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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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“…revealed CTCF as a potential novel co-factor for E2f3 at cell fate genes specifically in NPCs. CTCF is a well-known insulator protein associated with enhancer regions and, as recently demonstrated, with a sub-population of promoter sites (Shen et al., 2012; Phillips-Cremins and Corces, 2013).”
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Ibf1 and Ibf2 are novel CP190‐interacting proteins required for insulator function
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“Loop pixels are better concentrated near CTCF, H3K4me3 and H3K27ac peaks after denoising 1,28–31 (Extended Data Fig.”
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“High-resolution 3C-based studies have mapped regulatory interactions, often 25 falling within TADs, that connect regulatory elements to target gene promoters [8, 9].”
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MethodQuantitative profiling of peptides from RNAs classified as noncoding
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BackgroundHELLS and PRDM9 form a pioneer complex to open chromatin at meiotic recombination hot spotsPreprint
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“In addition, the Sanger project extended the catalog to include structural and regulatory variation (Nellåker et al. 2012; Shen et al. 2012; Yalcin et al. 2011, 2012b).”
Signaling by Steroid Hormones in the 3D Nuclear Space
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“Genome-wide studies of chromosome conformation highlighted that contacts between enhancers and promoters occur in a complex fashion: enhancers frequently contact multiple targets and a given gene can be submitted to the activity of several enhancers [67].”
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“We also analyzed the proximity between promoter regions and Encode-annotated enhancers, in the mouse (Shen et al. 2012).”
BackgroundA comparative analysis of chromatin accessibility in cattle, pig, and mouse tissues
Halstead, M. M., Kern, C., Saelao, P., Wang, Y., Chanthavixay, G., Medrano, J. F. F., Eenennaam, A. L. V., Korf, I. F., Tuggle, C. K., Ernst, C. W., et al. (2020) · BMC Genomics · doi:10.1186/s12864-020-07078-9 · Cited by 72
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“compared regions bound by CTCF in mouse liver to 15 other mouse tissues from the ENCODE Project [42].”
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Mouse MORC3 is a GHKL ATPase that localizes to H3K4me3 marked chromatin
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“The MORC3 (7-456) holoenzyme showed a ratio of roughly 70% monomer/30% dimer without added ligand (Fig.”
BackgroundMethodResultInfluentialSuper-enhancer switching drives a burst in gene expression at the mitosis-to-meiosis transition
Maezawa, S., Sakashita, A., Yukawa, M., Chen, X., Takahashi, K., Alavattam, K. G., Nakata, I., Weirauch, M. T., Barski, A., & Namekawa, S. H. (2020) · Nature Structural & Molecular Biology · doi:10.1038/s41594-020-0488-3 · Cited by 77
β-actin dependent chromatin remodeling mediates compartment level changes in 3D genome architecture
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Cis-regulatory architecture of a brain signaling center predates the origin of chordates
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“Long-range chromatin loops that play regulatory roles in gene expression include Hox cluster silencing [84,85], control of SHH gene by an enhancer that is located 1 Mb away in human [86] and a validated set of cell type-specific enhancers in mouse [87].”
Placenta Extracellular Vesicles: Messengers Connecting Maternal and Fetal Systems
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“Rhesus macaque TSC and those differentiated into synctioTB were permissive for infection with Zika (ZIKV) virus strain DAK AR 41,524 [115].”
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Gene regulation in the 3D genome
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“However, assignment by nearest gene model is the most widely used method, and it has been shown that patterns of enhancer activity correlate strongly with patterns of nearestgene expression (Ernst et al. 2011; Shen et al. 2012).”
MethodDUSP6 mediates resistance to JAK2 inhibition and drives leukemic progression
Kong, T., Laranjeira, A. B. A., Yang, K., Fisher, D. A. C., Yu, L. C., Frégonnière, L. P. D. L., Wang, A. Z., Ruzinova, M. B., Fowles, J. S., Fulbright, M. C., et al. (2022) · Nature Cancer · doi:10.1038/s43018-022-00486-8 · Cited by 48
Dynamic enhancers control skeletal muscle identity and reprogramming
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Tet1 and Tet2 Protect DNA Methylation Canyons against Hypermethylation
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High-throughput functional screening using a homemade dual-glow luciferase assay.
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Identification and analysis of murine pancreatic islet enhancers
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“In line with this, mammalian CTCF is essential for the viability of mouse ESCs and other cell types (Soshnikova et al. 2010; Sleutels et al. 2012; Nora et al. 2017).”
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Genome-wide distribution of Auts2 binding localizes with active neurodevelopmental genes
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Dnmt3a Protects Active Chromosome Domains against Cancer-Associated Hypomethylation
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“LADs and enhancer (downloaded from http://chromosome.sdsc.edu/mouse/download.html) coordinates in MEFs were previously published (56,57) and converted to mm10 coordinates using the liftover tool at UCSC (58).”
CG dinucleotides enhance promoter activity independent of DNA methylationPreprint
Hartl, D., Krebs, A. R., Grand, R. S., Baubec, T., Isbel, L., Wirbelauer, C., Burger, L., & Schübeler, D. (2019) · Genome Research · doi:10.1101/gr.241653.118 · Cited by 62
“We profiled four TFs with CpGs in their canonical motifs and relatively broad expression pattern (Figure 2A, Supplemental Figure 2A-D, data from (Shen et al. 2012)).”
MethodSohni, A., Bartoccetti, M., Khoueiry, R., Spans, L., Velde, J. V., Troyer, L. D., Pulakanti, K., Claessens, F., Rao, S., & Koh, K. P. (2015) · Molecular and Cellular Biology · doi:10.1128/mcb.01172-14 · Cited by 52
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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