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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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Cites
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BackgroundInfluentialA bivalent chromatin structure marks key developmental genes in embryonic stem cells
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BackgroundA long noncoding RNA maintains active chromatin to coordinate homeotic gene expression
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BackgroundInfluentialSelf-citationMediator and cohesin connect gene expression and chromatin architecture
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BackgroundSt. Jude Children's Research Hospital–Washington University Pediatric Cancer Genome Project (2012) · Nature Genetics · doi:10.1038/ng.1102 · Cited by 1,724 · cited 1×
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BackgroundChromatin architecture reorganization during stem cell differentiation
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BackgroundHistone Methyltransferase Activity of a Drosophila Polycomb Group Repressor Complex
Müller, J., Hart, C. M., Francis, N. J., Vargas, M. L., Sengupta, A. K., Wild, B., Miller, E., O’Connor, M. B., Kingston, R. E., & Simon, J. A. (2002) · Cell · doi:10.1016/s0092-8674(02)00976-5 · Cited by 1,553
Self-citationCzermin, B., Melfi, R., McCabe, D., Seitz, V., Imhof, A., & Pirrotta, V. (2002) · Cell · doi:10.1016/s0092-8674(02)00975-3 · Cited by 1,536 · cited 1×
“Disruption of H3K27 methylation is believed to be a key defect in human cancers such as glioblastoma (Cao et al., 2002; Czermin et al., 2002; Kuzmichev et al., 2002; Lewis et al., 2013; M€uller et al., 2002; Pengelly et al., 432 Molecular Cell 65, 432–446, February 2, 2017 ª 2017 Elsevier Inc 2013;…”
BackgroundThe long-range interaction landscape of gene promoters
Sanyal, A., Lajoie, B. R., Jain, G., & Dekker, J. (2012) · Nature · doi:10.1038/nature11279 · Cited by 1,489
Self-citationIterative correction of Hi-C data reveals hallmarks of chromosome organization
Imakaev, M., Fudenberg, G., McCord, R. P., Naumova, N., Goloborodko, A., Lajoie, B. R., Dekker, J., & Mirny, L. A. (2012) · Nature Methods · doi:10.1038/nmeth.2148 · Cited by 1,423
Inhibition of PRC2 Activity by a Gain-of-Function H3 Mutation Found in Pediatric Glioblastoma
Lewis, P. W., Müller, M. M., Koletsky, M. S., Cordero, F., Lin, S., Banaszynski, L. A., Garcia, B. A., Muir, T. W., Becher, O. J., & Allis, C. D. (2013) · Science · doi:10.1126/science.1232245 · Cited by 1,345
Dostie, J., Richmond, T., Arnaout, R., Selzer, R. R., Lee, W. L., Honan, T., Rubio, E. D., Krumm, A., Lamb, J., Nusbaum, C., et al. (2006) · Genome Research · doi:10.1101/gr.5571506 · Cited by 1,237 · cited 2×
“…nm - 400 nm HoxD 5µm 1µm 5µm 1µm CSETW Phc1-KO ESC 5µm 1µm 5µm 1µm 400 nm - 400 nm ecnecseroulfipE MROTSD3 ecnecseroulfipE MROTSD3 400 nm - 400 nm (legend on next page) Molecular Cell 65, 432–446, February 2, 2017 435 developmentally regulated PRC1-occupied regions by 5C (Dostie et al., 2006).”
Self-citationArchitectural protein subclasses shape 3D organization of genomes during lineage commitment
Phillips-Cremins, J. E., Sauria, M. E. G., Sanyal, A., Gerasimova, T. I., Lajoie, B. R., Bell, J. S. K., Ong, C.-T., Hookway, T. A., Guo, C., Sun, Y., et al. (2013) · Cell · doi:10.1016/j.cell.2013.04.053 · Cited by 1,187 · cited 3×
“…did not correlate with cohesin (based on Smc1a and Smc3 localization) or Mediator (Med12 and Med1), two complexes associated with TAD structure (Figures 7B and S6A) (Dixon et al., 2012; Hou et al., 2012; Kagey et al., 2010; Phillips-Cremins et al., 2013; Rao et al., 2014; Sofueva et al., 2013).”
