Spatial partitioning of the regulatory landscape of the X-inactivation centre
Open accessAbstract
In eukaryotes transcriptional regulation often involves multiple long-range elements and is influenced by the genomic environment. A prime example of this concerns the mouse X-inactivation centre (Xic), which orchestrates the initiation of X-chromosome inactivation (XCI) by controlling the expression of the non-protein-coding Xist transcript. The extent of Xic sequences required for the proper regulation of Xist remains unknown. Here we use chromosome conformation capture carbon-copy (5C) and super-resolution microscopy to analyse the spatial organization of a 4.5-megabases (Mb) region including Xist. We discover a series of discrete 200-kilobase to 1 Mb topologically associating domains (TADs), present both before and after cell differentiation and on the active and inactive X. TADs align with, but do not rely on, several domain-wide features of the epigenome, such as H3K27me3 or H3K9me2 blocks and lamina-associated domains. TADs also align with coordinately regulated gene clusters. Disruption of a TAD boundary causes ectopic chromosomal contacts and long-range transcriptional misregulation. The Xist/Tsix sense/antisense unit illustrates how TADs enable the spatial segregation of oppositely regulated chromosomal neighbourhoods, with the respective promoters of Xist and Tsix lying in adjacent TADs, each containing their known positive regulators. We identify a novel distal regulatory region of Tsix within its TAD, which produces a long intervening RNA, Linx. In addition to uncovering a new principle of cis-regulatory architecture of mammalian chromosomes, our study sets the stage for the full genetic dissection of the X-inactivation centre.
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Genes in the same topological domain correlate across normal brain samples.
“Consistent with prior studies16, we found that genes in the same domain correlate across samples, but that genes separated by a boundary show lower correlation (Fig. 1e).”
From Insulator dysfunction and oncogene activation in IDH mutant gliomas (2016) · cites this paper as [16]
The transcriptome-analysis passage (labeled Abstract, Fig. 4b) reports that genes within the same TAD had more correlated expression profiles than genes in different domains. But it measured 17 time points during female mouse embryonic stem-cell differentiation, not correlations across normal brain samples. (LLM, conf=0.88)
Experimental — accuracy not yet measuredGenes separated by a domain boundary show lower correlation across normal brain samples.
“Consistent with prior studies16, we found that genes in the same domain correlate across samples, but that genes separated by a boundary show lower correlation (Fig. 1e).”
From Insulator dysfunction and oncogene activation in IDH mutant gliomas (2016) · cites this paper as [16]
The passage on gene expression dynamics during early differentiation reports that genes within the same TAD had more correlated expression profiles than genes in different domains. It measured female mouse embryonic stem cells over a differentiation time course, not normal brain samples, so it does not support that setting. (LLM, conf=0.88)
Experimental — accuracy not yet measuredMetazoan genomes are organised into megabase-scale segregated domains that are often invariant between cell types, termed TADs.
“metazoan genomes are organised into megabase-scale segregated domains that are often invariant between cell types, termed topologically associating domains (TADs) [432–434].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [433]
Eukaryotic chromosomes are partitioned into topologically associated domains (TADs).
“Second, it was demonstrated that eukaryotic chromosomes are partitioned into so-called topologically associated domains (TADs) [35,36,37], which appear to restrict the areas of enhancer action [38,39,40,41].”
From Enhancer Function in the 3D Genome (2023) · cites this paper as [35]
The genome is hierarchically organized into 3D structures, from nucleosome clutches and chromatin loops to TADs, active or repressive compartments, and chromosome territories.
“Indeed, the genome is now known to be hierarchically organized in a series of 3D structures, starting from nucleosome clutches, to chromatin loops, to chromosomal domains called topologically associating domains (TADs), and finally to active or repressive compartments and chromosome territories 15,46,[48][49][50] .”
From Advances in epigenetics link genetics to the environment and disease (2019) · cites this paper as [48]
The improved 5C protocol reduces the number of cells required by 5- to 10-fold and shortens the protocol from 8 days to 4 days.
“These changes enable proceeding through the 3C protocol in a single tube per sample, allow handling of over 20 samples in parallel, reduce the amount of cells needed by a factor 5 to 10 and cut down the time needed to complete the protocol from 8 days (Nora et al. 2012) to 4 days.”
From Targeted Degradation of CTCF Decouples Local Insulation of Chromosome Domains from Genomic Compartmentalization (2017) · cites this paper as Nora et al. 2012
Loop extrusion mediated by cohesin and CTCF mediates the formation of chromatin loops and self-interacting TADs.
“loop extrusion mediated by cohesin and CTCF mediates the formation of chromatin loops and self-interacting Topologically Associating Domains (TADs)”
From Neuronal DNA double-strand breaks lead to genome structural variations and 3D genome disruption in neurodegeneration (2023) · cites this paper as [85]
Mammalian genomes are organized into a hierarchy of Megabase-scale topologically associating domains (TADs) and smaller, nested subTADs.
