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A unique chromatin signature uncovers early developmental enhancers in humans
Open accessAbstract
Cell-fate transitions involve the integration of genomic information encoded by regulatory elements, such as enhancers, with the cellular environment. However, identification of genomic sequences that control human embryonic development represents a formidable challenge. Here we show that in human embryonic stem cells (hESCs), unique chromatin signatures identify two distinct classes of genomic elements, both of which are marked by the presence of chromatin regulators p300 and BRG1, monomethylation of histone H3 at lysine 4 (H3K4me1), and low nucleosomal density. In addition, elements of the first class are distinguished by the acetylation of histone H3 at lysine 27 (H3K27ac), overlap with previously characterized hESC enhancers, and are located proximally to genes expressed in hESCs and the epiblast. In contrast, elements of the second class, which we term 'poised enhancers', are distinguished by the absence of H3K27ac, enrichment of histone H3 lysine 27 trimethylation (H3K27me3), and are linked to genes inactive in hESCs and instead are involved in orchestrating early steps in embryogenesis, such as gastrulation, mesoderm formation and neurulation. Consistent with the poised identity, during differentiation of hESCs to neuroepithelium, a neuroectoderm-specific subset of poised enhancers acquires a chromatin signature associated with active enhancers. When assayed in zebrafish embryos, poised enhancers are able to direct cell-type and stage-specific expression characteristic of their proximal developmental gene, even in the absence of sequence conservation in the fish genome. Our data demonstrate that early developmental enhancers are epigenetically pre-marked in hESCs and indicate an unappreciated role of H3K27me3 at distal regulatory elements. Moreover, the wealth of new regulatory sequences identified here provides an invaluable resource for studies and isolation of transient, rare cell populations representing early stages of human embryogenesis.
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“The TRIM33-occupied regions upstream of Bim and Atp1b3 were enriched for H3K27 acetylation but not for H3K4 tri-methylation, suggesting that these elements are active enhancers”
From The transcriptional cofactor TRIM33 prevents apoptosis in B lymphoblastic leukemia by deactivating a single enhancer (2015) · cites this paper as Rada-Iglesias et al., 2011
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“Since H3K27ac modification reliably marks active enhancers located in the distal regions of a given gene, 34”
From Kupffer-cell-derived IL-6 is repurposed for hepatocyte dedifferentiation via activating progenitor genes from injury-specific enhancers (2023) · cites this paper as [34]
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“Currently mono-methylation of histone H3 lysine 4 (H3K4me1), associated with the binding of Trithorax/MLL complexes, is taken to be the hallmark of both ‘primed’ and active enhancers, whilst active enhancers additionally tend to associate with the acetylation of histone H3 lysine 27 (H3K27ac) [133–137].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [135]
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“Previous studies suggested that higher levels and a bimodal distribution pattern of monomethylated histone 3 lysine 4 (H3K4me1) correlate with enhancer function (Hoffman et al., 2010; Rada-Iglesias et al., 2011).”
From Hippo Signaling Influences HNF4A and FOXA2 Enhancer Switching during Hepatocyte Differentiation (2014) · cites this paper as Rada-Iglesias et al., 2011
