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The accessible chromatin landscape of the human genome
Open accessAbstract
DNase I hypersensitive sites (DHSs) are markers of regulatory DNA and have underpinned the discovery of all classes of cis-regulatory elements including enhancers, promoters, insulators, silencers and locus control regions. Here we present the first extensive map of human DHSs identified through genome-wide profiling in 125 diverse cell and tissue types. We identify ∼2.9 million DHSs that encompass virtually all known experimentally validated cis-regulatory sequences and expose a vast trove of novel elements, most with highly cell-selective regulation. Annotating these elements using ENCODE data reveals novel relationships between chromatin accessibility, transcription, DNA methylation and regulatory factor occupancy patterns. We connect ∼580,000 distal DHSs with their target promoters, revealing systematic pairing of different classes of distal DHSs and specific promoter types. Patterning of chromatin accessibility at many regulatory regions is organized with dozens to hundreds of co-activated elements, and the transcellular DNase I sensitivity pattern at a given region can predict cell-type-specific functional behaviours. The DHS landscape shows signatures of recent functional evolutionary constraint. However, the DHS compartment in pluripotent and immortalized cells exhibits higher mutation rates than that in highly differentiated cells, exposing an unexpected link between chromatin accessibility, proliferative potential and patterns of human variation. An extensive map of human DNase I hypersensitive sites, markers of regulatory DNA, in 125 diverse cell and tissue types is described; integration of this information with other ENCODE-generated data sets identifies new relationships between chromatin accessibility, transcription, DNA methylation and regulatory factor occupancy patterns. This paper describes the first extensive map of human DNaseI hypersensitive sites — markers of regulatory DNA — in 125 diverse cell and tissue types. Integration of this information with other data sets generated by ENCODE (Encyclopedia of DNA Elements) identified new relationships between chromatin accessibility, transcription, DNA methylation and regulatory-factor occupancy patterns. Evolutionary-conservation analysis revealed signatures of recent functional constraint within DNaseI hypersensitive sites.
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“Assisted loading events are coupled with increases in enhancer activity as measured by DNase hypersensitivity or H3K27 acetylation (H3K27ac), two well-established markers for active enhancers38–40.”
From Synergistic gene expression during the acute phase response is characterized by transcription factor assisted loading (2017) · cites this paper as [40]
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“According to recent estimates, the number of enhancers in the human genome ranges from 400,000 to 1,000,000 [22,23].”
From Enhancer Function in the 3D Genome (2023) · cites this paper as [23]
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“To some degree this can be overcome by correlative approaches (e.g. correlating open chromatin status between promoters and enhancers across large numbers of cell types) but such links remain inferential45,134,135.”
From Towards a comprehensive catalogue of validated and target-linked human enhancers (2020) · cites this paper as [45]
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“most genetic variation that contributes to common psychiatric disorders is not in protein-coding regions”
From Defining the genetic, genomic, cellular, and diagnostic architectures of psychiatric disorders (2019) · cites this paper as Thurman et al., 2012
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“Thus, methods that measure chromatin accessibility by combining sensitivity to enzymatic digestion with sequencing6–8 provide an integrated map of chromatin states that encompasses a diverse repertoire of functional regulatory elements2,5.”
From Droplet-based combinatorial indexing for massive-scale single-cell chromatin accessibility (2019) · cites this paper as [2]
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“Both classical observations5 and recent genome-wide efforts2 have shown that active regulatory elements are canonically nucleosome free and accessible to transcriptional machinery.”
From Droplet-based combinatorial indexing for massive-scale single-cell chromatin accessibility (2019) · cites this paper as [2]
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“We found that chromatin accessibility from bulk ATAC-seq8 and DNase-seq2 and the aggregate chromatin accessibility across the different single-cell technologies18,19,24,25 were highly correlated (Fig. 1c,d).”