“Mammalian genomes are organized into a hierarchy of Megabase (Mb)-scale topologically associating domains (TADs) (Dixon et al., 2012; Nora et al., 2012) and smaller, nested subTADs (Dixon et al., 2012; Nora et al., 2012; Phillips-Cremins et al., 2013; Rao et al., 2014).”
From Disease-Associated Short Tandem Repeats Co-localize with Chromatin Domain Boundaries (2018) · cites this paper as Nora et al., 2012
There is enrichment for CTCF at human ES cell boundaries compared to loci internal to domains.
“Consistent with previous reports, we found enrichment for the architectural protein CCCTC-binding factor (CTCF) at human ES cell boundaries compared to loci internal to domains (Figure S6A-B) (Dixon et al., 2012; Nora et al., 2012; Phillips-Cremins et al., 2013).”
From Disease-Associated Short Tandem Repeats Co-localize with Chromatin Domain Boundaries (2018) · cites this paper as Nora et al., 2012
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 Nora et al., 2012
Topologically associating domains (TADs) exist at intermediate scales (100 kb to 1 Mb).
“At intermediate scales (100 kb to 1 Mb), a major discovery is the existence of topologically associating domains (TADs) (Dixon et al., 2012, Nora et al., 2012, Sexton et al., 2012).”
From Multiscale 3D Genome Rewiring during Mouse Neural Development (2017) · cites this paper as Nora et al., 2012
Mammalian chromosomes are structured into largely tissue-invariant TADs in which DNA interactions are more frequent within a given domain than with regions in other domains.
“Recent chromosome conformation studies have revealed that mammalian chromosomes are structured into largely tissue-invariant TADs in which the DNA interactions are more frequent within a given domain than with regions in other domains4,5.”
From Disruption of chromatin folding domains by somatic genomic rearrangements in human cancer (2020) · cites this paper as [5]
Disruption of domain boundaries can result in ectopic interactions between neighboring domains and affect the regulation of nearby genes.
“The disruption of domain boundaries can result in ectopic interactions between neighboring domains and affect the regulation of nearby genes5,9.”
From Disruption of chromatin folding domains by somatic genomic rearrangements in human cancer (2020) · cites this paper as [5]
TADs were identified through Hi-C and their existence has been confirmed by alternative methods such as intrinsic 3C (i3C) and Genome Architecture Mapping (GAM).
“TADs were identified through Hi-C3,4 and their existence have since been confirmed by alternative methods such as intrinsic 3C (i3C),18 which avoids the cross-linking step and Genome Architecture Mapping (GAM),19 which avoids the ligation step.”
From Recent evidence that TADs and chromatin loops are dynamic structures (2018) · cites this paper as [3]
TADs are characterized by preferential contacts between loci inside the same TAD and insulation from loci in adjacent TADs.
“First, chromatin is organized into Topological Associating Domains (TADs) that are characterized by preferential contacts between loci inside the same TAD and insulation from loci in adjacent TADs.3,4”
From Recent evidence that TADs and chromatin loops are dynamic structures (2018) · cites this paper as [3]
TADs correspond to functional regulatory domains by primarily restricting contact between enhancers and promoters to occur within the same TAD.
“A large body of evidence suggests that TADs correspond to functional regulatory domains by primarily restricting contact between enhancers and promoters to occur within the same TAD3,21–25”
From Recent evidence that TADs and chromatin loops are dynamic structures (2018) · cites this paper as [3]
Deletion of a boundary between two TADs causes ectopic contacts between previously insulated loci and can cause aberrant gene expression through improper enhancer-promoter contact.
“Accordingly, deletion of a boundary between two TADs causes ectopic contacts between previously insulated loci3 and can cause aberrant gene expression through improper enhancer-promoter contact.27,28”
From Recent evidence that TADs and chromatin loops are dynamic structures (2018) · cites this paper as [3]
CTCF and cohesin play an important functional role in TAD formation and maintenance.
“suggesting an important functional role of CTCF and cohesin in TAD formation and maintenance (Fig. 2A).”
From Recent evidence that TADs and chromatin loops are dynamic structures (2018) · cites this paper as [3]
DNA FISH and single-cell Hi-C studies show that genome organization is highly variable between cells and that even strong Hi-C loop anchors only contact in a small subset of cells.
“Both DNA FISH3,9,36–39 and single-cell Hi-C40,41 studies show that genome organization is highly variable between cells and that even strong Hi-C loop anchors only contact in a small subset of cells”
From Recent evidence that TADs and chromatin loops are dynamic structures (2018) · cites this paper as [3]
TAD boundaries are near universally enriched in CTCF and cohesin ChIP-Seq peaks.