BackgroundSelf-citationPax6 Controls Progenitor Cell Identity and Neuronal Fate in Response to Graded Shh Signaling
Ericson, J., Rashbass, P., Schedl, A., Brenner‐Morton, S., Kawakami, A., van Heyningen, V., Jessell, T. M., & Briscoe, J. (1997) · Cell · doi:10.1016/s0092-8674(00)80323-2 · Cited by 1,044 · cited 10×
“Formation of the domain at the Pax6 locus was not impacted by removal of H2A119Ub and was eliminated by removal of Ring1b, behaviors consistent with it requiring the canonical PRC1 complex.”
InfluentialShen, X., Liu, Y., Hsu, Y.-J., Fujiwara, Y., Kim, J., Mao, X., Yuan, G.-C., & Orkin, S. H. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.10.016 · Cited by 1,021 · cited 3×
“Though H3K27me3 is only partially diminished at developmentally regulated PcG targets in the Ezh2 KO ESCs (Shen et al., 2008), we found that enrichment of canonical PRC1 subunits was reduced.”
BackgroundMethodDesign and analysis of ChIP-seq experiments for DNA-binding proteins
Kharchenko, P. V., Tolstorukov, M. Y., & Park, P. J. (2008) · Nature Biotechnology · doi:10.1038/nbt.1508 · Cited by 914 · cited 2×
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MethodSuper-resolution imaging reveals distinct chromatin folding for different epigenetic states
Boettiger, A. N., Bintu, B., Moffitt, J. R., Wang, S., Beliveau, B. J., Fudenberg, G., Imakaev, M., Mirny, L. A., Wu, C.-T., & Zhuang, X. (2016) · Nature · doi:10.1038/nature16496 · Cited by 871 · cited 4×
“New insight came from the recent observation that large Polycomb-repressed regions inDrosophila form densely packed chromatin that is distinct from other inactive or active chromatin states (Boettiger et al., 2016).”
BackgroundMethodInfluentialTranscriptional regulation by Polycomb group proteins
Di Croce, L., & Helin, K. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2669 · Cited by 864 · cited 1×
“Polycomb group (PcG) complexes, including PRC1 and PRC2, silence developmentally regulated genes (Di Croce and Helin, 2013).”
BackgroundPCGF Homologs, CBX Proteins, and RYBP Define Functionally Distinct PRC1 Family Complexes
Gao, Z., Zhang, J., Bonasio, R., Strino, F., Sawai, A., Parisi, F., Kluger, Y., & Reinberg, D. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.01.002 · Cited by 852 · cited 1×
“PRC1 is a large family of complexes broadly classified as canonical and variant PRC1 (Figure 1A) (Farcas et al., 2012; Gao et al., 2012; Morey et al., 2012, 2013; Tavares et al., 2012).”
BackgroundChromatin Compaction by a Polycomb Group Protein Complex
Francis, N. J., Kingston, R. E., & Woodcock, C. L. F. (2004) · Science · doi:10.1126/science.1100576 · Cited by 841 · cited 5×
“…(H2AK119Ub), create compacted chromatin structures in vitro, and bring together distant genomic regions in vivo (Bantignies et al., 2011; Buchwald et al., 2006; Cheutin andCavalli, 2014; Eskeland et al., 2010; Francis et al., 2004; Grau et al., 2011; Schoenfelder et al., 2015; Wang et al., 2004).”
BackgroundInfluentialSelf-citationHomeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling
Briscoe, J., Sussel, L., Serup, P., Hartigan-O'Connor, D., Jessell, T., Rubenstein, J., & Ericson, J. (1999) · Nature · doi:10.1038/19315 · Cited by 807 · cited 2×
“438 Molecular Cell 65, 432–446, February 2, 2017 factors, Nkx2-2 and Pax6 (Briscoe et al., 1999; Ericson et al., 1997).”
Blackledge, N. P., Farcas, A. M., Kondo, T., King, H. W., McGouran, J. F., Hanssen, L. L. P., Ito, S., Cooper, S., Kondo, K., Koseki, Y., et al. (2014) · Cell · doi:10.1016/j.cell.2014.05.004 · Cited by 778 · cited 2×
“440 Molecular Cell 65, 432–446, February 2, 2017 consistent with a hierarchical recruitment model in which variant PRC1 recruits PRC2 (Blackledge et al., 2014; Tavares et al., 2012), we found that PRC2 catalyzed H3K27me3, and canonical PRC1 components Cbx7 and Phc1 were reduced at PRC1 target loci (Figure 6D; data not…”
BackgroundSimon, J. A., & Kingston, R. E. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.02.013 · Cited by 754 · cited 2×
“…(Cao et al., 2002; Czermin et al., 2002; Kuzmichev et al., 2002; Lewis et al., 2013; M€uller et al., 2002; Pengelly et al., 432 Molecular Cell 65, 432–446, February 2, 2017 ª 2017 Elsevier Inc 2013; Schwartzentruber et al., 2012; Simon and Kingston, 2013; Voigt and Reinberg, 2013; Wu et al., 2012).”
