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Heterochromatin drives compartmentalization of inverted and conventional nuclei
Open accessAbstract
The nucleus of mammalian cells displays a distinct spatial segregation of active euchromatic and inactive heterochromatic regions of the genome 1,2. In conventional nuclei, microscopy shows that euchromatin is localized in the nuclear interior and heterochromatin at the nuclear periphery 1,2. Genome-wide chromosome conformation capture (Hi-C) analyses show this segregation as a plaid pattern of contact enrichment within euchromatin and heterochromatin compartments 3, and depletion between them. Many mechanisms for the formation of compartments have been proposed, such as attraction of heterochromatin to the nuclear lamina 2,4, preferential attraction of similar chromatin to each other 1,4-12, higher levels of chromatin mobility in active chromatin 13-15 and transcription-related clustering of euchromatin 16,17. However, these hypotheses have remained inconclusive, owing to the difficulty of disentangling intra-chromatin and chromatin-lamina interactions in conventional nuclei 18. The marked reorganization of interphase chromosomes in the inverted nuclei of rods in nocturnal mammals 19,20 provides an opportunity to elucidate the mechanisms that underlie spatial compartmentalization. Here we combine Hi-C analysis of inverted rod nuclei with microscopy and polymer simulations. We find that attractions between heterochromatic regions are crucial for establishing both compartmentalization and the concentric shells of pericentromeric heterochromatin, facultative heterochromatin and euchromatin in the inverted nucleus. When interactions between heterochromatin and the lamina are added, the same model recreates the conventional nuclear organization. In addition, our models allow us to rule out mechanisms of compartmentalization that involve strong euchromatin interactions. Together, our experiments and modelling suggest that attractions between heterochromatic regions are essential for the phase separation of the active and inactive genome in inverted and conventional nuclei, whereas interactions of the chromatin with the lamina are necessary to build the conventional architecture from these segregated phases.
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“Despite the disruption of Lamin B1, the A/B compartmentalization of the genome remained relatively unaffected which is in concordance with the observations in retinal rod neurons, where despite the loss of heterochromatin interactions with the nuclear lamina, phase separation drives the formation of A/B compartments135.”
From Neuronal DNA double-strand breaks lead to genome structural variations and 3D genome disruption in neurodegeneration (2023) · cites this paper as [135]
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ГЕНОМНЫЕ ИСТОЧНИКИ РАЗНООБРАЗИЯ КАК ДРАЙВЕРЫ ДОМЕСТИКАЦИИ (обзор)
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“The HiC data shows that the change of chromatin structure is likely driven by the aggregation of prairies, consistent with the finding that attractions between heterochromatic regions are crucial for the formation of compartment (50), and facilitated by the large number of cell cycles the cells experienced.”
ResultKeenan, C. R., Coughlan, H. D., Iannarella, N., Johanson, T. M., Chan, W. F., Garnham, A. L., Smyth, G. K., & Allan, R. S. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.08.13.249078 · Cited by 3
“The mechanisms driving the formation of these distinct compartments have been unclear but recent modelling suggests that biophysical attractions between heterochromatic regions, and not euchromatic regions, drives the phase separation of active and inactive domains leading to the subsequent tethering of heterochromati…”
BackgroundResultInfluentialDynamic chromosomal interactions and control of heterochromatin positioning by Ki-67Preprint
van Schaik, T., Manzo, S. G., Vouzas, A. E., Liu, N. Q., Teunissen, H., de Wit, E., Gilbert, D. M., & van Steensel, B. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.10.20.465140 · Cited by 3
Structure-function relationships in mitochondrial transcriptional condensatesPreprint
Feric, M., Sarfallah, A., Dar, F., Temiakov, D., Pappu, R. V., & Misteli, T. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.12.30.474545 · Cited by 3
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Effects of Lamina-Chromatin Attachment on Super Long-Range Chromatin InteractionsPreprint
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“However, current efforts on studying the effects of LAD-lamin attachment are limited to smaller genomes such as Drosophila [30], or one or a few chromosomes of mammalian genomes [23, 19].”