“After TADs were discovered through Hi-C studies, it quickly became clear that TAD boundaries are near universally enriched in CTCF and cohesin ChIP-Seq peaks,3,4,16”
From Recent evidence that TADs and chromatin loops are dynamic structures (2018) · cites this paper as [3]
The CTCF/cohesin anchored loop domain matching the Hi-C corner-peak actually only exists in a small subset of cells, consistent with high cell-to-cell variability in contact probability observed in DNA FISH studies.
“The CTCF/cohesin anchored loop domain matching the Hi-C corner-peak actually only exists in a small subset of cells, which is also consistent with the high levels of cell-to-cell variability in contact probability observed in DNA FISH studies.3,9,36–39”
From Recent evidence that TADs and chromatin loops are dynamic structures (2018) · cites this paper as [3]
Individual chromosomes are partitioned into megabase-sized topologically associating domains (TADs), regions with relatively high intradomain DNA interaction frequencies as measured by Hi-C chromosome conformation capture data.
“Furthermore, individual chromosomes are partitioned into megabase- sized topologically associating domains (TADs), regions with relatively high intradomain DNA interaction frequencies as measured by Hi-C chromosome conformation capture data (Dixon et al., 2012; Nora et al., 2012).”
From Insulated Neighborhoods: Structural and Functional Units of Mammalian Gene Control (2016) · cites this paper as Nora et al., 2012
TADs identified by processing Hi-C data with the Hidden Markov algorithm can also be identified when this algorithm is used to process cohesin ChIA-PET data.
“Nonetheless, the TADs identified by processing Hi-C data with the Hidden Markov algorithm (Dixon et al., 2012; Nora et al., 2012) can also be identified when this algorithm is used to process cohesin ChIA-PET data (Ji et al., 2016).”
From Insulated Neighborhoods: Structural and Functional Units of Mammalian Gene Control (2016) · cites this paper as Nora et al., 2012
Genome-wide, high-resolution understanding of chromosome cell-cycle dynamics is still limited by current technologies.
“genome-wide, high-resolution understanding of chromosome cell-cycle dynamics11 is still limited by current technologies”
From Cell-cycle dynamics of chromosomal organization at single-cell resolution (2017) · cites this paper as [4]
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“Thus, even the most significant long-range interactions among Tsix/Xite, Chic1, and Linx (Nora et al., 2012; see Figure 2A), rather than corresponding to stable loops of interveningDNA, seem to be due to probabilistic events within highly variable distance distributions, occurring in 34% (Tsix/Xite-Linx), 45% (Tsix/Xi…”
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- Authors
- Nora, E. P., Lajoie, B. R., Schulz, E. G., Giorgetti, L., Okamoto, I., Servant, N., Piolot, T., van Berkum, N. L., Meisig, J., Sedat, J., Gribnau, J., Barillot, E., Blüthgen, N., Dekker, J., & Heard, E.
- Affiliations
- Institut Curie (FR)
- University of Massachusetts Chan Medical School (US)
- Centre National de la Recherche Scientifique (FR)
- Inserm (FR)
- Humboldt-Universität zu Berlin (DE)
- University of California, San Francisco (US)
- Erasmus MC (NL)
- Corresponding author
- Dekker, Job
- ORCID
- Venue
- Nature
- Published
- 2012-04-11
- Volume
- 485
- Issue
- 7398
- Pages
- 381-385
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3555144
- OpenAlex
- W2161212572
- Cited by
- 2,895
- References
- 32
- Citations by year
- 2026: 145 · 2025: 168 · 2024: 181 · 2023: 213 · 2022: 241 · 2021: 276 · 2020: 255 · 2019: 300 · 2018: 247 · 2017: 241 · 2016: 201 · 2015: 173 · 2014: 112 · 2013: 103 · 2012: 34
- FWCI
- 50.79
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (publishedVersion)
- PubMed Central (acceptedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- The Journal of the American Medical Association (JAMA) Network (American Medical Association) (submittedVersion)
- EUR Research Repository (Erasmus University Rotterdam) (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Max Planck Digital Library (submittedVersion, other-oa)
- Funders
- W. M. Keck Foundation
- European Commission (257082, 242129)
- Agence Nationale de la Recherche (ANR-10-INBS-0009)
- Bundesministerium für Bildung und Forschung
- National Institutes of Health
- National Human Genome Research Institute (R01HG003143)
- FP7 Ideas: European Research Council (250367)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Keywords
- X inactivation center, XIST, Tsix, topologically associating domains, 3D genome organization, long-range transcriptional regulation, X chromosome inactivation, chromatin interactions, embryonic stem cells, cell differentiation, lamina-associated domains, distal regulatory regions
- MeSH terms
- Animals, Cell Differentiation, Female, Fibroblasts, Gene Expression Regulation, Histones, Male, Methylation, Molecular Sequence Data, Promoter Regions, Genetic, X Chromosome, In Situ Hybridization, Fluorescence, DNA, Intergenic, RNA, Untranslated, Epigenesis, Genetic, X Chromosome Inactivation, Mice, Embryonic Stem Cells, Epigenomics, Transcriptome, RNA, Long Noncoding
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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