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Global reorganisation of cis-regulatory units upon lineage commitment of human embryonic stem cells
Open accessAbstract
Long-range cis-regulatory elements such as enhancers coordinate cell-specific transcriptional programmes by engaging in DNA looping interactions with target promoters. Deciphering the interplay between the promoter connectivity and activity of cis-regulatory elements during lineage commitment is crucial for understanding developmental transcriptional control. Here, we use Promoter Capture Hi-C to generate a high-resolution atlas of chromosomal interactions involving ~22,000 gene promoters in human pluripotent and lineage-committed cells, identifying putative target genes for known and predicted enhancer elements. We reveal extensive dynamics of cis-regulatory contacts upon lineage commitment, including the acquisition and loss of promoter interactions. This spatial rewiring occurs preferentially with predicted changes in the activity of cis-regulatory elements and is associated with changes in target gene expression. Our results provide a global and integrated view of promoter interactome dynamics during lineage commitment of human pluripotent cells.
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“Notably, some contacts between PcG-associated regions, including poised promoters and enhancers in ESCs, are retained after these regions are activated during cell differentiation [141, 143].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [141]
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“the chromatin state of the promoter at dual-state CRUs typically corresponded to the majority state of its enhancers, consistent with a competition of opposing regulatory effects at the promoters.”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [141]
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“Upon early neural differentiation, about a third of single-state CRUs in human ESCs became dual-state, while around half of all dual-state CRUs became single-state [141].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [141]
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“Finally, some enhancers are marked with H3K27me3 alone and are considered to be “Polycomb-repressed” [139–141].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [141]
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“In mammals, PcG-associated promoters and enhancers also engage in multitudes of looping contacts, particularly in early development [139, 141, 276, 357].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [141]
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“In mammalian differentiation models, in contrast, extensive remodelling of enhancer–promoter contacts is typically observed consistently with enhancer activation [141, 394–397].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [141]
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“Nonetheless, a significant minority of enhancers in human ESCs also show pre-existing “permissive” promoter contacts prior to activation [141, 394].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [141]
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“Capture Hi-C analyses in multiple cell types consistently detect enhancer–promoter contacts that cross TAD boundaries [141, 243].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [141]
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“with 20% of CRUs detected in these cells being “dual-state”, i.e. containing a mixture of active and poised or Polycomb-repressed enhancers [141].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [141]
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“Changes in CRU state were predominantly driven by coordinated alterations in the chromatin state of enhancers and their promoter contacts, and were associated with significant changes in gene expression [141].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [141]
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“Enhancers vastly outnumber promoters in human and mouse genomes [131], and consistently promoters often contact more than one enhancer in the same cell type [141, 243, 278, 279].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [141]
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“Analyses in human ESCs and early ES-derived neural progenitors found that, as expected, enhancers within a CRU tended to have the same activity state in a given cell type [141].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [141]
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Citations
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MethodComprehensive Mapping of Long-Range Interactions Reveals Folding Principles of the Human Genome
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MethodTopological domains in mammalian genomes identified by analysis of chromatin interactions
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MethodIntegrative analysis of 111 reference human epigenomes
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BackgroundHistone H3K27ac separates active from poised enhancers and predicts developmental state
Creyghton, M. P., Cheng, A. W., Welstead, G. G., Kooistra, T., Carey, B. W., Steine, E. J., Hanna, J., Lodato, M. A., Frampton, G. M., Sharp, P. A., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1016071107 · Cited by 4,302 · cited 1×
“…activity associated with poised and active enhancers and have been used to show that widespread changes in enhancer position and activity occur upon cell fate decisions such as the lineage commitment of pluripotent cells (Creyghton et al., 2010; Rada-Iglesias et al., 2011; Zentner et al., 2011).”
BackgroundHeintzman, N. D., Stuart, R. K., Hon, G., Fu, Y., Ching, C. W., Hawkins, R. D., Barrera, L. O., Van Calcar, S., Qu, C., Ching, K. A., et al. (2007) · Nature Genetics · doi:10.1038/ng1966 · Cited by 3,398 · cited 1×
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Non-coding variants impact cis-regulatory coordination in a cell type-specific manner
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“The genome involves several promoter–enhancer interactions that are particular to developmental stages and cell types (Freire-Pritchett et al. 2017) and are frequently created simultaneously with genetic alterations during mouse ESC differentiation from neural stem cells to cerebral cortex (Bonev…”
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“This was further substantiated genome-wide by using promoter capture technologies in various experimental conditions in vivo (Javierre et al. 2016; Andrey et al. 2017; Freire-Pritchett et al. 2017).”