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“Although a large number of energy functions could reproduce the Hi-C map ( Di Pierro et al., 2016 ; Falk et al., 2019 ; Jost et al., 2014 ), the CCM is perhaps the simplest copolymer model with only one unknown energy parameter, ϵ .”
BackgroundNode features of chromosome structure networks and their connections to genome annotation
Xu, Y., Das, P., McCord, R. P., & Shen, T. (2024) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2024.05.026 · Cited by 2
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“Nuclear inversion occurs due to the release of heterochromatin from the nuclear lamina during rod differentiation, enabling a transition to the conventional nuclear organization when interactions between heterochromatin and the lamina are established (Falk et al ., 2019; Solovei et al ., 2009).”
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“…of inactive B compartment depends on HP1 protein and L1 repeat RNA, active A compartments self-assemble via multivalent interactions involving RNA polymerase II (Pol II), transcription factors and co-factors, splicing factors, nascent RNA-binding proteins, and histone modifications [71–73].”
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Characterization of H3K9me3 and DNA methylation co-marked CpG-rich regions during mouse development
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“As compartment A and B derived from Hi-C datasets are regarded as euchromatin and hetero-chromatin respectively [19, 20], we calculated the percentages of universal CHMs in Hi-C compartments from 5 cell types (ESCs, NPCs, ncxNPCs, CNs, ncxCNs) [21] (see Methods for details).”
MethodSteric repulsion introduced by loop constraints modulates the microphase separation of chromatins
Wei, J., Xue, Y., Liu, Y., Tian, H., Shao, Y., & Gao, Y. Q. (2024) · The Journal of Chemical Physics · doi:10.1063/5.0189692 · Cited by 2
Pericentromeric satellite RNAs as flexible protein partners in the regulation of nuclear structure
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“C – can be added to specifically represent pericentromeric heterochromatin (Falk et al., 2019) — adjacent to centromeres and establishing heterochromatic states that are naturally more compact.”
Tsukamoto, S., & Mofrad, M. R. K. (2025) · Journal of Chemical Physics · doi:10.1063/5.0232328 · Cited by 1
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“In addition to transcription, other properties of interest include the structure [166–168], dynamics [64], and in vitro phase behaviors of nucleosome arrays [169, 170] as well as the compartmentalization [171–173], radial organization [174, 175], and looping interactions of chromatin [176, 177].”
DeepExDC interprets genomic compartmentalization changes in single-cell Hi-C data
Lv, H., Cao, P., Long, W., Yin, X., Xu, S., & Fu, L. (2025) · Briefings in Bioinformatics · doi:10.1093/bib/bbaf301 · Cited by 2
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“Reconstruction of spatial organization of interphase chromosomes is a complex problem of polymer physics [4] which is now becoming a hot topic of theoretical research in the field of genome biology [5-7].”
BackgroundThe silencing factor Sir3 is a molecular bridge that sticks together distant lociPreprint
Ruault, M., Scolari, V. F., Lazar‐Stefanita, L., Hocher, A., Loïodice, I., Noûs, C., Koszul, R., & Taddei, A. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.29.178368 · Cited by 2
“2014), or anchoring of heterochromatin to the nuclear lamina (Falk et al. 2019).”
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Cluster size determines internal structure of transcription factories in human cells
Semeraro, M., Negro, G., Forte, G., Suma, A., Gonnella, G., Cook, P. R., & Marenduzzo, D. (2025) · eLife · doi:10.1101/2023.01.16.524198 · Cited by 2
Genome folding principles revealed in condensin-depleted mitotic chromosomesPreprint
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“Constitutive heterochromatin also likely functions independent of its role in transcriptional repression to regulate genome architecture and stability(Falk et al. 2019).”
Ab-trapping - a peripheral staining artifact in antibody-based microscopy and genomicsPreprint
Chudzik, K., Sato, Y., Yan, X., Ullrich, S., Trakarnphornsombat, W., Schermelleh, L., Fudenberg, G., Kimurâ, H., Robson, M. I., & Solovei, I. V. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.04.09.648027 · Cited by 2
Widespread 3D genome reorganization precedes programmed DNA rearrangement in Oxytricha trifallaxPreprint
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Polymer physics view of peripheral chromatin: de Gennes' self-similar carpet
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A guide to studying 3D genome structure and dynamics in the kidney
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“The hierarchical 3D organization of the genome with condensation of heterochromatin regions and their separation from euchromatin regions is required for proper compartmentalization and function of the nucleus 103 .”