From Droplet-based combinatorial indexing for massive-scale single-cell chromatin accessibility (2019) · cites this paper as [2]
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Metadata
- Authors
- Thurman, R. E., Rynes, E., Humbert, R., Vierstra, J., Maurano, M. T., Haugen, E., Sheffield, N. C., Stergachis, A. B., Wang, H., Vernot, B., Garg, K., John, S., Sandstrom, R., Bates, D., Boatman, L., Canfield, T. K., Diegel, M., Dunn, D., Ebersol, A. K., Frum, T., Giste, E., Johnson, A. K., Johnson, E. M., Kutyavin, T., Lajoie, B., Lee, B.-K., Lee, K., London, D., Lotakis, D., Neph, S., Neri, F., Nguyen, E. D., Qu, H., Reynolds, A. P., Roach, V., Safi, A., Sanchez, M. E., Sanyal, A., Shafer, A., Simon, J. M., Song, L., Vong, S., Weaver, M., Yan, Y., Zhang, Z., Zhang, Z., Lenhard, B., Tewari, M., Dorschner, M. O., Hansen, R. S., Navas, P. A., Stamatoyannopoulos, G., Iyer, V. R., Lieb, J. D., Sunyaev, S. R., Akey, J. M., Sabo, P. J., Kaul, R., Furey, T. S., Dekker, J., Crawford, G. E., & Stamatoyannopoulos, J. A.
- Affiliations
- University of Washington (US)
- Duke University (US)
- Cape Town HVTN Immunology Laboratory / Hutchinson Centre Research Institute of South Africa (ZA)
- University of Massachusetts Chan Medical School (US)
- The University of Texas at Austin (US)
- Chinese Academy of Sciences (CN)
- University of North Carolina at Chapel Hill (US)
- University of Bergen (NO)
- Brigham and Women's Hospital (US)
- Corresponding author
- Stamatoyannopoulos, John A.
- ORCID
- Rynes, Eric
- Vierstra, Jeff
- Maurano, Matthew T.
- Haugen, Eric
- Sheffield, Nathan C.
- Stergachis, Andrew B.
- Vernot, Benjamin
- Garg, Kavita
- Sandstrom, Richard
- Bates, Daniel
- Frum, Tristan
- Lajoie, Bryan
- Lee, Bum-Kyu
- Lee, Kristen
- Lotakis, Dimitra
- Neph, Shane
- Qu, Hongzhu
- Reynolds, Alex P.
- Safi, Alexias
- Sanyal, Amartya
- Simon, Jeremy M.
- Song, Lingyun
- Zhang, Zhancheng
- Zhang, Zhuzhu
- Lenhard, Boris
- Tewari, Muneesh
- Iyer, Vishwanath R.
- Sunyaev, Shamil R.
- Akey, Joshua M.
- Sabo, Peter J.
- Kaul, Rajinder
- Furey, Terrence S.
- Dekker, Job
- Crawford, Gregory E.
- Stamatoyannopoulos, John A.
- Venue
- Nature
- Published
- 2012-09
- Volume
- 489
- Issue
- 7414
- Pages
- 75-82
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3721348
- OpenAlex
- W1964963969
- Cited by
- 2,679
- References
- 38
- Citations by year
- 2026: 81 · 2025: 97 · 2024: 119 · 2023: 140 · 2022: 170 · 2021: 218 · 2020: 192 · 2019: 199 · 2018: 227 · 2017: 238 · 2016: 238 · 2015: 247 · 2014: 242 · 2013: 235 · 2012: 31
- FWCI
- 96.99
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Nature (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- UNC Libraries
- Funders
- National Science Foundation (HHSN261200800001E, DGE-0-718124, 0718124)
- Norges Forskningsråd
- National Institutes of Health (#HHSN261200800001E, 5u54hg004563-04, HG004563)
- National Institute of Mental Health (R01MH084676)
- National Human Genome Research Institute (U54‑HG004563, U54HG004592, HG004592, HG004563, R01HG003143)
- National Cancer Institute (HHSN261200800001E), P30CA016086)
- National Institute of General Medical Sciences (R01GM076036, GM076036)
- National Institute of Diabetes and Digestive and Kidney Diseases (F30DK095678)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- DNase I hypersensitive sites, chromatin accessibility, cis-regulatory elements, enhancers, promoter, insulators, silencers, locus control region, cell type-specific gene regulation, DNA methylation, transcription factor occupancy, evolutionary constraints, mutation rate, pluripotent cells, human diversity, ENCODE
- MeSH terms
- Chromatin, Deoxyribonuclease I, DNA, DNA-Binding Proteins, Encyclopedias as Topic, Humans, Promoter Regions, Genetic, Regulatory Sequences, Nucleic Acid, Transcription Factors, Transcription, Genetic, Genome, Human, DNA Footprinting, Evolution, Molecular, DNA Methylation, Genomics, Transcription Initiation Site, Molecular Sequence Annotation, Mutation Rate
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