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“In addition to the ‘primed’ and active states, enhancers can also reside in a ‘poised’ state exhibiting both H3K4me1 and H3 lysine 27 trimethylation (H3K27me3) that is associated with Polycomb repressive complexes [131, 135, 136, 138].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [135]
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“We inhibited p300 catalytic activity with the small molecule A48530, but did not observe a decrease in TF binding (Fig. 2N–O vs. Fig. 2B–C) or nucleosome occupancy (Fig. S3M), despite a marked reduction in H3K27 acetylation (Fig. S3N)”
From Single-molecule states link transcription factor binding to gene expression (2024) · cites this paper as [30]
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Cites
Core Transcriptional Regulatory Circuitry in Human Embryonic Stem Cells
Boyer, L. A., Lee, T. I., Cole, M. F., Johnstone, S. E., Levine, S. S., Zucker, J. P., Guenther, M. G., Kumar, R. M., Murray, H. L., Jenner, R. G., et al. (2005) · Cell · doi:10.1016/j.cell.2005.08.020 · Cited by 4,505
GREAT improves functional interpretation of cis-regulatory regions
McLean, C. Y., Bristor, D., Hiller, M., Clarke, S. L., Schaar, B. T., Lowe, C. B., Wenger, A. M., & Bejerano, G. (2010) · Nature Biotechnology · doi:10.1038/nbt.1630 · Cited by 4,502
Heintzman, N. D., Stuart, R. K., Hon, G., Fu, Y., Ching, C. W., Hawkins, R. D., Barrera, L. O., Van Calcar, S., Qu, C., Ching, K. A., et al. (2007) · Nature Genetics · doi:10.1038/ng1966 · Cited by 3,398
Histone modifications at human enhancers reflect global cell-type-specific gene expression
Heintzman, N. D., Hon, G. C., Hawkins, R. D., Kheradpour, P., Stark, A., Harp, L. F., Ye, Z., Lee, L. K., Stuart, R. K., Ching, C. W., et al. (2009) · Nature · doi:10.1038/nature07829 · Cited by 2,533
Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors
Ieda, M., Fu, J.-D., Delgado-Olguin, P., Vedantham, V., Hayashi, Y., Bruneau, B. G., & Srivastava, D. (2010) · Cell · doi:10.1016/j.cell.2010.07.002 · Cited by 2,454
Widespread transcription at neuronal activity-regulated enhancers
Kim, T.-K., Hemberg, M., Gray, J. M., Costa, A. M., Bear, D. M., Wu, J., Harmin, D. A., Laptewicz, M., Barbara-Haley, K., Kuersten, S., et al. (2010) · Nature · doi:10.1038/nature09033 · Cited by 2,450
A Chromatin Landmark and Transcription Initiation at Most Promoters in Human Cells
Guenther, M. G., Levine, S. S., Boyer, L. A., Jaenisch, R., & Young, R. A. (2007) · Cell · doi:10.1016/j.cell.2007.05.042 · Cited by 2,002
ChIP-seq accurately predicts tissue-specific activity of enhancers
Visel, A., Blow, M. J., Li, Z., Zhang, T., Akiyama, J. A., Holt, A., Plajzer-Frick, I., Shoukry, M., Wright, C., Chen, F., et al. (2009) · Nature · doi:10.1038/nature07730 · Cited by 1,639
c-Myc Regulates Transcriptional Pause Release
Rahl, P. B., Lin, C. Y., Seila, A. C., Flynn, R. A., McCuine, S., Burge, C. B., Sharp, P. A., & Young, R. A. (2010) · Cell · doi:10.1016/j.cell.2010.03.030 · Cited by 1,279
Self-citationVISTA Enhancer Browser—a database of tissue-specific human enhancers
Visel, A., Minovitsky, S., Dubchak, I., & Pennacchio, L. A. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkl822 · Cited by 1,080
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Items 501–600 of 1,013
H3K4me2 reliably defines transcription factor binding regions in different cells
Wang, Y., Li, X., & Hu, H. (2014) · Genomics · doi:10.1016/j.ygeno.2014.02.002 · Cited by 97
Chromatin features and the epigenetic regulation of pluripotency states in ESCs
Tee, W., & Reinberg, D. (2014) · Development · doi:10.1242/dev.096982 · Cited by 98
Defining stem cell types: understanding the therapeutic potential of ESCs, ASCs, and iPS cells
