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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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“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]
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“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]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measuredIn the citing paper
“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]
In the citing paper
“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
In the citing paper
“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
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“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
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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
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“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
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“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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Metadata
- 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
- 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
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