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3D structures of individual mammalian genomes studied by single-cell Hi-C
Open accessAbstract
The folding of genomic DNA from the beads-on-a-string-like structure of nucleosomes into higher-order assemblies is crucially linked to nuclear processes. Here we calculate 3D structures of entire mammalian genomes using data from a new chromosome conformation capture procedure that allows us to first image and then process single cells. The technique enables genome folding to be examined at a scale of less than 100 kb, and chromosome structures to be validated. The structures of individual topological-associated domains and loops vary substantially from cell to cell. By contrast, A and B compartments, lamina-associated domains and active enhancers and promoters are organized in a consistent way on a genome-wide basis in every cell, suggesting that they could drive chromosome and genome folding. By studying genes regulated by pluripotency factor and nucleosome remodelling deacetylase (NuRD), we illustrate how the determination of single-cell genome structure provides a new approach for investigating biological processes.
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“In regard to chromatin structure, Stevens and colleagues reported that the combination of chromosome conformation capture (3C) and tagged fluorescent imaging was able to detect the folding of a genomic sequence <100bp in a single cell (303).”
From Epigenetic Modifications in Stress Response Genes Associated With Childhood Trauma (2019) · cites this paper as [303]
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“Currently, single-cell Hi-C studies confirm the presence of TADs in individual cells but demonstrate significant variability in their shape (i.e., in the folding of DNA within TADs) [142,143,144,145].”
From Enhancer Function in the 3D Genome (2023) · cites this paper as [144]
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InfluentialThe relationship between genome structure and function
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BackgroundResultWalking along chromosomes with super-resolution imaging, contact maps, and integrative modeling
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Coolpup.py: versatile pile-up analysis of Hi-C data
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“Stevens et al. (8) carried out Hi-C analysis of eight single haploid mouse ESCs.”
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“We observed that genomic reads from GC-poor regions tended to localize to the periphery of the nucleus, consistent with reports describing the localization of the inactive B compartment (16).”
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“NuRD Activity Alters the Protein Binding Repertoire of Regulatory Sequences What effect might a change in chromatin structure have at sites of active transcription? Mbd3 and Chd4 binding patterns are highly correlated with those of pluripotency-associated transcription factors (Figure S1C; Miller et al., 2016; Stevens…”
BackgroundResultSelf-citationMultiscale and integrative single-cell Hi-C analysis with Higashi
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“11 Comparison with 3D structure modeling for imputing sparse contact maps Calculating self-consistent 3D genome structures from scHi-C is potentially an alternative approach for imputing missing contacts in the original scHi-C dataset [27, 28].”
BackgroundMechanosensing and Mechanoregulation of Endothelial Cell Functions
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An Overview of Methods for Reconstructing 3-D Chromosome and Genome Structures from Hi-C Data
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“Nagano et al. and Stevens et al. [34, 120, 121] applied a simulated annealing technique to sample single-cell datasets, while sometimes using contacts as distance re-straints at different data resolutions.”
DUX-miR-344-ZMYM2-Mediated Activation of MERVL LTRs Induces a Totipotent 2C-like State
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“We then studied the gene regulation by ZMYM2 and its partner proteins using our own (Figure 4G) and published (Macfarlan et al., 2012; Stevens et al., 2017) RNA-seq datasets (Table S2).”