BackgroundSelf-citationYaffe, E., & Tanay, A. (2011) · Nature Genetics · doi:10.1038/ng.947 · Cited by 614
Tavares, L., Dimitrova, E., Oxley, D., Webster, J. A., Poot, R. A., Demmers, J., Bezstarosti, K., Taylor, S., Ura, H., Koide, H., et al. (2012) · Cell · doi:10.1016/j.cell.2011.12.029 · Cited by 583
Eskeland, R., Leeb, M., Grimes, G. R., Kress, C., Boyle, S., Sproul, D., Gilbert, N., Fan, Y., Skoultchi, A. I., Wutz, A., et al. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.02.032 · Cited by 571 · cited 9×
“Other ESC lines used in this study:Ring1b / ,Ring1bI53A/I53A (Eskeland et al., 2010; Illingworth et al., 2015), Kdm2bT/T (Boulard et al., 2015), Ezh2 / (Shen et al., 2008).”
BackgroundMethodInfluentialCTCF establishes discrete functional chromatin domains at the Hox clusters during differentiation
Narendra, V., Rocha, P. P., An, D., Raviram, R., Skok, J. A., Mazzoni, E. O., & Reinberg, D. (2015) · Science · doi:10.1126/science.1262088 · Cited by 535 · cited 3×
“PRC1 and PRC2 were lost from anterior HoxA cluster genes (Hoxa1–Hoxa5) upon neural differentiation (Figure 3A) (Mazzoni et al., 2013; Narendra et al., 2015).”
BackgroundHou, C., Li, L., Qin, Z. S., & Corces, V. G. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.08.031 · Cited by 525 · cited 2×
“…did not correlate with cohesin (based on Smc1a and Smc3 localization) or Mediator (Med12 and Med1), two complexes associated with TAD structure (Figures 7B and S6A) (Dixon et al., 2012; Hou et al., 2012; Kagey et al., 2010; Phillips-Cremins et al., 2013; Rao et al., 2014; Sofueva et al., 2013).”
BackgroundKDM2B links the Polycomb Repressive Complex 1 (PRC1) to recognition of CpG islands
Farcas, A. M., Blackledge, N. P., Sudbery, I. M., Long, H. K., McGouran, J. F., Rose, N. R., Lee, S., Sims, D., Cerase, A., Sheahan, T. W., et al. (2012) · eLife · doi:10.7554/elife.00205 · Cited by 502 · cited 1×
“PRC1 is a large family of complexes broadly classified as canonical and variant PRC1 (Figure 1A) (Farcas et al., 2012; Gao et al., 2012; Morey et al., 2012, 2013; Tavares et al., 2012).”
BackgroundVersatile design and synthesis platform for visualizing genomes with Oligopaint FISH probes
Beliveau, B. J., Joyce, E. F., Apostolopoulos, N., Yilmaz, F., Fonseka, C. Y., McCole, R. B., Chang, Y. K., Li, J. B., Senaratne, T. N., Williams, B. R., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1213818110 · Cited by 456 · cited 2×
“Alexa 647 labeled Oligopaint FISH probe library was prepared as described (Beliveau et al., 2012) with minor modifications.”
MethodStructure and E3‐ligase activity of the Ring–Ring complex of Polycomb proteins Bmi1 and Ring1b
Buchwald, G., van der Stoop, P. P. M., Weichenrieder, O., Anastassis Perrakis, A., van Lohuizen, M., & Sixma, T. K. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601144 · Cited by 453 · cited 2×
“PRC1 family complexes can catalyze ubiquitylation of histone H2A on lysine 119 (H2AK119Ub), create compacted chromatin structures in vitro, and bring together distant genomic regions in vivo (Bantignies et al., 2011; Buchwald et al., 2006; Cheutin andCavalli, 2014; Eskeland et al., 2010; Francis et al., 2004; Grau et…”
BackgroundPolycomb-dependent regulatory contacts between distant Hox loci in Drosophila
Bantignies, F., Roure, V., Comet, I., Leblanc, B., Schuettengruber, B., Bonnet, J., Tixier, V., Mas, A., & Cavalli, G. (2011) · Cell · doi:10.1016/j.cell.2010.12.026 · Cited by 429 · cited 5×
“Similarly, Drosophila Polycomb (Pc) is required for long-range loops between Antp and Abd-B genes (Bantignies et al., 2011).”