Álvarez, C. V., García-Lavandeira, M., Garcia-Rendueles, M. E. R., Díaz‐Rodriguez, E., Garcia-Rendueles, Á. R., Pérez-Romero, S., Vila, T. V., Rodrigues, J. S., Lear, P., & Bravo, S. B. (2012) · Journal of Molecular Endocrinology · doi:10.1530/jme-12-0072 · Cited by 97
Gene regulation at a distance: From remote enhancers to 3D regulatory ensembles
Spitz, F. (2016) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2016.06.017 · Cited by 99
Wang, M., Li, Z., Zhang, Y., Zhang, Y., Xie, Y., Ye, L., Zhuang, Y., Lin, K., Zhao, F., Guo, J., et al. (2021) · The Plant Cell · doi:10.1093/plcell/koab028 · Cited by 95
Woo, V., Eshleman, E. M., Hashimoto‐Hill, S., Whitt, J., Wu, S.-E., Engleman, L., Rice, T., Karns, R. A., Qualls, J. E., Haslam, D. B., et al. (2021) · Cell Host & Microbe · doi:10.1016/j.chom.2021.09.010 · Cited by 94
Engelen, E., Brandsma, J. H., Moen, M. J., Signorile, L., Dekkers, D. H. W., Demmers, J., Kockx, C. E. M., Özgür, Z., van IJcken, W. F. J., van den Berg, D. L. C., et al. (2015) · Nature Communications · doi:10.1038/ncomms8155 · Cited by 98
Chromatin-enriched lncRNAs can act as cell-type specific activators of proximal gene transcription
Werner, M. S., Sullivan, M. A., Shah, R. N., Nadadur, R. D., Grzybowski, A. T., Galat, V., Moskowitz, I. P. G., & Ruthenburg, A. J. (2017) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3424 · Cited by 96
Chromatin Regulation of Neuronal Maturation and Plasticity
Gallegos, D. A., Chan, U., Chen, L., & West, A. E. (2018) · Trends in Neurosciences · doi:10.1016/j.tins.2018.02.009 · Cited by 98
Copper affects the binding of HIF-1α to the critical motifs of its target genes
Wu, Z., Zhang, W., & Kang, Y. J. (2018) · Metallomics · doi:10.1039/c8mt00280k · Cited by 93
Svotelis, A., Bianco, S., Madore, J., Huppé, G., Nordell-Markovits, A., Mes‐Masson, A., & Gévry, N. Y. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.284 · Cited by 98
Dlx1andDlx2Promote Interneuron GABA Synthesis, Synaptogenesis, and Dendritogenesis
Pla, R., Stanco, A., Howard, M. A., Rubin, A. N., Vogt, D. L., Mortimer, N., Cobos, I., Potter, G. B., Lindtner, S., Price, J. D., et al. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx241 · Cited by 103
Chen, R. A.-J., Downand, T. A., Stempor, P., Chen, Q. B., Egelhofer, T. A., Hillier, L. W., Jeffers, T. E., & Ahringer, J. (2013) · Genome Research · doi:10.1101/gr.153668.112 · Cited by 95
The RNA Pol II Elongation Factor Ell3 Marks Enhancers in ES Cells and Primes Future Gene Activation
Lin, C., Garruss, A. S., Luo, Z., Guo, F., & Shilatifard, A. (2012) · Cell · doi:10.1016/j.cell.2012.12.015 · Cited by 96
Progress and challenges in bioinformatics approaches for enhancer identification
Kleftogiannis, D., Kalnis, P., & Bajić, V. B. (2015) · Briefings in Bioinformatics · doi:10.1093/bib/bbv101 · Cited by 92
Adelman, K., & Egan, E. D. (2017) · Nature · doi:10.1038/543183a · Cited by 92
Hogan, N. T., Whalen, M. B., Stolze, L. K., Hadeli, N. K., Lam, M. T. Y., Springstead, J. R., Glass, C. K., & Romanoski, C. E. (2017) · eLife · doi:10.7554/elife.22536 · Cited by 92
De novo DNA demethylation and noncoding transcription define active intergenic regulatory elementsPreprint
Schlesinger, F. J., Smith, A. D., Gingeras, T., Hannon, G. J., & Hodges, E. C. (2013) · Genome Research · doi:10.1101/gr.157271.113 · Cited by 96
Zhang, H., Zhang, N., Liu, Y., Su, P., Liang, Y., Li, Y., Wang, X., Chen, T., Song, X., Sang, Y., et al. (2021) · Cancer Research · doi:10.1158/0008-5472.can-21-1188 · Cited by 92
Short-term memory of danger signals and environmental stimuli in immune cells
Monticelli, S., & Natoli, G. (2013) · Nature Immunology · doi:10.1038/ni.2636 · Cited by 92
McClellan, M. J., Wood, C. D., Ojeniyi, O. O., Cooper, T. J., Kanhere, A., Arvey, A. J., Webb, H., Palermo, R. D., Harth-Hertle, M. L., Kempkes, B., et al. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003636 · Cited by 91
