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Polycomb Repressive Complex 1 Generates Discrete Compacted Domains that Change during Differentiation
Open accessAbstract
Master regulatory genes require stable silencing by the polycomb group (PcG) to prevent misexpression during differentiation and development. Some PcG proteins covalently modify histones, which contributes to heritable repression. The role for other effects on chromatin structure is less understood. We characterized the organization of PcG target genes in ESCs and neural progenitors using 5C and super-resolution microscopy. The genomic loci of repressed PcG targets formed discrete, small (20-140 Kb) domains of tight interaction that corresponded to locations bound by canonical polycomb repressive complex 1 (PRC1). These domains changed during differentiation as PRC1 binding changed. Their formation depended upon the Polyhomeotic component of canonical PRC1 and occurred independently of PRC1-catalyzed ubiquitylation. PRC1 domains differ from topologically associating domains in size and boundary characteristics. These domains have the potential to play a key role in transmitting epigenetic silencing of PcG targets by linking PRC1 to formation of a repressive higher-order structure.
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“The spatial organization of chromatin, including a variety of long-range DNA interactions, plays a key role in controlling gene expression and maintaining cellular identity (Gorkin et al., 2014; Kundu et al., 2017; Narendra et al., 2015; Schoenfelder et al., 2015; Zirkel et al., 2018).”
From Loss of epigenetic information as a cause of mammalian aging (2023) · cites this paper as Kundu et al., 2017
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BackgroundHistone H2AK119 Mono-Ubiquitination Is Essential for Polycomb-Mediated Transcriptional Repression
Tamburri, S., Lavarone, E., Fernández-Pérez, D., Conway, E., Zanotti, M., Manganaro, D., & Pasini, D. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.11.021 · Cited by 360
Phase separation of Polycomb-repressive complex 1 is governed by a charged disordered region of CBX2Preprint
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“Pluripotent embryonic stem cells (ESCs), which predominately express PHC1 and compaction-deficient CBX7, display condensed Hox gene clusters whose structure is dependent on canonical PRC1 (Eskeland et al. 2010; Kundu et al. 2017).”
Self-citationNuclear condensates of the Polycomb protein chromobox 2 (CBX2) assemble through phase separation
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“The model can explain why the presence of PHC protein, RING1B, and H3K27me3 is required for compaction of chromatin (25, 27, 28, 76, 77) and be tested in the future.”
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The SS18-SSX Fusion Oncoprotein Hijacks BAF Complex Targeting and Function to Drive Synovial Sarcoma
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BackgroundTranscriptional and epigenomic landscapes of CNS and non-CNS vascular endothelial cells
Sabbagh, M. F., Heng, J. S., Luo, C., Castanon, R. G., Nery, J. R., Rattner, A., Goff, L. A., Ecker, J. R., & Nathans, J. (2018) · eLife · doi:10.7554/elife.36187 · Cited by 245
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BackgroundInfluentialDNA methylation in mammalian development and disease
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Rodríguez-Carballo, E., Lopez‐Delisle, L., Zhan, Y., Fabre, P. J., Beccari, L. L., El-Idrissi, I., Huynh, T. H. N., Özadam, H., Dekker, J., & Duboule, D. (2017) · Genes & Development · doi:10.1101/gad.307769.117 · Cited by 180
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MethodSelf-citationCohesin Disrupts Polycomb-Dependent Chromosome Interactions in Embryonic Stem Cells
Rhodes, J. D. P., Feldmann, A., Hernández-Rodríguez, B., Díaz, N., Brown, J. M., Fursova, N. A., Blackledge, N. P., Prathapan, P., Dobrinic, P., Huseyin, M. K., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2019.12.057 · Cited by 187
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“In mESCs, cPRC1-induced chromatin compaction was found to rely mainly on CBX2 and PHC, and compaction was independent of its ubiquitination activity [91–95] – the SAM domain of PHC1/2 (Box 3), that mediates head-to-tail oligomerization of PRC1, and intrinsically disordered regions (IDRs) of CBX2, are both essential fo…”
BackgroundA molecular roadmap for the emergence of early-embryonic-like cells in culture
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InfluentialVilarrasa‐Blasi, R., Soler-Vila, P., Verdaguer-Dot, N., Russiñol, N., Stefano, M. D., Chapaprieta, V., Clot, G., Farabella, I., Cuscó, P., Kulis, M., et al. (2021) · Nature Communications · doi:10.1038/s41467-020-20849-y · Cited by 146
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“…of RING1B does not directly contribute to its ability to alter chromatin architecture and supports the notion that chromatin architecture and histone ubiquitination are functionally separable (Isono et al. 2013; Taherbhoy et al. 2015; Rose et al. 2016; Kundu et al. 2017; Fursova et al. 2019).”
