A unique chromatin signature uncovers early developmental enhancers in humans
Open accessAbstract
Cell-fate transitions involve the integration of genomic information encoded by regulatory elements, such as enhancers, with the cellular environment. However, identification of genomic sequences that control human embryonic development represents a formidable challenge. Here we show that in human embryonic stem cells (hESCs), unique chromatin signatures identify two distinct classes of genomic elements, both of which are marked by the presence of chromatin regulators p300 and BRG1, monomethylation of histone H3 at lysine 4 (H3K4me1), and low nucleosomal density. In addition, elements of the first class are distinguished by the acetylation of histone H3 at lysine 27 (H3K27ac), overlap with previously characterized hESC enhancers, and are located proximally to genes expressed in hESCs and the epiblast. In contrast, elements of the second class, which we term 'poised enhancers', are distinguished by the absence of H3K27ac, enrichment of histone H3 lysine 27 trimethylation (H3K27me3), and are linked to genes inactive in hESCs and instead are involved in orchestrating early steps in embryogenesis, such as gastrulation, mesoderm formation and neurulation. Consistent with the poised identity, during differentiation of hESCs to neuroepithelium, a neuroectoderm-specific subset of poised enhancers acquires a chromatin signature associated with active enhancers. When assayed in zebrafish embryos, poised enhancers are able to direct cell-type and stage-specific expression characteristic of their proximal developmental gene, even in the absence of sequence conservation in the fish genome. Our data demonstrate that early developmental enhancers are epigenetically pre-marked in hESCs and indicate an unappreciated role of H3K27me3 at distal regulatory elements. Moreover, the wealth of new regulatory sequences identified here provides an invaluable resource for studies and isolation of transient, rare cell populations representing early stages of human embryogenesis.
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The TRIM33-occupied regions upstream of Bim and Atp1b3 were enriched for H3K27 acetylation but not for H3K4 tri-methylation, suggesting that these elements are active enhancers.
“The TRIM33-occupied regions upstream of Bim and Atp1b3 were enriched for H3K27 acetylation but not for H3K4 tri-methylation, suggesting that these elements are active enhancers”
From The transcriptional cofactor TRIM33 prevents apoptosis in B lymphoblastic leukemia by deactivating a single enhancer (2015) · cites this paper as Rada-Iglesias et al., 2011
The paper describes H3K27ac enrichment with little or no H3K4me3 as part of the signature of putative active enhancers (Abstract; page unavailable). It does not report TRIM33 occupancy or measurements at regions upstream of Bim and Atp1b3, so it supports the interpretation of the marks but not the claim about those specific regions. (LLM, conf=0.85)
Experimental — accuracy not yet measuredH3K27ac modification reliably marks active enhancers located in the distal regions of a given gene.
“Since H3K27ac modification reliably marks active enhancers located in the distal regions of a given gene, 34”
From Kupffer-cell-derived IL-6 is repurposed for hepatocyte dedifferentiation via activating progenitor genes from injury-specific enhancers (2023) · cites this paper as [34]
The Abstract identifies H3K27ac as part of the signature of putative active enhancers in human embryonic stem cells and reports that over 95% of these regions lie away from promoters. It does not establish H3K27ac alone as a reliable marker of active enhancers generally; it also reports no enrichment for the tested modifications at previously described adult tissue-specific enhancers. (LLM, conf=0.87)
Experimental — accuracy not yet measuredH3K4me1, associated with the binding of Trithorax/MLL complexes, is taken to be the hallmark of both primed and active enhancers, whilst active enhancers additionally tend to associate with H3K27ac.
“Currently mono-methylation of histone H3 lysine 4 (H3K4me1), associated with the binding of Trithorax/MLL complexes, is taken to be the hallmark of both ‘primed’ and active enhancers, whilst active enhancers additionally tend to associate with the acetylation of histone H3 lysine 27 (H3K27ac) [133–137].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [135]
The paper’s opening summary (page not provided) describes H3K4me1 at both active and poised enhancers, with H3K27ac distinguishing the active class. It does not establish the claimed association of H3K4me1 with Trithorax/MLL-complex binding. (LLM, conf=0.88)
Experimental — accuracy not yet measuredHigher levels and a bimodal distribution pattern of H3K4me1 correlate with enhancer function.
“Previous studies suggested that higher levels and a bimodal distribution pattern of monomethylated histone 3 lysine 4 (H3K4me1) correlate with enhancer function (Hoffman et al., 2010; Rada-Iglesias et al., 2011).”
From Hippo Signaling Influences HNF4A and FOXA2 Enhancer Switching during Hepatocyte Differentiation (2014) · cites this paper as Rada-Iglesias et al., 2011
Enhancers can reside in a poised state exhibiting both H3K4me1 and H3K27me3 that is associated with Polycomb repressive complexes.
“In addition to the ‘primed’ and active states, enhancers can also reside in a ‘poised’ state exhibiting both H3K4me1 and H3 lysine 27 trimethylation (H3K27me3) that is associated with Polycomb repressive complexes [131, 135, 136, 138].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [135]
Inhibiting p300 catalytic activity with A485 did not decrease TF binding or nucleosome occupancy, despite a marked reduction in H3K27 acetylation.
“We inhibited p300 catalytic activity with the small molecule A48530, but did not observe a decrease in TF binding (Fig. 2N–O vs. Fig. 2B–C) or nucleosome occupancy (Fig. S3M), despite a marked reduction in H3K27 acetylation (Fig. S3N)”
From Single-molecule states link transcription factor binding to gene expression (2024) · cites this paper as [30]
The Abstract reports p300-bound enhancers with differing H3K27ac marks and comparable nucleosome depletion, but it does not describe an inhibitor experiment. Searches of our copy for A485, p300 catalytic inhibition, and effects on TF binding or nucleosome occupancy found no passage addressing the claimed treatment response. (LLM, conf=0.78)
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- Authors
- Rada-Iglesias, A., Bajpai, R., Swigut, T., Brugmann, S. A., Flynn, R. A., & Wysocka, J.
- Affiliations
- Stanford Medicine (US)
- Corresponding author
- Wysocka, Joanna
- Venue
- Nature
- Published
- 2010-12-15
- Volume
- 470
- Issue
- 7333
- Pages
- 279-283
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4445674
- OpenAlex
- W2154746182
- Cited by
- 2,233
- References
- 39
- Citations by year
- 2026: 70 · 2025: 108 · 2024: 118 · 2023: 134 · 2022: 117 · 2021: 154 · 2020: 162 · 2019: 144 · 2018: 151 · 2017: 158 · 2016: 154 · 2015: 181 · 2014: 190 · 2013: 185 · 2012: 140
- FWCI
- 50.78
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institute of Dental and Craniofacial Research (K99DE019853)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Keywords
- enhancers, poised enhancers, human embryonic stem cells, chromatin signatures, H3K4me1, H3K27ac, H3K27me3, P300, SMARCA4, nucleosome density, epiblast, neuroectoderm differentiation, gastrulation, mesoderm formation, neurulation
- MeSH terms
- Acetylation, Animals, Cell Differentiation, Cell Line, Chromatin, DNA Helicases, Enhancer Elements, Genetic, Germ Layers, Histones, Humans, Lysine, Mesoderm, Methylation, Nuclear Proteins, RNA, Transcription Factors, Zebrafish, Gene Expression Regulation, Developmental, Epigenesis, Genetic, Embryonic Development, Chromatin Immunoprecipitation, p300-CBP Transcription Factors, Embryonic Stem Cells, Neural Plate, Neurulation, Gastrulation
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