BackgroundInfluentialA Switch Between Topological Domains Underlies HoxD Genes Collinearity in Mouse Limbs
Andrey, G., Montavon, T., Mascrez, B., Gonzãlez, F., Noordermeer, D., Leleu, M., Trono, D., Spitz, F., & Duboule, D. (2013) · Science · doi:10.1126/science.1234167 · Cited by 423 · cited 2×
“…are proposed to define domains of long-range interaction that tie distant enhancer regions to Hox genes, within specific TAD domains, and thereby determine the activation of these genes in a spatially appropriate manner (Andrey et al., 2013; Darbellay and Duboule, 2016; Noordermeer et al., 2011).”
BackgroundPolycomb repressive complex PRC1 spatially constrains the mouse embryonic stem cell genome
Schoenfelder, S., Sugar, R., Dimond, A., Javierre, B.-M., Armstrong, H., Mifsud, B., Dimitrova, E., Matheson, L., Tavares-Cadete, F., Furlan-Magaril, M., et al. (2015) · Nature Genetics · doi:10.1038/ng.3393 · Cited by 398 · cited 4×
“PRC1 family complexes can catalyze ubiquitylation of histone H2A on lysine 119 (H2AK119Ub), create compacted chromatin structures in vitro, and bring together distant genomic regions in vivo (Bantignies et al., 2011; Buchwald et al., 2006; Cheutin andCavalli, 2014; Eskeland et al., 2010; Francis et al., 2004; Grau et…”
BackgroundInfluentialCohesin-mediated interactions organize chromosomal domain architecture
Sofueva, S., Yaffe, E., Chan, W., Georgopoulou, D., Vietri Rudan, M., Mira‐Bontenbal, H., Pollard, S. M., Schroth, G. P., Tanay, A., & Hadjur, S. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.237 · Cited by 394 · cited 2×
“…did not correlate with cohesin (based on Smc1a and Smc3 localization) or Mediator (Med12 and Med1), two complexes associated with TAD structure (Figures 7B and S6A) (Dixon et al., 2012; Hou et al., 2012; Kagey et al., 2010; Phillips-Cremins et al., 2013; Rao et al., 2014; Sofueva et al., 2013).”
BackgroundThe Dynamic Architecture of Hox Gene Clusters
Noordermeer, D., Leleu, M., Splinter, E., Rougemont, J., de Laat, W. L., & Duboule, D. (2011) · Science · doi:10.1126/science.1207194 · Cited by 391 · cited 3×
“…are proposed to define domains of long-range interaction that tie distant enhancer regions to Hox genes, within specific TAD domains, and thereby determine the activation of these genes in a spatially appropriate manner (Andrey et al., 2013; Darbellay and Duboule, 2016; Noordermeer et al., 2011).”
BackgroundBeliveau, B. J., Boettiger, A. N., Avendaño, M. S., Jungmann, R., McCole, R. B., Joyce, E. F., Kim-Kiselak, C., Bantignies, F., Fonseka, C. Y., Erceg, J., et al. (2015) · Nature Communications · doi:10.1038/ncomms8147 · Cited by 384 · cited 1×
“We used stochastic optical reconstruction microscopy (STORM) and an ‘‘oligo-paint’’ strategy that was previously applied to PcG targets in Drosophila and mammals (Beliveau et al., 2012, 2015; Boettiger et al., 2016).”
MethodSelf-citationNonoverlapping Functions of the Polycomb Group Cbx Family of Proteins in Embryonic Stem Cells
Morey, L., Pascual, G., Cozzuto, L., Roma, G., Wutz, A., Benitah, S. A., & Croce, L. D. (2012) · Cell stem cell · doi:10.1016/j.stem.2011.12.006 · Cited by 343 · cited 2×
“Since Cbx7 is lost upon differentiation, we used Cbx2 and Cbx8 as markers of canonical PRC1 (Creppe et al., 2014; Morey et al., 2012; O’Loghlen et al., 2012).”