Demystifying the secret mission of enhancers: linking distal regulatory elements to target genes
Yao, L., Berman, B. P., & Farnham, P. (2015) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2015.1087961 · Cited by 93
Ou, Z., Sun, Y., Li, L., You, N., Liu, X., Li, H., Ma, Y., Cao, L., Han, Y., Liu, M., et al. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0898-16.2016 · Cited by 91
Human evolution: the non-coding revolution
Franchini, L. F., & Pollard, K. S. (2017) · BMC Biology · doi:10.1186/s12915-017-0428-9 · Cited by 90
Kartikasari, A. E. R., Zhou, J. X., Kanji, M. S., Chan, D. N., Sinha, A., Grapin‐Botton, A., Magnuson, M. A., Lowry, W. E., & Bhushan, A. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.78 · Cited by 90
Murtha, M. J., Keskin, Z. T., Tang, Z., Strino, F., Chen, X. X., Wang, Y., Xi, X., Basilico, C., Brown, S. M., Bonneau, R., et al. (2014) · Nature Methods · doi:10.1038/nmeth.2885 · Cited by 94
Aday, A. W., Zhu, L. J., Lakshmanan, A., Wang, J., & Lawson, N. D. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2011.03.007 · Cited by 93
Proserpio, V., Fittipaldi, R., Ryall, J. G., Sartorelli, V., & Caretti, G. (2013) · Genes & Development · doi:10.1101/gad.217240.113 · Cited by 99
Hawkins, R. D., Larjo, A., Tripathi, S. K., Wagner, U., Luu, Y., Lönnberg, T., Raghav, S. K., Lee, L. K., Lund, R., Ren, B., et al. (2013) · Immunity · doi:10.1016/j.immuni.2013.05.011 · Cited by 92
Blassberg, R. A., Patel, H., Watson, T., Gouti, M., Metzis, V., Delàs, M. J., & Briscoe, J. (2022) · Nature Cell Biology · doi:10.1038/s41556-022-00910-2 · Cited by 93
The Chromatin Fingerprint of Gene Enhancer Elements
Zentner, G. E., & Scacheri, P. C. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.r111.296491 · Cited by 92
Andzelm, M. M., Cherry, T. J., Harmin, D. A., Boeke, A. C., Lee, C., Hemberg, M., Pawlyk, B. S., Malik, A. N., Flavell, S. W., Sandberg, M. A., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.02.038 · Cited by 89
Long distance relationships: Enhancer–promoter communication and dynamic gene transcription
Marsman, J., & Horsfield, J. A. (2012) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2012.10.008 · Cited by 91
Glinsky, G. V. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv081 · Cited by 93
Williams, K., Christensen, J. F., Rappsilber, J., Nielsen, A. L., Johansen, J. V., & Helin, K. (2014) · PLoS ONE · doi:10.1371/journal.pone.0096545 · Cited by 91
The Epigenetic State of PRDM16-Regulated Enhancers in Radial Glia Controls Cortical Neuron Position
Baizabal, J., Mistry, M., Garcίa, M. T., Gómez, N., Olukoya, O., Tran, D., Johnson, M. B., Walsh, C. A., & Harwell, C. C. (2018) · Neuron · doi:10.1016/j.neuron.2018.04.033 · Cited by 89
Specification and formation of the neural crest: Perspectives on lineage segregation
Prasad, M. S., Charney, R. M., & García‐Castro, M. I. (2018) · genesis · doi:10.1002/dvg.23276 · Cited by 94
Runx1 Transcription Factor Is Required for Myoblasts Proliferation during Muscle Regeneration
Umansky, K. B., Gruenbaum‐Cohen, Y., Tsoory, M., Feldmesser, E., Goldenberg, D., Brenner, O. J., & Groner, Y. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005457 · Cited by 88
Epigenetic regulation in neural crest development
Hu, N., Strobl‐Mazzulla, P. H., & Bronner-Fraser, M. E. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.09.034 · Cited by 95
Proinflammatory Stimuli Engage Brahma Related Gene 1 and Brahma in Endothelial Injury
Fang, F., Chen, D., Yu, L., Dai, X. J., Yang, Y., Tian, W., Cheng, X. F., Xu, H., Weng, X., Fang, M., et al. (2013) · Circulation Research · doi:10.1161/circresaha.113.301296 · Cited by 88
Is H3K4me1 at enhancers correlative or causative?