BackgroundGenome control by SMC complexes
Hoencamp, C., & Rowland, B. D. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-023-00609-8 · Cited by 147
A promoter interaction map for cardiovascular disease genetics
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Transcription organizes euchromatin via microphase separation
Hilbert, L., Sato, Y., Kuznetsova, K., Bianucci, T., Kimurâ, H., Jülicher, F., Honigmann, A., Zaburdaev, V., & Vastenhouw, N. L. (2021) · Nature Communications · doi:10.1038/s41467-021-21589-3 · Cited by 148
Developing in 3D: the role of CTCF in cell differentiation
Arzate‐Mejía, R. G., Targa, F. R., & Corces, V. G. (2018) · Development · doi:10.1242/dev.137729 · Cited by 144
“Chromosomes occupy positions in the nucleus termed chromosome territories (Cremer et al., 2006; Stevens et al., 2017) and each chromosome can be further organized into interaction domains such as compartments, topologically associating domains (TADs) and loop domains (Ay et al., 2014; Crane et al.,…”
BackgroundThree-dimensional chromatin packing and positioning of plant genomes
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Determining cellular CTCF and cohesin abundances to constrain 3D genome models
Cattoglio, C., Pustova, I., Walther, N., Ho, J. J., Hantsche-Grininger, M., Inouye, C. J., Hossain, M. J., Dailey, G. M., Ellenberg, J., Darzacq, X., et al. (2019) · eLife · doi:10.7554/elife.40164 · Cited by 133
“, 2013), endogenous Halo-tagging of proteins has thus become the gold standard (Chong et al., 2018; Hansen et al., 2017; Komatsubara et al., 2019; Rhodes et al., 2017a; Rhodes et al., 2017b; Stevens et al., 2017; Teves et al., 2016; Teves et al., 2018; Youmans et al., 2018), because it avoids the now well-established…”
BackgroundDiehl, A. G., Ouyang, N., & Boyle, A. P. (2020) · Nature Communications · doi:10.1038/s41467-020-15520-5 · Cited by 139
Conte, M., Fiorillo, L., Bianco, S., Chiariello, A. M., Esposito, A., & Nicodemi, M. (2020) · Nature Communications · doi:10.1038/s41467-020-17141-4 · Cited by 130
The three-dimensional genome: regulating gene expression during pluripotency and development
Andrey, G., & Mundlos, S. (2017) · Development · doi:10.1242/dev.148304 · Cited by 134
“Specifically, around 36% of compartments switch from one type to another as human ESCs differentiate into various lineages (Dixon et al., 2015).”
BackgroundResultInfluentialInterchromosomal interactions: A genomic love story of kissing chromosomes
Maass, P. G., Barutcu, A. R., & Rinn, J. L. (2018) · The Journal of Cell Biology · doi:10.1083/jcb.201806052 · Cited by 124
“201806052 31 within single nuclei (Nagano et al., 2013; Ramani et al., 2017; Stevens et al., 2017).”
BackgroundSingle-cell measurement of higher-order 3D genome organization with scSPRITE
Arrastia, M. V., Jachowicz, J. W., Ollikainen, N., Curtis, M. S., Lai, C., Quinodoz, S. A., Selck, D. A., Ismagilov, R. F., & Guttman, M. (2021) · Nature Biotechnology · doi:10.1038/s41587-021-00998-1 · Cited by 127
Chromatin conformation analysis of primary patient tissue using a low input Hi-C method
Díaz, N., Kruse, K., Erdmann, T., Staiger, A. M., Ott, G., Lenz, G., & Vaquerizas, J. M. (2018) · Nature Communications · doi:10.1038/s41467-018-06961-0 · Cited by 129
The nuclear matrix protein HNRNPU maintains 3D genome architecture globally in mouse hepatocytesPreprint
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“We conducted two replicates of Hi-C experiments, and the results are highly consistent (Supplemental Fig.”
InfluentialCook, P. R., & Marenduzzo, D. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky763 · Cited by 117
“Moreover, TADs are sometimes invisible in single-cell data (56,57), and––if detected––their borders weaken as cells progress through G1 into S phase (58).”
Applications of Single-Cell DNA Sequencing
Evrony, G. D., Hinch, A. G., & Luo, C. (2021) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-111320-090436 · Cited by 129
Single-cell nuclear architecture across cell types in the mouse brain
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Absolute quantification of cohesin, CTCF and their regulators in human cells
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Plant Systems Biology at the Single-Cell Level
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Three-dimensional genome structures of single sensory neurons in mouse visual and olfactory systems
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Epigenetic differences between naïve and primed pluripotent stem cells
Takahashi, S., Kobayashi, S., & Hiratani, I. (2017) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-017-2703-x · Cited by 116
Barrington, C., Georgopoulou, D., Pezic, D., Varsally, W., Herrero, J., & Hadjur, S. (2019) · Nature Communications · doi:10.1038/s41467-019-10725-9 · Cited by 102
Chromatin topology, condensates and gene regulation: shifting paradigms or just a phase?
Mir, M., Bickmore, W. A., Furlong, E. E. M., & Narlikar, G. J. (2019) · Development · doi:10.1242/dev.182766 · Cited by 113
“We also placed emphasis on recent evidence from single cell studies using 3C-based methods (Stevens et al., 2017; Flyamer et al., 2017; Nagano et al., 2013) and imaging approaches (Bintu et al., 2018; Finn et al., 2019; Cattoni et al., 2017), both of which have suggested that chromatin topology…”
Stochastic motion and transcriptional dynamics of pairs of distal DNA loci on a compacted chromosome
Brückner, D. B., Chen, H., Barinov, L., Zoller, B., & Gregor, T. (2023) · Science · doi:10.1126/science.adf5568 · Cited by 112
“However, these structures are not static, but have been revealed to be heterogeneous across cells [24, 25] and dynamic and short-lived in time [26, 27].”
