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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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Erdel, F. (2020) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2020.03.006 · Cited by 30
Major nuclear locales define nuclear genome organization and function beyond A and B compartmentsPreprint
Gholamalamdari, O., van Schaik, T., Wang, Y., Kumar, P., Zhang, L., Zhang, Y., Gonzalez, G. A. H., Vouzas, A. E., Zhao, P. A., Gilbert, D. M., et al. (2024) · eLife · doi:10.7554/elife.99116 · Cited by 31
“…is seen normally in retinal rod cells of nocturnal mammals, which lack both LBR and LMNA expression ( Solovei et al., 2013 ), but Hi-C reveals largely unchanged A and B compartments, despite the inversion of euchromatin and heterochromatin nuclear positioning in these cells ( Falk et al., 2019 ).”
Dynamics of microcompartment formation at the mitosis-to-G1 transition
Goel, V. Y., Aboreden, N. G., Jusuf, J. M., Zhang, H., Mori, L., Mirny, L. A., Blobel, G. A., Banigan, E. J., & Hansen, A. S. (2025) · Nature Structural & Molecular Biology · doi:10.1038/s41594-025-01687-2 · Cited by 35
DNA methylation in satellite repeats disorders
Francastel, C., & Magdinier, F. (2019) · Essays in Biochemistry · doi:10.1042/ebc20190028 · Cited by 32
Attach and stretch: Emerging roles for genome–lamina contacts in shaping the 3D genome
Rullens, P. M. J., & Kind, J. (2020) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2020.11.006 · Cited by 26
Zhou, Y., Petrovic, J., Zhao, J., Zhang, W., Bigdeli, A., Zhang, Z., Berger, S. L., Pear, W. S., & Faryabi, R. B. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.01.015 · Cited by 28
Temporally Correlated Active Forces Drive Segregation and Enhanced Dynamics in Chromosome Polymers
Brahmachari, S., Markovich, T., MacKintosh, F. C., & Onuchic, J. N. (2024) · PRX Life · doi:10.1103/prxlife.2.033003 · Cited by 28
The molecular basis of lamin-specific chromatin interactions
Wang, B., Kronenberg‐Tenga, R., Rosti, V., Soldateschi, E. D. P., Luo, Q., Iannacchero, U. M., Pinet, L., Eibauer, M., Boujemaa‐Paterski, R., Schuler, B., et al. (2025) · Nature Structural & Molecular Biology · doi:10.1038/s41594-025-01622-5 · Cited by 28
“The two types of lamin proteins have been described to form two separate but interconnected filamentous meshworks 5 , wherein the B-type lamin meshwork is localized closer to the nuclear membrane 6,7 .”
Tidying-up the plant nuclear space: domains, functions, and dynamics
Santos, A. P., Gaudin, V., Mozgová, I., Pontvianne, F., Schubert, D. S. P., Tek, A. L., Dvořáčková, M., Liu, C., Fransz, P. F., Rosa, S., et al. (2020) · Journal of Experimental Botany · doi:10.1093/jxb/eraa282 · Cited by 29
The epigenetic regulation of centromeres and telomeres in plants and animals
Achrem, M., Szućko-Kociuba, I., & Kalinka, A. (2020) · Comparative Cytogenetics · doi:10.3897/compcytogen.v14i2.51895 · Cited by 29
“Based on the studies of the nucleus of mammalian cells, chromatin was divided into following compartments A – euchromatin, B – facultative heterochromatin (Solovei et al. 2016) and C – pericentromeric constitutive heterochromatin (Falk et al. 2019).”
BackgroundGenome-in-a-Box: Building a Chromosome from the Bottom Up
Birnie, A., & Dekker, C. (2020) · ACS Nano · doi:10.1021/acsnano.0c07397 · Cited by 30
A Liquid State Perspective on Dynamics of Chromatin Compartments
Laghmach, R., Pierro, M. D., & Potoyan, D. A. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.781981 · Cited by 25
Contessoto, V. G., Dudchenko, O., Aiden, E. L., Wolynes, P. G., Onuchic, J. N., & Pierro, M. D. (2023) · Nature Communications · doi:10.1038/s41467-023-35909-2 · Cited by 27
Nuclear genome organization in fungi: from gene folding to Rabl chromosomes
Torres, D. E., Reckard, A. T., Klocko, A. D., & Seidl, M. F. (2023) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuad021 · Cited by 29
“Pr esumabl y, inter actions between heter oc hr omatic r egions, e v en when the small AT-rich isochores across fungal genomes are formed into heterochromatin, could be crucial for phase separation into the active “A” and silent “B” compartments (Falk et al. 2019 ).”
InfluentialLipiński, W. P., Zehnder, J., Abbas, M., Güntert, P., Spruijt, E., & Wiegand, T. (2023) · Chemistry - A European Journal · doi:10.1002/chem.202301159 · Cited by 30
Structure and dynamics of nuclear A/B compartments and subcompartments
Oji, A., Choubani, L., Miura, H., & Hiratani, I. (2024) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2024.102406 · Cited by 28
Brunet, A., Forsberg, F., Fan, Q., Sæther, T., & Collas, P. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00917 · Cited by 27
On the relations of phase separation and Hi-C maps to epigenetics
Singh, P. B., & Newman, A. G. (2020) · Royal Society Open Science · doi:10.1098/rsos.191976 · Cited by 27
Heterochromatin Networks: Topology, Dynamics, and Function (a Working Hypothesis)
Erenpreisa, J. A., Krigerts, J., Salmiņa, K., Gerashchenko, B. I., Freivalds, T., Kurg, R., Winter, R., Krufczik, M., Zayakin, P., Hausmann, M., et al. (2021) · Cells · doi:10.3390/cells10071582 · Cited by 26
“The role of nucleolar and nuclear envelope determinants for cell nucleus organization by heterochromatin was established nearly 50 years ago [81] and detailed by more recent studies [21,65,82].”