BackgroundResultInfluentialKent, S., Brown, K., Yang, C., Alsaihati, N., Tian, C., Wang, H., & Ren, X. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108248 · Cited by 123
“…site interactions as well as local compaction (Eskeland et al., 2010; Francis et al., 2004; Grau et al., 2011; Isono et al., 2013; Joshi et al., 2015; Kundu et al., 2017; Lau et al., 2017; Schoenfelder et al., 2015); however, there is a lack of a model to unify previous observations.”
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“The compacted, globular structure is lost upon removal of the Pcgroup protein, Polyhomeotic (Ph) [14,15,115], which suggests that PRC1 activity (of which Ph is a core component), rather than the K27me3 deposited by PRC2, is they key determinant of these structural features.”
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Old cogs, new tricks: the evolution of gene expression in a chromatin context
Talbert, P. B., Meers, M. P., & Henikoff, S. (2019) · Nature Reviews Genetics · doi:10.1038/s41576-019-0105-7 · Cited by 115
Polycomb-mediated genome architecture enables long-range spreading of H3K27 methylation
Kraft, K., Yost, K. E., Murphy, S. E., Magg, A., Long, Y., Corces, M. R., Granja, J. M., Wittler, L., Mundlos, S., Cech, T. R., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2201883119 · Cited by 118
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Eeftens, J. M., Kapoor, M., Michieletto, D., & Brangwynne, C. P. (2021) · Nature Communications · doi:10.1038/s41467-021-26147-5 · Cited by 109
A Non-canonical BCOR-PRC1.1 Complex Represses Differentiation Programs in Human ESCs
Wang, Z., Gearhart, M. D., Lee, Y.-W., Kumar, I., Ramazanov, B. R., Zhang, Y., Hernandez, C. C., Lü, A., Neuenkirchen, N., Deng, J., et al. (2018) · Cell stem cell · doi:10.1016/j.stem.2017.12.002 · Cited by 110
“Once recruited to a target, PRC1 deposits H2AK119ub and contributes to chromatin compaction, clustering of PRC-bound regions and gene silencing (Eskeland et al., 2010; Fischle et al., 2003; Kundu et al., 2017; Wang et al., 2004; Wani et al., 2016).”
BackgroundCuadrado, A., Giménez-Llorente, D., Kojic, A., Rodríguez-Corsino, M., Cuartero, Y., Martín‐Serrano, G., Goméz-López, G., Martı́-Renom, M. A., & Losada, A. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.05.078 · Cited by 105
“It has been proposed that compaction within each Polycomb domain may contribute to repression by creating a local chromatin environment that is not compatible with enhancer activation (Boettiger et al., 2016; Kundu et al., 2017).”