Račko, D., Benedetti, F., Dorier, J., & Stasiak, A. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx1123 · Cited by 120
Simultaneous quantification of protein–DNA contacts and transcriptomes in single cells
Rooijers, K., Markodimitraki, C. M., Rang, F. J., de Vries, S. S., Chialastri, A., de Luca, K. L., Mooijman, D., Dey, S. S., & Kind, J. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0150-y · Cited by 109
Mechanisms of Chromosome Folding and Nuclear Organization: Their Interplay and Open QuestionsPreprint
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Genome-wide stability of the DNA replication program in single mammalian cells
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3C and 3C-based techniques: the powerful tools for spatial genome organization deciphering
Han, J., Zhang, Z., & Wang, K. (2018) · Molecular Cytogenetics · doi:10.1186/s13039-018-0368-2 · Cited by 104
CscoreTool: fast Hi-C compartment analysis at high resolution
Zheng, X., & Zheng, Y. (2017) · Bioinformatics · doi:10.1093/bioinformatics/btx802 · Cited by 96
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“Single-cell chromosome conformation capture methods, such as single-cell Hi-C (scHi-C), [1, 2, 3, 4, 5, 6] enable quantitative assessment of 3D conformation of chromosomes in individual cells.”
MethodMultiscale modeling of genome organization with maximum entropy optimization
Lin, X., Qi, Y., Latham, A. P., & Zhang, B. (2021) · The Journal of Chemical Physics · doi:10.1063/5.0044150 · Cited by 93
Dynamic transcriptome and chromatin architecture in granulosa cells during chicken folliculogenesis
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“Open chromatin could facilitate the binding of transcription factors and the formation of long-range chromatin contacts (e.g., loop domain) (Stevens et al., 2017).”
BackgroundInfluential
Metadata
- Authors
- Stevens, T. J., Lando, D., Basu, S., Atkinson, L. P., Cao, Y., Lee, S. F., Leeb, M., Wohlfahrt, K. J., Boucher, W., O’Shaughnessy-Kirwan, A., Cramard, J., Faure, A. J., Ralser, M., Blanco, E., Morey, L., Sansó, M., Palayret, M. G. S., Lehner, B., Di Croce, L., Wutz, A., Hendrich, B., Klenerman, D., & Laue, E. D.
- Affiliations
- MRC Laboratory of Molecular Biology (GB)
- University of Cambridge (GB)
- Wellcome/MRC Cambridge Stem Cell Institute (GB)
- European Molecular Biology Laboratory (ES)
- Institució Catalana de Recerca i Estudis Avançats (ES)
- Corresponding author
- Laue, Ernest D.
- ORCID
- Venue
- Nature
- Published
- 2017-03-13
- Volume
- 544
- Issue
- 7648
- Pages
- 59-64
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC5385134
- OpenAlex
- W2597274540
- Cited by
- 832
- References
- 41
- Citations by year
- 2026: 42 · 2025: 73 · 2024: 62 · 2023: 71 · 2022: 95 · 2021: 115 · 2020: 95 · 2019: 121 · 2018: 99 · 2017: 58
- FWCI
- 41.56
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Wellcome Trust (082010/Z/07/Z, 277899, 206291/Z/17/Z, 082010)
- Medical Research Council (MR/M010082/1, MC_PC_12009, MR/P019471/1)
- Cancer Research UK Cambridge Institute, University of Cambridge
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
- Keywords
- 3D genome organization, single-cell Hi-C, chromosome conformation capture, topologically associating domains, chromatin looping, lamina-associated domains, mouse embryonic stem cells, cell-to-cell variability, pluripotency factors, nucleosome remodeling, nuclear organization
- MeSH terms
- Mouse Embryonic Stem Cells, CCCTC-Binding Factor, Cohesins, Animals, Chromosomal Proteins, Non-Histone, DNA, Enhancer Elements, Genetic, Gene Expression Regulation, Haploidy, Models, Molecular, Molecular Conformation, Nucleosomes, Promoter Regions, Genetic, Repressor Proteins, Reproducibility of Results, G1 Phase, Genome, Cell Cycle Proteins, Chromosomes, Mammalian, Chromatin Assembly and Disassembly, Mice, Gene Regulatory Networks, Mi-2 Nucleosome Remodeling and Deacetylase Complex, Molecular Imaging, Single-Cell Analysis
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