Rada-Iglesias, Á. (2017) · Nature Genetics · doi:10.1038/s41588-017-0018-3 · Cited by 90
Transcription-driven chromatin repression of Intragenic transcription start sites
Nielsen, M., Ard, R., Leng, X., Ivanov, M., Kindgren, P., Pelechano, V., & Marquardt, S. (2019) · PLoS Genetics · doi:10.1371/journal.pgen.1007969 · Cited by 87
The histone variant H2A.Z is an important regulator of enhancer activity
Brunelle, M., Nordell-Markovits, A., Rodrigue, S., Lupien, M., Jacques, P., & Gévry, N. Y. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv825 · Cited by 90
Transcriptional and epigenetic networks of helper T and innate lymphoid cells
Shih, H., Sciumè, G., Poholek, A. C., Vahedi, G., Hirahara, K., Villarino, A. V., Bonelli, M. M., Bosselut, R., Kanno, Y., Muljo, S. A., et al. (2014) · Immunological Reviews · doi:10.1111/imr.12208 · Cited by 91
Widiez, T., Symeonidi, A., Luo, C., Lam, E., Lawton, M., & Rensing, S. A. (2014) · The Plant Journal · doi:10.1111/tpj.12542 · Cited by 90
Miller, E. L., Hargreaves, D. C., Kadoch, C., Chang, C.-Y., Calarco, J. P., Hodges, H. C., Buenrostro, J. D., Cui, K., Greenleaf, W. J., Zhao, K., et al. (2017) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3384 · Cited by 89
McEnhancer: predicting gene expression via semi-supervised assignment of enhancers to target genes
Hafez, D., Calviello, A. K., Krueger, S., Hwang, Y.-C., Wang, L., Zinzen, R. P., & Ohler, U. (2017) · Genome biology · doi:10.1186/s13059-017-1316-x · Cited by 86
Nagata, K., Hojo, H., Chang, S. H., Okada, H., Yano, F., Chijimatsu, R., Omata, Y., Mori, D., Makii, Y., Kawata, M., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33744-5 · Cited by 86
John, E., Wienecke-Baldacchino, A. K., Bouvy‐Liivrand, M., Heinäniemi, M., Carlberg, C., & Sinkkonen, L. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks025 · Cited by 88
The enhancer and promoter landscape of human regulatory and conventional T-cell subpopulations
Schmidl, C., Hansmann, L., Lassmann, T., Balwierz, P. J., Kawaji, H., Itoh, M., Kawai, J., Nagao-Sato, S., Suzuki, H., Andreesen, R., et al. (2014) · Blood · doi:10.1182/blood-2013-02-486944 · Cited by 88
DNA Methylation is Developmentally Regulated for Genes Essential for Cardiogenesis
Chamberlain, A. A., Lin, M., Lister, R., Maslov, A., Wang, Y., Suzuki, M., Wu, B., Greally, J. M., Zheng, D., & Zhou, B. (2014) · Journal of the American Heart Association · doi:10.1161/jaha.114.000976 · Cited by 89
Jjingo, D., Conley, A. B., Wang, J., Mariño‐Ramírez, L., Lunyak, V. V., & Jordan, I. K. (2014) · Mobile DNA · doi:10.1186/1759-8753-5-14 · Cited by 89
Rhee, H. S., Closser, M., Guo, Y., Bashkirova, E., Tan, G. C., Gifford, D. K., & Wichterle, H. (2016) · Neuron · doi:10.1016/j.neuron.2016.11.037 · Cited by 86
Determinants of transcription factor regulatory range
Chen, C.-H., Zheng, R., Tokheim, C., Dong, X., Fan, J., Wan, C., Tang, Q., Brown, M., Liu, J. S., Meyer, C. A., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-16106-x · Cited by 85
Large-Scale Identification of Coregulated Enhancer Networks in the Adult Human Brain
Vermunt, M. W., Reinink, P., Korving, J., de Bruijn, E., Creyghton, P. M., Başak, O., Geeven, G., Toonen, P. W., Lansu, N. R., Meunier, C., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.09.023 · Cited by 86
Cheng, L. L., Itahana, Y., Lei, Z. D., Chia, N., Wu, Y., Yu, Y., Zhang, S. L., Thike, A. A., Pandey, A., Rozen, S., et al. (2012) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-12-0036 · Cited by 89
Fasciani, A., D’Annunzio, S., Poli, V., Fagnocchi, L., Beyes, S., Michelatti, D., Corazza, F., Antonelli, L., Gregoretti, F., Oliva, G., et al. (2020) · Nature Genetics · doi:10.1038/s41588-020-00724-8 · Cited by 87
