Chromatin architecture reorganization during stem cell differentiation
Open accessAbstract
Higher-order chromatin structure is emerging as an important regulator of gene expression. Although dynamic chromatin structures have been identified in the genome, the full scope of chromatin dynamics during mammalian development and lineage specification remains to be determined. By mapping genome-wide chromatin interactions in human embryonic stem (ES) cells and four human ES-cell-derived lineages, we uncover extensive chromatin reorganization during lineage specification. We observe that although self-associating chromatin domains are stable during differentiation, chromatin interactions both within and between domains change in a striking manner, altering 36% of active and inactive chromosomal compartments throughout the genome. By integrating chromatin interaction maps with haplotype-resolved epigenome and transcriptome data sets, we find widespread allelic bias in gene expression correlated with allele-biased chromatin states of linked promoters and distal enhancers. Our results therefore provide a global view of chromatin dynamics and a resource for studying long-range control of gene expression in distinct human cell lineages. An analysis of genome-wide chromatin interactions during human embryonic stem cell differentiation reveals changes in chromatic organization and simultaneously identifies allele-resolved chromatin structure and differences in gene expression during differentiation. Higher-order chromatin structures are among the factors influencing gene expression, although how these structures evolve during differentiation and lineage specification in mammalian systems is still unclear. Bing Ren and colleagues have mapped the differences in genome-wide chromatin interactions between human embryonic stem cells and their differentiated progeny. They delineate biases in allelic gene expression that correlate with allele-biased chromatin interactions between distal enhancers and proximal promoters.
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Standard Hi-C cannot discriminate whether an interacting fragment originated from the same or the other allele, while allele-specific interaction maps can separate cis-allele from trans-allele interactions, improving analysis of chromatin dynamics and gene regulation.
“While standard Hi-C cannot discriminate whether an interacting fragment originated from the same or the other allele, allele-specific interaction maps can separate cis-allele from trans-allele interactions, thereby greatly improving the analysis of chromatin dynamics and gene regulation 20, 21.”
From SNPsplit: Allele-specific splitting of alignments between genomes with known SNP genotypes (2016) · cites this paper as [20]
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredThe classic model is that enhancers recruit cell- and condition-specific TFs and then loop in 3D space to interact with their target promoter.
“The classic model is that enhancers recruit cell- and condition-specific TFs and then loop in 3D space to interact with their target promoter90.”
From Towards a comprehensive catalogue of validated and target-linked human enhancers (2020) · cites this paper as [90]
The Results (Chromatin state and dynamic interactions; Allelic imbalances in gene expression, page not available) describe cell-type-specific enhancer looping and interactions between enhancers and target promoters. The Discussion (page not available) mentions transcription-factor binding sites at cell-type-specific interaction regions, but our copy does not say that enhancers recruit cell- and condition-specific transcription factors as a step preceding those loops. (LLM, conf=0.85)
Experimental — accuracy not yet measuredIn mammalian differentiation models, extensive remodelling of enhancer-promoter contacts is typically observed consistently with enhancer activation.
“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 [397]
The Results section, ‘Chromatin state and dynamic interactions’ (page unavailable), reports changing long-range interactions during lineage specification associated with H3K4me1 and enhancer density. It does not establish that the extensively remodelled contacts are specifically enhancer–promoter contacts or that their remodelling consistently accompanies enhancer activation. The separate ‘Allelic imbalances in gene expression’ results link enhancer activity to promoter contacts, but examine allelic differences rather than contact remodelling during differentiation. (LLM, conf=0.84)
Experimental — accuracy not yet measuredThese methods have been used to decipher pathological evolution in tumors and somatic mosaicism in healthy tissues and in non-cancerous disease.
“These methods have been used to decipher pathological evolution in tumors11,15,195–197 and somatic mosaicism198 in healthy tissues and in non-cancerous disease199–203.”
From Revealing the vectors of cellular identity with single-cell genomics (2016) · cites this paper as [195]
Fundamentally different chromosome topologies have so far primarily been observed when comparing different developmental lineages.
“Fundamentally different chromosome topologies have so far primarily been observed when comparing different developmental lineages (Dixon et al., 2015, Krijger et al., 2016).”
From The cohesin release factor WAPL restricts chromatin loop extension (2017) · cites this paper as Dixon et al., 2015
A/B compartments are functionally related to gene expression and can switch extensively during differentiation.
“which are functionally related to gene expression and can switch extensively during differentiation (Dixon et al., 2015).”