BackgroundMethodWhat are memories made of? How Polycomb and Trithorax proteins mediate epigenetic memory
Steffen, P. A., & Ringrose, L. (2014) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3789 · Cited by 338 · cited 1×
“H3K27me3 modification does not directly silence gene expression but helps to guide the heritability of silenced domains and to recruit another key family of PcG complexes called PRC1 (Campos et al., 2014; Entrevan et al., 2016; Simon and Kingston, 2013; Steffen and Ringrose, 2014).”
BackgroundSAM Domain Polymerization Links Subnuclear Clustering of PRC1 to Gene Silencing
Isono, K., Endo, T. A., Ku, M., Yamada, D., Suzuki, R., Sharif, J., Ishikura, T., Toyoda, T., Bernstein, B., & Koseki, H. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.08.016 · Cited by 318 · cited 2×
“All canonical PRC1 in mESCs contains Phc1, and the Ph protein inDrosophila andmice has been implicated in long-range interactions via the function of its SAM domain (Isono et al., 2013; Wani et al., 2016).”
BackgroundA Histone Mutant Reproduces the Phenotype Caused by Loss of Histone-Modifying Factor Polycomb
Pengelly, A. R., Copur, Ö., Jäckle, H., Herzig, A., & Müller, J. (2013) · Science · doi:10.1126/science.1231382 · Cited by 297
Chromatin Immunoprecipitation (ChIP)Preprint
Carey, M., Peterson, C. L., & Smale, S. T. (2009) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot5279 · Cited by 264
Epigenetic Temporal Control of Mouse Hox Genes in Vivo
Soshnikova, N. V., & Duboule, D. (2009) · Science · doi:10.1126/science.1171468 · Cited by 257
Compaction of chromatin by diverse Polycomb group proteins requires localized regions of high chargePreprint
Grau, D., Chapman, B., Garlick, J. D., Borowsky, M. L., Francis, N. J., & Kingston, R. E. (2011) · Genes & Development · doi:10.1101/gad.17288211 · Cited by 252 · cited 5×
“…(H2AK119Ub), create compacted chromatin structures in vitro, and bring together distant genomic regions in vivo (Bantignies et al., 2011; Buchwald et al., 2006; Cheutin andCavalli, 2014; Eskeland et al., 2010; Francis et al., 2004; Grau et al., 2011; Schoenfelder et al., 2015; Wang et al., 2004).”
BackgroundInfluentialSelf-citationMicroRNA Regulation of Cbx7 Mediates a Switch of Polycomb Orthologs during ESC Differentiation
O’Loghlen, A., Muñoz-Cabello, A. M., Gaspar‐Maia, A., Wu, H., Banito, A., Kunowska, N., Racek, T., Pemberton, H. N., Beolchi, P., Lavial, F., et al. (2012) · Cell stem cell · doi:10.1016/j.stem.2011.12.004 · Cited by 213 · cited 1×
“Since Cbx7 is lost upon differentiation, we used Cbx2 and Cbx8 as markers of canonical PRC1 (Creppe et al., 2014; Morey et al., 2012; O’Loghlen et al., 2012).”
MethodMorey, L., Aloia, L., Cozzuto, L., Benitah, S. A., & Di Croce, L. (2013) · Cell Reports · doi:10.1016/j.celrep.2012.11.026 · Cited by 201 · cited 1×
“PRC1 is a large family of complexes broadly classified as canonical and variant PRC1 (Figure 1A) (Farcas et al., 2012; Gao et al., 2012; Morey et al., 2012, 2013; Tavares et al., 2012).”
BackgroundChromatin topology is coupled to Polycomb group protein subnuclear organization
Wani, A. H., Boettiger, A. N., Schorderet, P., Ergün, A., Munger, C., Sadreyev, R. I., Zhuang, X., Kingston, R. E., & Francis, N. J. (2016) · Nature Communications · doi:10.1038/ncomms10291 · Cited by 191
Self-citationThe E3 ubiquitin ligase activity of RING1B is not essential for early mouse developmentPreprint
Illingworth, R. S., Moffat, M., Mann, A. R., Read, D., Hunter, C. J., Pradeepa, M. M., Adams, I. R., & Bickmore, W. A. (2015) · Genes & Development · doi:10.1101/gad.268151.115 · Cited by 157 · cited 8×
“Thesewere generous gifts fromWendy Bickmore, Timothy Bestor and Stuart Orkin labs.”