Updated review on green tea polyphenol epigallocatechin-3-gallate as a cancer epigenetic regulator
Li, F., Qasim, S., Li, D., & Dou, Q. P. (2021) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2020.11.018 · Cited by 87
Barral, A., Pozo, G., Ducrot, L., Papadopoulos, G. L., Sauzet, S., Oldfield, A., Cavalli, G., & Déjardin, J. (2022) · Molecular Cell · doi:10.1016/j.molcel.2021.12.037 · Cited by 87
Aiolos Promotes Anchorage Independence by Silencing p66Shc Transcription in Cancer Cells
Li, X., Zhao, X., Du, W., Zhang, Z., Wei, Y., Wang, H., Zhu, Z., Qin, L., Wang, L., Niu, Q., et al. (2014) · Cancer Cell · doi:10.1016/j.ccr.2014.03.020 · Cited by 85
Zhang, Q., Bai, B., Mei, X., Wan, C., Cao, H., Li, D., Wang, S., Zhang, M., Wang, Z., Wu, J., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-05451-7 · Cited by 84
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Caprara, G., Prosperini, E., Piccolo, V., Sigismondo, G., Melacarne, A., Cuomo, A., Boothby, M. R., Rescigno, M., Bonaldi, T., & Natoli, G. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1701117 · Cited by 83
Predicting gene expression from DNA sequence using deep learning models
Barbadilla-Martínez, L., Klaassen, N. H. M., van Steensel, B., & de Ridder, J. (2025) · Nature Reviews Genetics · doi:10.1038/s41576-025-00841-2 · Cited by 89
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Ma, K. H., Hung, H. A., & Svaren, J. P. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.1370-16.2016 · Cited by 84
Erceg, J., Pakozdi, T., Marco-Ferreres, R., Ghavi-Helm, Y., Girardot, C., Bracken, A. P., & Furlong, E. E. M. (2017) · Genes & Development · doi:10.1101/gad.292870.116 · Cited by 88
Epigenomics of cancer – emerging new concepts
Hassler, M. R., & Egger, G. (2012) · Biochimie · doi:10.1016/j.biochi.2012.05.007 · Cited by 85
OCT4 Acts as an Integrator of Pluripotency and Signal-Induced Differentiation
Simándi, Z., Horváth, A., Wright, L. C., Cuaranta‐Monroy, I., Luca, I. D., Károlyi, K., Sauer, S., Deleuze, J., Gudas, L. J., Cowley, S. M., et al. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.06.039 · Cited by 85
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Kikuchi, M., Morita, S., Wakamori, M., Sato, S., Uchikubo‐Kamo, T., Suzuki, T., Dohmae, N., Shirouzu, M., & Umehara, T. (2023) · Nature Communications · doi:10.1038/s41467-023-39735-4 · Cited by 86
González, A. J., Setty, M. N., & Leslie, C. S. (2015) · Nature Genetics · doi:10.1038/ng.3402 · Cited by 85
Acetylated histone H3K56 interacts with Oct4 to promote mouse embryonic stem cell pluripotency
Tan, Y., Xue, Y., Song, C., & Grunstein, M. R. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1309914110 · Cited by 82
An autonomous CEBPA enhancer specific for myeloid-lineage priming and neutrophilic differentiation
Avellino, R., Havermans, M., Erpelinck-Verschueren, C. A. J., Sanders, M. A., Hoogenboezem, R. M., van de Werken, H. J. G., Rombouts, E. J. C., van Lom, K., van Strien, P. M. H., Gebhard, C., et al. (2016) · Blood · doi:10.1182/blood-2016-01-695759 · Cited by 87
Transcriptional enhancers and their communication with gene promoters
Ray-Jones, H., & Spivakov, M. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03903-w · Cited by 81
Boles, N. C., Fernandes, M., Swigut, T., Srinivasan, R., Schiff, L., Rada-Iglesias, Á., Wang, Q., Saini, J. S., Kiehl, T. R., Stern, J. H., et al. (2020) · Stem Cell Reports · doi:10.1016/j.stemcr.2020.03.009 · Cited by 81
Self-citationDynamics of histone acetylation during human early embryogenesis