BackgroundChromatin architecture and topology in pluripotent stem cells
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Deciphering High-Resolution 3D Chromatin Organization via Capture Hi-C
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Application of the 3C Method to Study the Developmental Genes in Drosophila Larvae
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“Conformational changes in developmental genes can proceed simultaneously with the activation of their expression (Schoenfelder et al., 2015a; Bonev et al., 2017; Freire-Pritchett et al., 2017; Rubin et al., 2017; Schoenfelder et al., 2018b; Novo et al., 2018), or a specific conformation can pre-exist and serves as a s…”
BackgroundDeep learning-based survival prediction using DNA methylation-derived 3D genomic information
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“Raw Hi-C sequencing data as fastq files for cancer [24], normal [47], and stem cell lines [19, 59] were downloaded from Sequence Read Archive (SRA) using sra-tools (v2.”
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“…can loop to several genes, and genes can interact with multiple distal elements, resulting in complex three-dimensional interaction networks that are often re-wired upon cell state change (Beagrie et al., 2017; Freire-Pritchett et al., 2017; Sanyal et al., 2012; Schoenfelder and Fraser, 2019).”
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Self-citationThe impact of endogenous retroviruses on nuclear organization and gene expressionPreprint
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“The significant interactions between promoters and enhancers identified using PCHi-C in neuronal progenitor cells 31 were used to assign target genes to the DNV containing enhancers.”
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Self-citationStructural variation in genomes and its role in disease
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Non-coding variants impact cis -regulatory coordination in a cell type-specific mannerPreprint
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Self-citationDisentangling spatial organization and splicing of rare intron classes in the human genomePreprint
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“However, there were regions in chromosomes 1, 11, 17, 19, 22, and Y that appeared to have a higher density of rare intron classes.”
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Self-citationWang, M., He, B., Hao, Y., Srinivasan, D., Shrinet, J., & Fraser, P. (2024) · Figshare · doi:10.6084/m9.figshare.26642443
Self-citationPushkarev, O., van Mierlo, G., Kribelbauer, J. F., Saelens, W., Gardeux, V., & Deplancke, B. (2024) · Figshare · doi:10.6084/m9.figshare.26333222
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Self-citationPushkarev, O., van Mierlo, G., Kribelbauer, J. F., Saelens, W., Gardeux, V., & Deplancke, B. (2024) · Figshare · doi:10.6084/m9.figshare.26750699
Pushkarev, O., van Mierlo, G., Kribelbauer, J. F., Saelens, W., Gardeux, V., & Deplancke, B. (2024) · Figshare · doi:10.6084/m9.figshare.26750702
Pushkarev, O., van Mierlo, G., Kribelbauer, J. F., Saelens, W., Gardeux, V., & Deplancke, B. (2024) · Figshare · doi:10.6084/m9.figshare.26333392
Pushkarev, O., van Mierlo, G., Kribelbauer, J. F., Saelens, W., Gardeux, V., & Deplancke, B. (2024) · Figshare · doi:10.6084/m9.figshare.26750705
Wolfe, J. C., Mikheeva, L. A., Hagras, H., & Zabet, N. R. (2021) · Figshare · doi:10.6084/m9.figshare.16960406
Pushkarev, O., van Mierlo, G., Kribelbauer, J. F., Saelens, W., Gardeux, V., & Deplancke, B. (2024) · Figshare · doi:10.6084/m9.figshare.26750696
Wang, M., He, B., Hao, Y., Srinivasan, D., Shrinet, J., & Fraser, P. (2024) · Figshare · doi:10.6084/m9.figshare.26642446
Self-citationWolfe, J. C., Mikheeva, L. A., Hagras, H., & Zabet, N. R. (2021) · Figshare · doi:10.6084/m9.figshare.16960409
Pushkarev, O., van Mierlo, G., Kribelbauer, J. F., Saelens, W., Gardeux, V., & Deplancke, B. (2024) · Figshare · doi:10.6084/m9.figshare.26750711
Pushkarev, O., van Mierlo, G., Kribelbauer, J. F., Saelens, W., Gardeux, V., & Deplancke, B. (2024) · Figshare · doi:10.6084/m9.figshare.26750693
Pushkarev, O., van Mierlo, G., Kribelbauer, J. F., Saelens, W., Gardeux, V., & Deplancke, B. (2024) · Figshare · doi:10.6084/m9.figshare.26750708
Identity rather than 3D position informs splicing of rare introns in the human genome
Springer, S. M., Fleck, K., Girardini, K. N., Riccard, S. M., Erceg, J., & Kanadia, R. (2025) · iScience · doi:10.1016/j.isci.2025.114532
“However, there were regions in chromosomes 1, 11, 17, 19, 22, and Y that appeared to have a higher density of rare intron classes (Figure 1E, insets of chromosomes 1 and 19).”