BackgroundMethodResultInfluentialFBXL10 protects Polycomb-bound genes from hypermethylation
Boulard, M., Edwards, J. R., & Bestor, T. H. (2015) · Nature Genetics · doi:10.1038/ng.3272 · Cited by 153 · cited 5×
“Thesewere generous gifts fromWendy Bickmore, Timothy Bestor and Stuart Orkin labs.”
BackgroundMethodInfluentialEpigenetic inheritance: histone bookmarks across generations
Campos, E. I., Stafford, J. M., & Reinberg, D. (2014) · Trends in Cell Biology · doi:10.1016/j.tcb.2014.08.004 · Cited by 152 · cited 1×
“H3K27me3 modification does not directly silence gene expression but helps to guide the heritability of silenced domains and to recruit another key family of PcG complexes called PRC1 (Campos et al., 2014; Entrevan et al., 2016; Simon and Kingston, 2013; Steffen and Ringrose, 2014).”
BackgroundSaltatory remodeling of Hox chromatin in response to rostrocaudal patterning signals
Mazzoni, E. O., Mahony, S., Peljto, M., Patel, T., Thornton, S. R., McCuine, S., Reeder, C., Boyer, L. A., Young, R. A., Gifford, D. K., et al. (2013) · Nature Neuroscience · doi:10.1038/nn.3490 · Cited by 148 · cited 2×
“PRC1 and PRC2 were lost from anterior HoxA cluster genes (Hoxa1–Hoxa5) upon neural differentiation (Figure 3A) (Mazzoni et al., 2013; Narendra et al., 2015).”
BackgroundSunwoo, H., Wu, J. Y. J., & Lee, J. T. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1503690112 · Cited by 143
Self-citationH3K27 modifications define segmental regulatory domains in the Drosophila bithorax complex
Bowman, S., Deaton, A. M., Domingues, H. G., Wang, P. I., Sadreyev, R. I., Kingston, R. E., & Bender, W. W. (2014) · eLife · doi:10.7554/elife.02833 · Cited by 122 · cited 1×
“The boundaries that define which Hox genes are expressed or repressed correlate with CTCF binding sites in Drosophila and are disrupted by mutation of CTCF binding sites in mammals (Bowman et al., 2014; Narendra et al., 2015).”
BackgroundSelf-citationRegulation of Genome Architecture and Function by Polycomb Proteins
Entrevan, M., Schuettengruber, B., & Cavalli, G. (2016) · Trends in Cell Biology · doi:10.1016/j.tcb.2016.04.009 · Cited by 117 · cited 1×
“H3K27me3 modification does not directly silence gene expression but helps to guide the heritability of silenced domains and to recruit another key family of PcG complexes called PRC1 (Campos et al., 2014; Entrevan et al., 2016; Simon and Kingston, 2013; Steffen and Ringrose, 2014).”
BackgroundPolycomb silencing: from linear chromatin domains to 3D chromosome folding
Cheutin, T., & Cavalli, G. (2014) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2013.11.016 · Cited by 102 · cited 1×
“Several groups have demonstrated that the ends of PcG-bound Hox loci can contact each other even though they are distant on the linear genome (Bantignies et al., 2011; Cheutin and Cavalli, 2014; Eskeland et al., 2010; Lonfat and Duboule, 2015; Schoenfelder et al., 2015).”
BackgroundMy5C: web tools for chromosome conformation capture studies
Lajoie, B. R., van Berkum, N. L., Sanyal, A., & Dekker, J. (2009) · Nature Methods · doi:10.1038/nmeth1009-690 · Cited by 89 · cited 2×
“…(Mm00658129_gH) Life Technology Cat# 4448892 ActB (Mm00607939_s1) Life Technology Cat# 4448892 Software and Algorithms my5Csuite primer design tools Lajoie et al., 2009 http://my5c.umassmed.edu/my5Cprimers/5C.php N-STORM module in Element software Nikon N/A BWA Li and Durbin, 2009…”
MethodSelf-citationMultiplexed Illumina sequencing libraries from picogram quantities of DNA
Bowman, S., Simon, M. D., Deaton, A. M., Tolstorukov, M. Y., Borowsky, M. L., & Kingston, R. E. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-466 · Cited by 78 · cited 1×
“Sequencing libraries were prepared as described (Bowman et al., 2013).”