Wu, K., Fan, D., Zhao, H., Liu, Z., Hou, Z., Tao, W., Yu, G., Yuan, S., Zhu, X., Kang, M., et al. (2023) · Cell Discovery · doi:10.1038/s41421-022-00514-y · Cited by 83
Muratani, M., Deng, N., Ooi, W. F., Lin, S. J., Xing, M., Xu, C., Qamra, A., Tay, S. T., Malik, S., Wu, J., et al. (2014) · Nature Communications · doi:10.1038/ncomms5361 · Cited by 84
Genome-Wide Evaluation of Histone Methylation Changes Associated with Leaf Senescence in Arabidopsis
Brusslan, J. A., Alvarez-Canterbury, A. M. R., Nair, N. U., Rice, J. C., Hitchler, M. J., & Pellegrini, M. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033151 · Cited by 81
A novel Nrf2-miR-29-desmocollin-2 axis regulates desmosome function in keratinocytes
Kurinna, S. M., Schäfer, M., Ostano, P., Karouzakis, E., Chiorino, G., Bloch, W., Bachmann, A., Gay, S., Garrod, D. R., Lefort, K., et al. (2014) · Nature Communications · doi:10.1038/ncomms6099 · Cited by 82
Hou, P.-S., Chuang, C.-Y., Kao, C.-F., Chou, S., Stone, L., Ho, H., Chien, C. L., & Kuo, H. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt567 · Cited by 84
Respuela, P., Nikolić, M., Tan, M., Frommolt, P., Zhao, Y., Wysocka, J., & Rada-Iglesias, Á. (2016) · Cell stem cell · doi:10.1016/j.stem.2015.09.010 · Cited by 81
Self-citationA KAP1 phosphorylation switch controls MyoD function during skeletal muscle differentiationPreprint
Singh, K., Cassano, M., Planet, E., Sebastian, S., Jang, S. M., Sohi, G., Faralli, H., Choi, J., Youn, H., Dilworth, F. J., et al. (2015) · Genes & Development · doi:10.1101/gad.254532.114 · Cited by 87
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Wang, S., Zang, C., Xiao, T., Fan, J., Mei, S., Qin, Q., Wu, Q., Li, X., Xu, K., He, H. H., et al. (2016) · Genome Research · doi:10.1101/gr.201574.115 · Cited by 81
MIRA: joint regulatory modeling of multimodal expression and chromatin accessibility in single cells
Lynch, A. W., Theodoris, C. V., Long, H. W., Brown, M., Liu, X. S., & Meyer, C. A. (2022) · Nature Methods · doi:10.1038/s41592-022-01595-z · Cited by 80
Lee, S.-M., Lee, Y., Bae, J.-B., Choi, J. K., Tayama, C., Hata, K., Yun, Y., Seong, J. K., & Kim, Y.-J. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1400604111 · Cited by 80
Highly enriched BEND3 prevents the premature activation of bivalent genes during differentiation
Zhang, J., Zhang, Y., You, Q., Huang, C., Zhang, T., Wang, M., Zhang, T., Yang, X., Xiong, J., Li, Y., et al. (2022) · Science · doi:10.1126/science.abm0730 · Cited by 80
Verzi, M. P., Shin, H., Roman, A. K. S., Liu, X. S., & Shivdasani, R. A. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.01185-12 · Cited by 80
Genome-wide analysis of condensin binding in Caenorhabditis elegans
Kranz, A.-L., Jiao, C.-Y., Winterkorn, L. H., Albritton, S. E., Kramer, M., & Ercan, S. (2013) · Genome biology · doi:10.1186/gb-2013-14-10-r112 · Cited by 80
Transcriptomic and epigenomic characterization of the developing bat wing
Eckalbar, W. L., Schlebusch, S. A., Mason, M. K., Gill, Z., Parker, A. V., Booker, B. M., Nishizaki, S. S., Nday, C. M., Terhune, E., Nevonen, K. A., et al. (2016) · Nature Genetics · doi:10.1038/ng.3537 · Cited by 82
Aoshima, K., Inoue, E., Sawa, H., & Okada, Y. (2015) · EMBO Reports · doi:10.15252/embr.201439700 · Cited by 79
Enhancers and chromatin structures: regulatory hubs in gene expression and diseases
Hu, Z., & Tee, W. (2017) · Bioscience Reports · doi:10.1042/bsr20160183 · Cited by 80
The ZZ domain of p300 mediates specificity of the adjacent HAT domain for histone H3
