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Histone modifications at human enhancers reflect global cell-type-specific gene expression
Open accessAbstract
The human body is composed of diverse cell types with distinct functions. Although it is known that lineage specification depends on cell-specific gene expression, which in turn is driven by promoters, enhancers, insulators and other cis-regulatory DNA sequences for each gene, the relative roles of these regulatory elements in this process are not clear. We have previously developed a chromatin-immunoprecipitation-based microarray method (ChIP-chip) to locate promoters, enhancers and insulators in the human genome. Here we use the same approach to identify these elements in multiple cell types and investigate their roles in cell-type-specific gene expression. We observed that the chromatin state at promoters and CTCF-binding at insulators is largely invariant across diverse cell types. In contrast, enhancers are marked with highly cell-type-specific histone modification patterns, strongly correlate to cell-type-specific gene expression programs on a global scale, and are functionally active in a cell-type-specific manner. Our results define over 55,000 potential transcriptional enhancers in the human genome, significantly expanding the current catalogue of human enhancers and highlighting the role of these elements in cell-type-specific gene expression.
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“ChIPseq using antibodies to H3K4Me3, a mark associated with active promoter sites (Ernst et al., 2011), and to H3K27Ac, a mark associated with enhancer elements (Heintzman et al., 2009), demonstrated mapped read peaks corresponding to at least four major transcriptional start sites within the SYNE1 locus (P1–P4), one of which (P3) lies immediately upstream of the p.L3206M mutation (Figure 3E).”
From Using Whole-Exome Sequencing to Identify Inherited Causes of Autism (2013) · cites this paper as Heintzman et al., 2009
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High-Resolution Profiling of Histone Methylations in the Human Genome
Barski, A., Cuddapah, S., Cui, K., Roh, T.-Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I., & Zhao, K. (2007) · Cell · doi:10.1016/j.cell.2007.05.009 · Cited by 6,845
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 · cited 7×
“Using previously described chromatin signatures for enhancers 5 , we predicted 36,589 enhancers in the HeLa genome (Fig.”
MethodInfluentialSelf-citationGenome-Wide Mapping of in Vivo Protein-DNA Interactions
Johnson, D. S., Mortazavi, A., Myers, R. M., & Wold, B. (2007) · Science · doi:10.1126/science.1141319 · Cited by 2,927
The ENCODE (ENCyclopedia Of DNA Elements) Project
(2004) · Science · doi:10.1126/science.1105136 · Cited by 2,390
Xie, X., Lu, J., Kulbokas, E. J., Golub, T. R., Mootha, V., Lindblad-Toh, K., Lander, E. S., & Kellis, M. (2005) · Nature · doi:10.1038/nature03441 · Cited by 1,872
Self-citationRobertson, G., Hirst, M., Bainbridge, M., Bilenky, M., Zhao, Y., Zeng, T., Euskirchen, G., Bernier, B., Varhol, R., Delaney, A., et al. (2007) · Nature Methods · doi:10.1038/nmeth1068 · Cited by 1,454
Genome-wide analysis of estrogen receptor binding sites
Carroll, J. S., Meyer, C. A., Song, J. S., Li, W., Geistlinger, T., Eeckhoute, J., Brodsky, A. S., Keeton, E. K., Fertuck, K. C., Hall, G., et al. (2006) · Nature Genetics · doi:10.1038/ng1901 · Cited by 1,397
Cohesin mediates transcriptional insulation by CCCTC-binding factor
Wendt, K. S., Yoshida, K., Itoh, T., Bando, M., Koch, B., Schirghuber, E., Tsutsumi, S., Nagae, G., Ishihara, K., Mishiro, T., et al. (2008) · Nature · doi:10.1038/nature06634 · Cited by 1,193
A Global Map of p53 Transcription-Factor Binding Sites in the Human Genome