BackgroundConway, E., Rossi, F., Fernández-Pérez, D., Ponzo, E., Ferrari, K. J., Zanotti, M., Manganaro, D., Rodighiero, S., Tamburri, S., & Pasini, D. (2021) · Molecular Cell · doi:10.1016/j.molcel.2021.06.020 · Cited by 112
Crispatzu, G., Rehimi, R., Pachano, T., Bleckwehl, T., Cruz-Molina, S., Xiao, C., Mahabir, E., Bazzi, H., & Rada-Iglesias, A. (2021) · Nature Communications · doi:10.1038/s41467-021-24641-4 · Cited by 97
Smchd1 regulates long-range chromatin interactions on the inactive X chromosome and at Hox clusters
Jansz, N., Keniry, A., Trussart, M., Bildsoe, H., Beck, T. J., Tonks, I. D., Mould, A. W., Hickey, P. F., Breslin, K. A., Iminitoff, M., et al. (2018) · Nature Structural & Molecular Biology · doi:10.1038/s41594-018-0111-z · Cited by 101
The Yin and Yang of Histone Marks in Transcription
Talbert, P. B., & Henikoff, S. (2021) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-120220-085159 · Cited by 102
DNA Methylation Directs Polycomb-Dependent 3D Genome Re-organization in Naive Pluripotency
McLaughlin, K. A., Flyamer, I. M., Thomson, J. P., Mjoseng, H. K., Shukla, R., Williamson, I., Grimes, G. R., Illingworth, R. S., Adams, I. R., Pennings, S., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.10.031 · Cited by 92
“1976 Cell Reports 29, 1974–1985, November 12, 2019 Altered Local Interactions at Polycomb Loci between Serum and 2i-Cultured mESCs Polycomb is responsible for forming selfinteracting topologically associated domains (TADs) at Hox loci as detected by chromosome conformation capture methods (Kundu et al., 2017; Noorderm…”
BackgroundInfluentialPRC2 activity, recruitment, and silencing: a comparative perspective
Bieluszewski, T., Xiao, J. Y., Yang, Y., & Wagner, D. (2021) · Trends in Plant Science · doi:10.1016/j.tplants.2021.06.006 · Cited by 100
Guo, J. K., Blanco, M. R., Walkup, W. G., Bonesteele, G., Urbinati, C. R., Banerjee, A. K., Chow, A. Y., Ettlin, O., Strehle, M. M., Peyda, P., et al. (2024) · Molecular Cell · doi:10.1016/j.molcel.2024.01.026 · Cited by 91
Wang, C., Colognori, D., Sunwoo, H., Wang, D., & Lee, J. T. (2019) · Nature Communications · doi:10.1038/s41467-019-10755-3 · Cited by 84
Self-citationWu, Q., Guo, Y., Lu, Y., Li, J., Guo, Y., & Jia, Z. (2020) · Genome biology · doi:10.1186/s13059-020-01984-7 · Cited by 84
“If the Z score of a 5C singleton is larger than 12, the singleton is removed [65] [66] [67] .”
BackgroundMethodHeterochromatin as an Important Driver of Genome Organization
Penagos‐Puig, A., & Furlan-Magaril, M. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.579137 · Cited by 92
“…and a C-terminal chromo-shadow domain that serves as a platform for HP1 dimerization and binding of numerous chromatin-modifying proteins and components of the nuclear envelope thus promoting heterochromatin spreading through large domains (Kwon and Workman, 2008; Eissenberg and Elgin, 2014).”
BackgroundDynamic Control of X-Chromosome Conformation and Repression by a Histone H4K20 Demethylase
Brejc, K., Bian, Q., Uzawa, S., Wheeler, B. S., Anderson, E., King, D. S., Kranzusch, P., Preston, C., & Meyer, B. J. (2017) · Cell · doi:10.1016/j.cell.2017.07.041 · Cited by 81
“At least two different mechanisms contribute to X chromosome structure: a demethylase-independent mechanism that initiates TAD formation and a demethylase-dependent mechanism that compacts X chromosomes and strengthens TADs.”
InfluentialForces driving the three‐dimensional folding of eukaryotic genomes
Rada-Iglesias, Á., Grosveld, F. G., & Papantonis, A. (2018) · Molecular Systems Biology · doi:10.15252/msb.20188214 · Cited by 84
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Roles of Polycomb complexes in regulating gene expression and chromatin structure in plants
Baile, F., Gómez‐Zambrano, Á., & Calonje, M. (2021) · Plant Communications · doi:10.1016/j.xplc.2021.100267 · Cited by 80
“Some reports have provided evidence that it is indispensable (Kundu et al., 2017), whereas others have shown that it is not (Illingworth et al., 2015; Pengelly et al., 2015).”
BackgroundMammalian PRC1 Complexes: Compositional Complexity and Diverse Molecular Mechanisms
Geng, Z., & Gao, Z. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228594 · Cited by 88
“The loss of Phc1 proteins led to a sharp decrease in the chromatin occupancy of canonical PRC1 components together with the disruption of PRC1-mediated chromatin loops [34].”