Zhang, Y., Xue, Y., Shi, J., Ahn, J., Mi, W., Ali, M., Wang, X., Klein, B. J., Wen, H., Li, W., et al. (2018) · Nature Structural & Molecular Biology · doi:10.1038/s41594-018-0114-9 · Cited by 78
Transcriptional control by enhancers and enhancer RNAs
Lewis, M. W., Shen, L., & Franco, H. L. (2019) · Transcription · doi:10.1080/21541264.2019.1695492 · Cited by 84
The high affinity IgE receptor: a signaling update
Blank, U., Huang, H., & Kawakami, T. (2021) · Current Opinion in Immunology · doi:10.1016/j.coi.2021.03.015 · Cited by 78
Chromatin organization and global regulation of Hox gene clusters
Montavon, T., & Duboule, D. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0367 · Cited by 83
Spatiotemporal clustering of the epigenome reveals rules of dynamic gene regulationPreprint
Yu, P., Shu Dong, X. I. A. O., Xin, X., Song, C., Huang, W., McDee, D., Tanaka, T. S., Wang, T., He, C., & Zhong, S. (2012) · Genome Research · doi:10.1101/gr.144949.112 · Cited by 78
Widespread Enhancer Activity from Core Promoters
Medina-Rivera, A., Santiago-Algarra, D., Puthier, D., & Spicuglia, S. (2018) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2018.03.004 · Cited by 78
Metabolic Reprogramming Induces Germinal Center B Cell Differentiation through Bcl6 Locus Remodeling
Haniuda, K., Fukao, S., & Kitamura, D. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108333 · Cited by 79
The histone chaperone Spt6 coordinates histone H3K27 demethylation and myogenesis
Wang, A. H., Zare, H., Mousavi, K., Wang, C., Moravec, C. E., Sirotkin, H. I., Ge, K., Gutierrez-Cruz, G., & Sartorelli, V. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.54 · Cited by 77
Acemel, R. D., Maeso, I., & Gómez-Skármeta, J. L. (2017) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.265 · Cited by 82
Mammalian Transcription Factor Networks: Recent Advances in Interrogating Biological Complexity
Wilkinson, A. C., Nakauchi, H., & Göttgens, B. (2017) · Cell Systems · doi:10.1016/j.cels.2017.07.004 · Cited by 76
Lu, Y., Sun, Y., Drummer, C., Nanayakkara, G., Shao, Y., Saaoud, F., Johnson, C., Zhang, R., Yu, D., Li, X., et al. (2019) · Redox Biology · doi:10.1016/j.redox.2019.101221 · Cited by 77
Metadata
- Authors
- Rada-Iglesias, A., Bajpai, R., Swigut, T., Brugmann, S. A., Flynn, R. A., & Wysocka, J.
- Affiliations
- Stanford Medicine (US)
- Corresponding author
- Wysocka, Joanna
- Venue
- Nature
- Published
- 2010-12-15
- Volume
- 470
- Issue
- 7333
- Pages
- 279-283
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4445674
- OpenAlex
- W2154746182
- Cited by
- 2,233
- References
- 39
- Citations by year
- 2026: 70 · 2025: 108 · 2024: 118 · 2023: 134 · 2022: 117 · 2021: 154 · 2020: 162 · 2019: 144 · 2018: 151 · 2017: 158 · 2016: 154 · 2015: 181 · 2014: 190 · 2013: 185 · 2012: 140
- FWCI
- 50.78
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institute of Dental and Craniofacial Research (K99DE019853)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Keywords
- enhancers, poised enhancers, human embryonic stem cells, chromatin signatures, H3K4me1, H3K27ac, H3K27me3, P300, SMARCA4, nucleosome density, epiblast, neuroectoderm differentiation, gastrulation, mesoderm formation, neurulation
- MeSH terms
- Acetylation, Animals, Cell Differentiation, Cell Line, Chromatin, DNA Helicases, Enhancer Elements, Genetic, Germ Layers, Histones, Humans, Lysine, Mesoderm, Methylation, Nuclear Proteins, RNA, Transcription Factors, Zebrafish, Gene Expression Regulation, Developmental, Epigenesis, Genetic, Embryonic Development, Chromatin Immunoprecipitation, p300-CBP Transcription Factors, Embryonic Stem Cells, Neural Plate, Neurulation, Gastrulation
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