Self-citationCreppe, C., Palau, A., Malinverni, R., Valero, V., & Buschbeck, M. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004851 · Cited by 77 · cited 1×
“Since Cbx7 is lost upon differentiation, we used Cbx2 and Cbx8 as markers of canonical PRC1 (Creppe et al., 2014; Morey et al., 2012; O’Loghlen et al., 2012).”
MethodNeural Stem Cells, Neurons, and Glia
Pollard, S. M., Benchoua, A., & Lowell, S. (2006) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(06)18010-6 · Cited by 73 · cited 1×
“Neural progenitors (NPC) were derived by in vitro differentiation from J1 ESC and maintained using previously described methods (Pollard et al., 2006).”
MethodStructure, function and evolution of topologically associating domains (TADs) atHOX loci
Lonfat, N., & Duboule, D. (2015) · FEBS Letters · doi:10.1016/j.febslet.2015.04.024 · Cited by 69
Determining Spatial Chromatin Organization of Large Genomic Regions Using 5C Technology
van Berkum, N. L., & Dekker, J. (2009) · Methods in molecular biology · doi:10.1007/978-1-60327-414-2_13 · Cited by 46 · cited 1×
“3C and 5C templates were prepared as described (van Berkum and Dekker, 2009).”
MethodSelf-citationTopological Domains, Metagenes, and the Emergence of Pleiotropic Regulations at Hox Loci
Darbellay, F., & Duboule, D. (2016) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2015.11.022 · Cited by 35 · cited 2×
“…are proposed to define domains of long-range interaction that tie distant enhancer regions to Hox genes, within specific TAD domains, and thereby determine the activation of these genes in a spatially appropriate manner (Andrey et al., 2013; Darbellay and Duboule, 2016; Noordermeer et al., 2011).”
BackgroundPutting a halt on PRC2 in pediatric glioblastoma
Voigt, P., & Reinberg, D. (2013) · Nature Genetics · doi:10.1038/ng.2647 · Cited by 10 · cited 1×
“…(Cao et al., 2002; Czermin et al., 2002; Kuzmichev et al., 2002; Lewis et al., 2013; M€uller et al., 2002; Pengelly et al., 432 Molecular Cell 65, 432–446, February 2, 2017 ª 2017 Elsevier Inc 2013; Schwartzentruber et al., 2012; Simon and Kingston, 2013; Voigt and Reinberg, 2013; Wu et al., 2012).”
Background
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1 of the 73 references couldn’t be matched to a known paper.
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Genome Regulation by Polycomb and Trithorax: 70 Years and Counting
Schuettengruber, B., Bourbon, H.-M., Di Croce, L., & Cavalli, G. (2017) · Cell · doi:10.1016/j.cell.2017.08.002 · Cited by 1,094
“In particular, oligomerization mediated by the SAM domain of the Ph/PHC1 subunit of cPRC1 (Figures 5D and 5E) is crucial for the condensation of individual Polycomb domains (Kundu et al., 2017) as well as for mediating long-range Polycomb domain interactions (Isono et al., 2013; Wani et al., 2016).”
Histone post-translational modifications - cause and consequence of genome function
Millán-Zambrano, G., Burton, A., Bannister, A. J., & Schneider, R. (2022) · Nature Reviews Genetics · doi:10.1038/s41576-022-00468-7 · Cited by 1,116
Organization of Chromatin by Intrinsic and Regulated Phase Separation
Gibson, B. A., Doolittle, L. K., Schneider, M. W. G., Jensen, L. E., Gamarra, N. I., Henry, L., Gerlich, D. W., Redding, S., & Rosen, M. K. (2019) · Cell · doi:10.1016/j.cell.2019.08.037 · Cited by 1,080
“Polycomb Group Regions: Polycomb group regions were defined as H3K27me3 ChIP-seq peaks from E14tga2 mouse ES cells (Consortium, 2012) that overlap with H3K27me3, H2Aub, EZH2, and Ring1b ChIP-seq peaks from mouse ES cells (Kundu et al., 2017).”
BackgroundThe role of 3D genome organization in development and cell differentiation
Zheng, H., & Xie, W. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0132-4 · Cited by 742
Loss of epigenetic information as a cause of mammalian aging
Yang, J.-H., Hayano, M., Griffin, P. T., Amorim, J. A., Bonkowski, M. S., Apostolides, J. K., Salfati, E. L., Blanchette, M., Munding, E. M., Bhakta, M., et al. (2023) · Cell · doi:10.1016/j.cell.2022.12.027 · Cited by 643
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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