BackgroundInfluentialAnnotation of chromatin states in 66 complete mouse epigenomes during development
van der Velde, A., Fan, K., Tsuji, J., Moore, J. E., Purcaro, M. J., Pratt, H., & Weng, Z. (2021) · Communications Biology · doi:10.1038/s42003-021-01756-4 · Cited by 68
Huseyin, M. K., & Klose, R. J. (2021) · Nature Communications · doi:10.1038/s41467-021-21130-6 · Cited by 69
Polycomb/Trithorax Antagonism: Cellular Memory in Stem Cell Fate and Function
Brand, M., Nakka, K. K., Zhu, J., & Dilworth, F. J. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.03.005 · Cited by 78
Huang, Y., Sicar, S., Ramirez-Prado, J. S., Manza-Mianza, D., Antunez-Sanchez, J., Brik-Chaouche, R., Rodriguez-Granados, N. R., An, J., Bergounioux, C., Mahfouz, M. M., et al. (2021) · Genome Research · doi:10.1101/gr.273771.120 · Cited by 52
“However, unlike their animal counterparts, these TAD-like structures mainly correspond to large heterochromatic compartments, suggesting that they should rather be referred to as Intergenic CONdensed Spacers (ICONS), because they are not functionally equivalent to TADs (Concia et al. 2020; Huang et al. 2020).”
BackgroundInfluentialTracing DNA paths and RNA profiles in cultured cells and tissues with ORCA
Mateo, L. J., Sinnott-Armstrong, N., & Boettiger, A. N. (2021) · Nature Protocols · doi:10.1038/s41596-020-00478-x · Cited by 65
Molecular Mechanisms of Facultative Heterochromatin Formation: An X-Chromosome Perspective
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Hanna, R., Flamier, A., Barabino, A., & Bernier, G. (2021) · Nature Communications · doi:10.1038/s41467-021-22129-9 · Cited by 73
Polycomb repressive complex 1 shapes the nucleosome landscape but not accessibility at target genesPreprint
King, H. W., Fursova, N. A., Blackledge, N. P., & Klose, R. J. (2018) · Genome Research · doi:10.1101/gr.237180.118 · Cited by 69
“Massively parallel sequencing, data processing and normalisation For ATAC-seq, DNase-seq, FAIRE-seq, ChIP-seq and BioCAP-seq, paired-end reads were aligned to the mouse mm10 genome using bowtie2 (Langmead and Salzberg 2012) with the “--no-mixed” and “--no-discordant” options.”
MethodCheutin, T., & Cavalli, G. (2018) · Nature Communications · doi:10.1038/s41467-018-05945-4 · Cited by 65
Cell Fate and Developmental Regulation Dynamics by Polycomb Proteins and 3D Genome Architecture
Loubière, V., Martinez, A., & Cavalli, G. (2019) · BioEssays · doi:10.1002/bies.201800222 · Cited by 63
Lamb, K. N., Bsteh, D., Dishman, S. N., Moussa, H. F., Fan, H., Stuckey, J. I., Norris, J. L., Cholensky, S. H., Li, D., Wang, J., et al. (2019) · Cell chemical biology · doi:10.1016/j.chembiol.2019.07.013 · Cited by 61
“Polycomb repressive complex 2 (PRC2), which contains the methyltransferase subunit EZH1/2, is responsible for deposition of the H3K27me3 mark (Cao et al., 2002; Czermin et al., 2002; Muller et al., 2002).”
BackgroundInfluentialExploiting epigenetic dependencies in ovarian cancer therapy
Coughlan, A. Y., & Testa, G. (2021) · International Journal of Cancer · doi:10.1002/ijc.33727 · Cited by 58
“vPRC1 (variant) catalyzes the majority of H2AK119ub1, which promotes repression at promoters, at least partially, through PRC2 recruitment,(42,44) while cPRC1 (canonical) promotes compaction and long-range repressive Polycomb body formation through subunits that confer structural changes on chromatin.(40,45,46)”
BackgroundEvolutionarily ancient BAH–PHD protein mediates Polycomb silencing
Wiles, E. T., McNaught, K. J., Silva, S. M. D., Kaur, G., Selker, J. M. L., Ormsby, T., Aravind, L., Musselman, C. A., & Selker, E. U. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1918776117 · Cited by 60
Bonnet, J., Boichenko, I., Kalb, R., Jeune, M. L., Maltseva, S., Pieropan, M., Finkl, K., Fierz, B., & Müller, J. (2022) · Genes & Development · doi:10.1101/gad.350014.122 · Cited by 57
“First, PRC1 compacts nucleosome arrays and thereby renders them refractory to nucleosome remodeling (Francis et al. 2001, 2004; Grau et al. 2011), and second, PRC1 compacts chromatin by mediating long-range interactions between distant chromosomal sites (Isono et al. 2013; Kundu et al. 2017).”