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Redundant and cooperative interactions between the genome and nuclear lamina
(2025) · Nature Structural & Molecular Biology · doi:10.1038/s41594-025-01670-x · Cited by 1
Coordinated control of genome–nuclear lamina interactions by topoisomerase 2B and lamin B receptor
van Schaik, T., Magnitov, M. D., de Haas, M. D., Breda, J., de Wit, E., Manjón, A. G., Medema, R. H., Gothe, H., Roukos, V., Buckle, A., et al. (2024) · bioRxiv · doi:10.1093/nar/gkaf964 · Cited by 3
“%) to interact with the nuclear lamina (NL) [ 1–3 ].”
The Role of Lamins in Genome Organisation: A Modelling Perspective
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“For example, some TEs play a supporting function in the interphase nucleus architecture (Jordan et al., 2003; Falk et al., 2019).”
Block copolymer concepts of how transcription organizes the stem cell genome
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“In summary, FUS-GFP partitioning, PS timescale and condensate morphology are drastically in fl uenced by the nucleic acid sequences present in the PN core.”
Сродство подобий: механизмы самоассоциации и компартментализации эукариотического хроматина
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“As a result, Hi-C data do not include heterochromatic regions, and heterochromatic interactions can only be revealed by simulations [Falk et al., 2019].”
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Interphase Nucleus and Transposable Elements (Review)
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Genome 3D Structure Generated through Chromatin Movement
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Chromatin unfolding via loops can drive clustered transposon insertion
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“The compartmentalization into A and B compartments, corresponding largely to euchromatin and heterochromatin, is driven by homotypic affinities among LINE-1 and among Alu repeats, respectively (25,68).”
Differential crosslinking and contractile motors drive nuclear chromatin compaction
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Analysis of Heteroсhromatin Mesoscale Architecture by Cryo-Electron Tomography
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1D Sequence Based 3D Chromatin Phase Separation: Forces, Processes, and Functions
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Metadata
- Authors
- Falk, M., Feodorova, Y., Naumova, N., Imakaev, M., Lajoie, B. R., Leonhardt, H., Joffe, B., Dekker, J., Fudenberg, G., Solovei, I., & Mirny, L. A.
- Affiliations
- Massachusetts Institute of Technology (US)
- Medical University Plovdiv (BG)
- Howard Hughes Medical Institute (US)
- Ludwig-Maximilians-Universität München (DE)
- Gladstone Institutes (US)
- Corresponding author
- Fudenberg, Geoffrey
- Solovei, Irina
- Mirny, Leonid A.
- ORCID
- Venue
- Nature
- Published
- 2019-06
- Volume
- 570
- Issue
- 7761
- Pages
- 395-399
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC7206897
- OpenAlex
- W2948487481
- Cited by
- 646
- References
- 55
- Citations by year
- 2026: 50 · 2025: 84 · 2024: 95 · 2023: 90 · 2022: 90 · 2021: 116 · 2020: 88 · 2019: 33
- FWCI
- 28.63
- Type
- journal article
- Language
- en
- Update notices
- correction (2019-08-02)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship@UMassChan (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Human Genome Research Institute (RM1HG007743, R01HG003143)
- National Institute of General Medical Sciences (R01GM114190)
- National Institute of Diabetes and Digestive and Kidney Diseases (U54DK107980)
- 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
- nuclear compartmentalization, heterochromatin, rod photoreceptors, nuclear lamina, euchromatin, pericentromeric heterochromatin, facultative heterochromatin, phase separation, chromosome conformation, chromatin organization, polymer simulation
- MeSH terms
- Animals, Cell Compartmentation, Cell Nucleus, Heterochromatin, Models, Biological, Time Factors, Euchromatin, Nuclear Lamina, Mice
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