BackgroundInfluentialGlobal chromatin relabeling accompanies spatial inversion of chromatin in rod photoreceptors
Smith, C. L., Lan, Y., Jain, R., Epstein, J. A., & Poleshko, A. S. (2021) · Science Advances · doi:10.1126/sciadv.abj3035 · Cited by 26
“…organized nuclear architecture, a recent study showed that the overall euchromatin and heterochromatin domain organization, chromatin compartments, and interactions between topologically associating domains (TADs) observed in conventional nuclei are maintained in murine rod cells ( 14 ).”
CTCF and cohesin promote focal detachment of DNA from the nuclear lamina
van Schaik, T., Liu, N. Q., Manzo, S. G., Peric‐Hupkes, D., de Wit, E., & van Steensel, B. (2022) · Genome biology · doi:10.1186/s13059-022-02754-3 · Cited by 29
“While chromatin positioning at the NL is not required for genome compartmentalization [51] and we do not find specific effects on gene expression in LADs, it remains unclear whether other phenotypes such as telomere maintenance and replication timing are affected by nuclear repositioning following perturbed cohesin dy…”
BackgroundInteractions of Chromatin with the Nuclear Lamina and Nuclear Pore Complexes
Shevelyov, Y. Y. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242115771 · Cited by 27
“Computer simulations of the nucleus that lost heterochromatin attachment to the NE confirm this model [106].”
MethodNoncoding RNA-chromatin association: Functions and mechanisms
Yin, Y., & Shen, X. (2023) · Fundamental Research · doi:10.1016/j.fmre.2023.03.006 · Cited by 28
“In addition, it has been reported that heterochromatin, where LINE1 repeats mainly localized, is the main driving force for compartmentalization of nuclei [112] .”
BackgroundMultiscale modelling of chromatin 4D organization in SARS-CoV-2 infected cells
Chiariello, A. M., Abraham, A., Bianco, S., Esposito, A., Fontana, A., Vercellone, F., Conte, M., & Nicodemi, M. (2024) · Nature Communications · doi:10.1038/s41467-024-48370-6 · Cited by 26
“Of course, more complicated descriptions of compartmentalization are possible and could include other mechanisms known to play a role for chromatin structure, such as interaction with nuclear envelope 19,36 .”
BackgroundMethodGenome folding principles uncovered in condensin-depleted mitotic chromosomes
Zhao, H., Lin, Y., Lin, E., Liu, F., Shu, L., Jing, D., Wang, B., Wang, M., Shan, F., Zhang, L., et al. (2024) · Nature Genetics · doi:10.1038/s41588-024-01759-x · Cited by 26
“Several recent studies performed integrative data analysis using a variety of model systems and explored the relationship between compartmental interactions and chromatin-associated features 1,15,25 .”
Role of dynamic nuclear deformation on genomic architecture reorganization
Seirin‐Lee, S., Osakada, F., Takeda, J., Tashiro, S., Kobayashi, R., Yamamoto, T., & Ochiai, H. (2019) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1007289 · Cited by 26
RETRACTED: Kinetic organization of the genome revealed by ultraresolution multiscale live imaging
Lee, J., Chen, L., Gaudin, S., Gupta, K., Novačić, A., Spakowitz, A. J., & Boettiger, A. N. (2025) · Science · doi:10.1126/science.adx2202 · Cited by 34
RetractedBuilding the genome architecture during the maternal to zygotic transition
Zhang, Y., & Xie, W. (2021) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2021.11.002 · Cited by 25
Uncovering the statistical physics of 3D chromosomal organization using data-driven modeling
Contessoto, V. G., Cheng, R. R., & Onuchic, J. N. (2022) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2022.102418 · Cited by 23
Spatial-Temporal Genome Regulation in Stress-Response and Cell-Fate Change
Erenpreisa, J. A., Giuliani, A., Yoshikawa, K., Falk, M., Hildenbrand, G. L., Salmiņa, K., Freivalds, T., Vainshelbaum, N. M., Weidner, J., Sievers, A., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032658 · Cited by 28
“After years of dispute, the nucleome molecular scientists finally reached a consensus that heterochromatin (HR) contacts play a primary role in the large-scale genome [26,27] organization, thus confirming the data obtained by a pleiad of the abovementioned scientists.”
BackgroundActivity-Driven Phase Transition Causes Coherent Flows of Chromatin
Eshghi, I., Zidovska, A., & Grosberg, A. Y. (2023) · Physical Review Letters · doi:10.1103/physrevlett.131.048401 · Cited by 29
Shin, S., Shi, G., & Thirumalai, D. (2023) · PRX Life · doi:10.1103/prxlife.1.013010 · Cited by 23
“Strikingly, the SPs extracted from the inter-chromosome Hi-C data for the inverted nuclei [28] when used in the SP-CCM simulations reproduce the observed unusual spatial pattern of nuclear compartmentalization in which the euchromatin are localized in the nuclear periphery whereas heterochromatin structures are in the…”
BackgroundMethodResultInfluential
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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