2013; Babaei et al., 2015).”
BackgroundUbiquitously expressed genes participate in cell‐specific functions via alternative promoter usage
Feng, G., Tong, M., Xia, B., Luo, G., Wang, M., Xie, D., Wan, H., Zhang, Y., Zhou, Q., & Wang, X. (2016) · EMBO Reports · doi:10.15252/embr.201541476 · Cited by 25
“By analyzing the public H3K4me3 ChIP-seq data of mESCs and MEFs [15], we observed an enrichment of H3K4me3 modification at the TSS regions of the SATS isoforms in mESCs, but not in MEFs (Fig 1B, left panel).”
Wiz binds active promoters and CTCF-binding sites and is required for normal behaviour in the mouse
Isbel, L., Prokopuk, L., Wu, H., Daxinger, L., Oey, H., Spurling, A., Lawther, A. J., Hale, M. W., & Whitelaw, E. (2016) · eLife · doi:10.7554/elife.15082 · Cited by 28
“To analyse the overlap of Wiz ChIP-seq peaks and ENCODE dataset (Shen et al., 2012) peaks, the latter were first downloaded from the UCSC genome browser (Karolchik et al.”
MethodKnights, A. J., Yik, J. J., Jusoh, H. M., Norton, L. J., Funnell, A. P. W., Pearson, R. C. M., Bell-Anderson, K. S., Crossley, M., & Quinlan, K. G. R. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.715748 · Cited by 26
“GSM769029 and GSM1000139, respectively) (48, 49).”
Gene regulation during development in the light of topologically associating domains
Remeseiro, S., Hörnblad, A., & Spitz, F. (2015) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.218 · Cited by 31
The Hematopoietic Stem and Progenitor Cell Cistrome
Hewitt, K. J., Johnson, K. D., Gao, X., Keleş, S., & Bresnick, E. H. (2016) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2016.01.002 · Cited by 29
Decoding the non‐coding genome: elucidating genetic risk outside the coding genome
Barr, C. L., & Misener, V. L. (2015) · Genes Brain & Behavior · doi:10.1111/gbb.12269 · Cited by 29
“…available for ligation to one another; religation under dilute conditions promotes the desired ligation events, positioning the originally distant DNA sequences adjacent to each another in the ligation products (Lieberman-Aiden et al. 2009; Miele & Dekker 2008; Rao et al. 2014; Shen et al. 2012).”
BackgroundSefer, E., Duggal, G., & Kingsford, C. (2016) · Journal of Computational Biology · doi:10.1089/cmb.2015.0210 · Cited by 26
“Since the development of the original 3C method, a number of enhancements to the protocol, such as 3C, 4C, 5C, Hi-C, and TCC, have been introduced (Simonis et al., 2006; Lieberman-Aiden et al., 2009; Kalhor et al., 2012; Duan et al., 2010).”
MethodGalupa, R., & Heard, É. (2017) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2017.82.035030 · Cited by 30
“…that enhancers and promoters establish spatial interactions, with intervening chromatin looping out (Tolhuis et al. 2002; Sanyal et al. 2012; Shen et al. 2012), and at the β-globin locus, forcing looping between the β-major promoter and the locus control region (LCR) induces transcription…”
BackgroundMaybury‐Lewis, S. Y., Brown, A. K., Yeary, M., Sloutskin, A., Dhakal, S., Juven‐Gershon, T., & Webb, A. E. (2021) · Aging Cell · doi:10.1111/acel.13499 · Cited by 27
CTCF and Its Multi-Partner Network for Chromatin Regulation
Moral‐Morales, A. D., Salgado-Albarrán, M., Sánchez-Pérez, Y., Wenke, N. K., Baumbach, J., & Soto‐Reyes, E. (2023) · Cells · doi:10.3390/cells12101357 · Cited by 30
Identification of a modular super-enhancer in murine retinal development
Honnell, V., Norrie, J. L., Patel, A. G., Ramirez, C., Zhang, J., Lai, Y., Wan, S., & Dyer, M. (2022) · Nature Communications · doi:10.1038/s41467-021-27924-y · Cited by 27
The combined action of CTCF and its testis-specific paralog BORIS is essential for spermatogenesis
Rivero-Hinojosa, S., Pugacheva, E. M., Kang, S., Méndez-Catalá, C. F., Kovalchuk, A. L., Strunnikov, A. V., Loukinov, D. I., Lee, J. T., & Lobanenkov, V. V. (2021) · Nature Communications · doi:10.1038/s41467-021-24140-6 · Cited by 32
Self-citationDisruption of ATRX-RNA interactions uncovers roles in ATRX localization and PRC2 function
Ren, W., Medeiros, N., Warneford-Thomson, R., Wulfridge, P., Yan, Q., Bian, J., Sidoli, S., Garcia, B., Skordalakes, E., Joyce, E., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15902-9 · Cited by 27
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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