Perez, C., Murat, P., Zeller, A., Liu, K. C., Crisp, A., & Sale, J. E. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.12.705511
“…cell types suggesting that they arise as a fundamental property of the genome (Dixon et al. , 2012; Nora et al. , 2012), although sub-megabase rearrangements of TAD structure and cis-regulatory contacts occur during differentiation (Phillips-Cremins et al. , 2013; Freire-Pritchett et al. , 2017).”
The functional and spatial organization of chromatin during Thymocyte development
Zouari, Y. B. (2018) · theses.fr (ABES) · doi:10.70675/1386d580z2888z41aaz8840z58384a36037b
Deciphering X chromosome architecture during mouse preimplantation development
Ranisavljevic, N. (2017) · theses.fr (ABES) · doi:10.70675/08dd1e70z4ea4z4fd1zbcf2z153b2944c2eb
Selective cross-TAD gene regulation by the Tcra enhancer during T cell development
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Transcription and Three‐Dimensional Genome Organization: Cause, Consequence, or Coordination?
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Cheng, N., Ouellette, T. W., Skead, K., Singhawansa, A., Elliott, M., Cescon, D. W., Bratman, S. V., Carvalho, D. D. D., Soave, D. M., & Awadalla, P. (2026) · Cell Genomics · doi:10.1016/j.xgen.2026.101364
A systematic single-cell analysis of enhancer RNAs across human and mouse
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“Enhancers are noncoding DNA elements that regulate the spatiotemporal expression of associated genes [ 1 ].”
Activation of alpha-globin transcription in primary mouse erythroid progenitors
Beagrie, R. A., & Oudelaar, A. M. (2020) · Discovery Research Portal (University of Dundee) · doi:10.17867/10000139
Metadata
- Authors
- Freire-Pritchett, P., Schoenfelder, S., Várnai, C., Wingett, S. W., Cairns, J., Collier, A. J., García-Vílchez, R., Furlan-Magaril, M., Osborne, C. S., Fraser, P., Rugg-Gunn, P. J., & Spivakov, M.
- Affiliations
- Babraham Institute (GB)
- King's College London (GB)
- Epigenetics Programme, Babraham Institute, Cambridge, United Kingdom
- Corresponding author
- Spivakov, Mikhail
- ORCID
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2017-03-23
- Volume
- 6
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC5407860
- OpenAlex
- W2602710346
- Cited by
- 161
- References
- 88
- Citations by year
- 2026: 9 · 2025: 12 · 2024: 13 · 2023: 16 · 2022: 20 · 2021: 25 · 2020: 17 · 2019: 19 · 2018: 24 · 2017: 6
- FWCI
- 7.37
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Research Portal (King's College London) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- UCL Discovery (University College London) (submittedVersion)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion, cc-by)
- Funders
- Wellcome (WT093736)
- Biotechnology and Biological Sciences Research Council (BB/J004480/1)
- Medical Research Council (MR/J003808/1)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- cis-regulatory elements, enhancers, lineage commitment, human embryonic stem cells, chromatin interactions, promoter capture Hi-C, enhancer target genes, pluripotency
- MeSH terms
- Human Embryonic Stem Cells, Cell Differentiation, Gene Expression Regulation, Humans, Promoter Regions, Genetic, Transcription, Genetic, Regulatory Elements, Transcriptional
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