Activity of PRC1 and Histone H2AK119 Monoubiquitination: Revising Popular Misconceptions
Cohen, I., Bar, C., & Ezhkova, E. (2020) · BioEssays · doi:10.1002/bies.201900192 · Cited by 58
Bakhoum, M. F., Francis, J. H., Agustinus, A. S., Earlie, E. M., Bona, M. D., Abramson, D. H., Paez, M. A. D., Masilionis, I., Molina, E., Shoushtari, A. N., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-25529-z · Cited by 58
Regulation of Chromatin Structure During Neural Development
Kishi, Y., & Gotoh, Y. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00874 · Cited by 51
“Furthermore, PcG proteinmediated chromatin interactions can take place beyond TAD boundaries and establish inter-TAD and inter-chromosomal associations in addition to those within TAD boundaries (Denholtz et al., 2013; Schoenfelder et al., 2015; Kundu et al., 2017).”
BackgroundOss-Ronen, L., Sarusi, T., & Cohen, I. (2022) · Cells · doi:10.3390/cells11152404 · Cited by 58
Role of remodeling and spacing factor 1 in histone H2A ubiquitination-mediated gene silencing
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Chromatin folding and nuclear architecture: PRC1 function in 3D
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Histone Lysine Methylation Dynamics Control EGFR DNA Copy-Number Amplification
Clarke, T. L., Tang, R., Chakraborty, D., Van Rechem, C., Ji, F., Mishra, S., Ma, A., Kaniskan, H. Ü., Jin, J., Lawrence, M. S., et al. (2020) · Cancer Discovery · doi:10.1158/2159-8290.cd-19-0463 · Cited by 50
“This looping interaction between distant H3K27me3 regions is similar to the Polycomb-mediated looping interactions described previously (33).”
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“Recently, it has been proposed that PcG domains can have distinct size and boundary characteristics (57); upon differentiation, loci directly involved in fate specification lose PcG-mediated looping interactions, allowing new active promoter/enhancer interactions.”
BackgroundRegulatory mechanisms governing chromatin organization and function
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Collective regulation of chromatin modifications predicts replication timing during cell cycle
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“Hi-C Hi-C interaction frequencies were transformed into distance-specific Z-score and chromatin interaction domains were called using local normalized Hi-C contrast as previously described (Kundu et al., 2017).”
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Self-citation
Metadata
- Authors
- Kundu, S., Ji, F., Sunwoo, H., Jain, G., Lee, J. T., Sadreyev, R. I., Dekker, J., & Kingston, R. E.
- Affiliations
- Harvard University (US)
- University of Massachusetts Chan Medical School (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Kingston, Robert E.
- ORCID
- Venue
- Molecular Cell
- Publisher
- Elsevier BV
- Published
- 2017-02
- Volume
- 65
- Issue
- 3
- Pages
- 432-446.e5
- ISSN
- 1097-2765 (ISSN-L)
- PMC
- PMC5421375
- OpenAlex
- W2585920126
- Cited by
- 333
- References
- 73
- Citations by year
- 2026: 19 · 2025: 23 · 2024: 27 · 2023: 23 · 2022: 45 · 2021: 55 · 2020: 41 · 2019: 48 · 2018: 35 · 2017: 17
- FWCI
- 15.74
- Type
- journal article
- Language
- en
- Update notices
- erratum (2018-07-05)
- Open access
- bronze
- doi.org
- Licence
- Locations
- Molecular Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- eScholarship@UMassChan (submittedVersion)
- Funders
- National Institutes of Health (5R01GM043901-24, DK107980, HG003143, P30 DK40561, R01-GM090278)
- Howard Hughes Medical Institute
- National Institute of General Medical Sciences
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
- Keywords
- PRC1, Polycomb group proteins, chromatin condensation, polyhomeotic, epigenetic silencing, chromatin looping, topologically associating domains, neural progenitor cells, embryonic stem cells, cell differentiation, chromatin organization, higher-order chromatin structure
- MeSH terms
- Protein Domains, Animals, Cell Differentiation, Cells, Cultured, Chromatin, DNA, Histones, Humans, Homeodomain Proteins, Gene Expression Regulation, Developmental, Epigenesis, Genetic, Mice, Embryonic Stem Cells, Ubiquitination, Neural Stem Cells, Polycomb Repressive Complex 1
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