From Multiscale 3D Genome Rewiring during Mouse Neural Development (2017) · cites this paper as Dixon et al., 2015
Deposition of chromatin marks is thought to contribute to compartment switching.
“The deposition of chromatin marks is thought to contribute to this process (Dixon et al., 2015, Nora et al., 2012)”
From Multiscale 3D Genome Rewiring during Mouse Neural Development (2017) · cites this paper as Dixon et al., 2015
A similar increase in insulation around SOX11 was observed in human cortical development.
“we observed a similar increase in insulation around SOX11 (Figure S3M).”
From Multiscale 3D Genome Rewiring during Mouse Neural Development (2017) · cites this paper as Dixon et al., 2015
TADs have similar boundaries in all human cell types examined.
“These TADs, which have similar boundaries in all human cell types examined, have been proposed to constrain enhancer-gene interactions because most DNA contacts occur within the TADs (Dixon et al., 2015; Dixon et al., 2012).”
From Insulated Neighborhoods: Structural and Functional Units of Mammalian Gene Control (2016) · cites this paper as Dixon et al., 2015
TADs constrain enhancer-gene interactions because most DNA contacts occur within the TADs.
“These TADs, which have similar boundaries in all human cell types examined, have been proposed to constrain enhancer-gene interactions because most DNA contacts occur within the TADs (Dixon et al., 2015; Dixon et al., 2012).”
From Insulated Neighborhoods: Structural and Functional Units of Mammalian Gene Control (2016) · cites this paper as Dixon et al., 2015
TAD boundaries are strikingly similar across cell types.
“the striking similarity of TAD boundaries across cell types (Dixon et al., 2015; Dixon et al., 2012)”
From Insulated Neighborhoods: Structural and Functional Units of Mammalian Gene Control (2016) · cites this paper as Dixon et al., 2015
Most TAD boundaries are shared by any two cell types.
“Studies on TADs have estimated that most TAD boundaries are shared by any two cell types (Dixon et al., 2015; Dixon et al., 2012).”
From Insulated Neighborhoods: Structural and Functional Units of Mammalian Gene Control (2016) · cites this paper as Dixon et al., 2015
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- Authors
- Dixon, J. R., Jung, I., Selvaraj, S., Shen, Y., Antosiewicz-Bourget, J. E., Lee, A. Y., Ye, Z., Kim, A., Rajagopal, N., Xie, W., Diao, Y., Liang, J., Zhao, H., Lobanenkov, V. V., Ecker, J. R., Thomson, J. A., & Ren, B.
- Affiliations
- Ludwig Cancer Research (BE)
- Peking University (CN)
- University of Illinois Urbana-Champaign (US)
- National Institutes of Health (US)
- Salk Institute for Biological Studies (US)
- University of Wisconsin–Madison (US)
- University of California San Diego (US)
- Corresponding author
- Ren, Bing
- ORCID
- Venue
- Nature
- Published
- 2015-02-18
- Volume
- 518
- Issue
- 7539
- Pages
- 331-336
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4515363
- OpenAlex
- W2080477348
- Cited by
- 1,646
- References
- 45
- Citations by year
- 2026: 76 · 2025: 101 · 2024: 112 · 2023: 132 · 2022: 141 · 2021: 202 · 2020: 181 · 2019: 186 · 2018: 186 · 2017: 133 · 2016: 130 · 2015: 63 · 2014: 1 · 2013: 1
- FWCI
- 74.52
- 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)
- RePEc: Research Papers in Economics (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by-nc-sa)
- Funders
- Howard Hughes Medical Institute
- California Institute of Regenerative Medicine (RN2-00905)
- Ludwig Institute for Cancer Research
- National Institutes of Health
- National Institute of General Medical Sciences (T32GM007198)
- National Institute of Environmental Health Sciences (U01ES017166, R01ES024984)
- 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 › Chromatin Remodeling and Cancer
- Keywords
- chromatin structure, chromatin interactions, human embryonic stem cells, stem cell differentiation, lineage specification, chromatin domains, distal enhancers, enhancer-promoter interactions, long-range gene regulation, epigenome, transcriptome
- MeSH terms
- Alleles, Cell Differentiation, Chromatin, Enhancer Elements, Genetic, Humans, Promoter Regions, Genetic, Reproducibility of Results, Cell Lineage, Allelic Imbalance, Chromatin Assembly and Disassembly, Epigenesis, Genetic, Gene Regulatory Networks, Embryonic Stem Cells, Epigenomics
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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