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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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MethodAnalysis of opo cis-regulatory landscape uncovers Vsx2 requirement in early eye morphogenesis
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“A mouse ChIP-seq study that examined the location of three chromatin modification marks (H3K4me3, H3K4me1, and H3K27ac), the CTCF factor and RNA polymerase II in 19 tissues and cell types showed that more than 70% of CNEs potentially function in gene regulation.(15) The CNEs predict regulators and these overwhelmingly…”
BackgroundEpigenetic and genetic mechanisms in red cell biology
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“Therefore, we also searched the ECCO database [41], comprising ~ 5 million sequences aligned to ~ 300,000 functional elements (such as promoters, enhancers and CTCF binding sites) experimentally identified by the mouse ENCODE project in 19 different tissues [42].”
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InfluentialEnhancers: A Focus on Synthetic Biology and Correlated Gene Expression
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BackgroundMethodInfluentialTargeting transcriptional machinery to inhibit enhancer-driven gene expression in heart failure
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“can act upstream or downstream of their target gene promoters and are often distal, separated by large inter-genic regions (Schoenfelder et al., 2010; Sanyal et al., 2012; Shen et al., 2012).”
BackgroundBioinformatics approaches to predict target genes from transcription factor binding data
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“A Proportion of Repurposed GREs Are Misclassified Interindividual Variabilities To analyze to what extent human regulatory elements can be faithfully modeled in the common marmoset, we compared our data to human datasets of matching tissues (Kundaje et al., 2015; Shen et al., 2012; Villar et al., 2015).”
BackgroundMethodResultInfluentialBagheri, H., Friedman, H. C., Siminovitch, K. A., & Peterson, A. C. (2020) · PLoS Genetics · doi:10.1371/journal.pgen.1008752 · Cited by 10
TADs or no TADS: Lessons From Single-cell Imaging of Chromosome Architecture
Gizzi, A. M. C., Cattoni, D. I., & Nöllmann, M. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.12.034 · Cited by 13
“The current paradigm posits that TADs restrict the action of most regulatory sequences, such as enhancers, within one “functional unit” (Shen et al. 2012; Symmons et al. 2014; Ghavi-Helm et al. 2014; Neems et al. 2016; Ji et al. 2016; Dowen et al. 2014; Ron et al. 2017; Lupiáñez et al. 2015).”
BackgroundCell Line Development for Therapeutic Protein Production
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How computer science can help in understanding the 3D genome architecture
Shavit, Y., Merelli, I., Milanesi, L., & Lió, P. (2015) · Briefings in Bioinformatics · doi:10.1093/bib/bbv085 · Cited by 12
Focussing reduced representation CpG sequencing through judicious restriction enzyme choice
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Chromatin states modify network motifs contributing to cell-specific functions
Zhao, H., Liu, T., Liu, L., Zhang, G., Pang, L., Yu, F., Fan, H., Ping, Y., Wang, L., Xu, C., et al. (2015) · Scientific Reports · doi:10.1038/srep11938 · Cited by 10
Multiscale Identification of Topological Domains in Chromatin
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“[17].”
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Mapping cis-regulatory elements in the midgestation mouse placenta
Starks, R. R., Kaur, H., & Tuteja, G. (2021) · Scientific Reports · doi:10.1038/s41598-021-01664-x · Cited by 9
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“Since the profile of active enhancer is naturally varied between different tissues and cell lines [28], we refined the boundaries of enhancers and generated enhancer calling using the hierarchical clustering method.”
Xie, D., Tong, M., Xia, B., Feng, G., Wang, L., Li, A., Luo, G., Wan, H., Zhang, Z., Zhang, H., et al. (2020) · RNA Biology · doi:10.1080/15476286.2020.1827591 · Cited by 8
Genome-wide identification of enhancer elements in the placenta
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Progress in identifying epigenetic mechanisms of xenobiotic-induced non-genotoxic carcinogenesis
Terranova, R., Vitobello, A., Río-Espínola, A. D., Wolf, C. R., Schwarz, M., Thomson, J. M., Meehan, R. R., & Moggs, J. G. (2017) · Current Opinion in Toxicology · doi:10.1016/j.cotox.2017.06.005 · Cited by 8
Spatiotemporal regulation of enhancers during cardiogenesis
Dupays, L., & Mohun, T. J. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2322-y · Cited by 9
Exploring the sampling universe of RNA-seq
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Whole‐genome sequencing analysis of Japanese autism spectrum disorder trios
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Permeable TAD boundaries and their impact on genome‐associated functions
Chang, L., & Noordermeer, D. (2024) · BioEssays · doi:10.1002/bies.202400137 · Cited by 10
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“Ele v ated le v-els of H3K27ac and H3K4me1 are linked with enhancer regions and correlate with open chromatin sites [ 13 , 17 ].”
HNF1B Alters an Evolutionarily Conserved Nephrogenic Program of Target Genes
Grand, K., Stoltz, M., Rizzo, L., Röck, R., Kaminski, M. M., Salinas, G., Getwan, M., Naert, T., Pichler, R., & Lienkamp, S. S. (2022) · Journal of the American Society of Nephrology · doi:10.1681/asn.2022010076 · Cited by 18
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“Transgenic overexpression of the paternally expressed Igf2 gene increased fetal growth (Sun et al., 1997), and upregulation or downregulation of IGF2 via aberrant imprinting is associated with the overgrowth disorder Beckwith-Wiedemann syndrome and the growth retardation disorder Silver-Russell…”
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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