Wei, C.-L., Wu, Q., Vega, V. B., Chiu, K. P., Ng, P., Zhang, T., Shahab, A., Yong, H. C., Fu, Y., Weng, Z., et al. (2006) · Cell · doi:10.1016/j.cell.2005.10.043 · Cited by 1,141
Analysis of the Vertebrate Insulator Protein CTCF-Binding Sites in the Human Genome
Kim, T. H., Abdullaev, Z., Smith, A. D., Ching, K. A., Loukinov, D. I., Green, R. D., Zhang, M. Q., Lobanenkov, V. V., & Ren, B. (2007) · Cell · doi:10.1016/j.cell.2006.12.048 · Cited by 1,022
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Bhatt, D. M., & Ghosh, S. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00071 · Cited by 281
Endocrine disrupting chemicals and the developmental programming of adipogenesis and obesity
Janesick, A., & Blumberg, B. (2011) · Birth Defects Research Part C Embryo Today Reviews · doi:10.1002/bdrc.20197 · Cited by 276
Intragenic Enhancers Act as Alternative Promoters
Kowalczyk, M. S., Hughes, J. R., Garrick, D., Lynch, M. D., Sharpe, J. A., Sloane-Stanley, J. A., McGowan, S. J., De Gobbi, M., Hosseini, M., Vernimmen, D., et al. (2012) · Molecular Cell · doi:10.1016/j.molcel.2011.12.021 · Cited by 267
Epigenetic Regulation of Pluripotency and Differentiation
Boland, M. J., Nazor, K. L., & Loring, J. F. (2014) · Circulation Research · doi:10.1161/circresaha.115.301517 · Cited by 284
Histone H3K27 acetylation is dispensable for enhancer activity in mouse embryonic stem cells
Zhang, T., Zhang, Z., Dong, Q., Xiong, J., & Zhu, B. (2020) · Genome Biology · doi:10.1186/s13059-020-01957-w · Cited by 266
Coordinated changes in AHRR methylation in lymphoblasts and pulmonary macrophages from smokers
Monick, M. M., Beach, S. R. H., Plume, J., Sears, R., Gerrard, M., Brody, G. H., & Philibert, R. A. (2012) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32021 · Cited by 264
Lineage-specific enhancers activate self-renewal genes in macrophages and embryonic stem cells
Soucie, E. L., Weng, Z., Geirsdóttir, L., Molawi, K., Maurizio, J., Fenouil, R., Mossadegh-Keller, N., Gimenez, G., VanHille, L., Beniazza, M., et al. (2016) · Science · doi:10.1126/science.aad5510 · Cited by 263
Wang, A., Yue, F., Li, Y., Xie, R., Harper, T. C., Patel, N. A., Muth, K., Palmer, J., Qiu, Y., Wang, J., et al. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.02.013 · Cited by 274
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Cabău, G., Crișan, T. O., Klück, V., Popp, R. A., & Joosten, L. A. B. (2019) · Immunological Reviews · doi:10.1111/imr.12833 · Cited by 267
The androgen receptor is a tumor suppressor in estrogen receptor–positive breast cancer
Hickey, T. E., Selth, L. A., Chia, K. M., Laven‐Law, G., Milioli, H. H., Roden, D. L., Jindal, S., Hui, M. N., Finlay-Schultz, J., Ebrahimie, E., et al. (2021) · Nature Medicine · doi:10.1038/s41591-020-01168-7 · Cited by 261
Kerenyi, M. A., Shao, Z., Hsu, Y., Guo, G., Luc, S., O’Brien, K., Fujiwara, Y., Peng, C., Nguyen, M., & Orkin, S. H. (2013) · eLife · doi:10.7554/elife.00633 · Cited by 267
Global view of enhancer–promoter interactome in human cells
He, B., Chen, C., Teng, L., & Tan, K. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1320308111 · Cited by 263
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Wang, X., Fang, Y., Liang, W., Wong, C. C., Qin, H., Gao, Y., Liang, M., Song, L., Zhang, Y., Fan, M., et al. (2024) · Cancer Cell · doi:10.1016/j.ccell.2024.08.019 · Cited by 262
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Chepelev, I., Wei, G., Wangsa, D., Tang, Q., & Zhao, K. (2012) · Cell Research · doi:10.1038/cr.2012.15 · Cited by 253
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Schnetz, M. P., Handoko, L., Akhtar‐Zaidi, B., Bartels, C. F., Pereira, C., Fisher, A. G., Adams, D. J., Flicek, P., Crawford, G. E., LaFramboise, T., et al. (2010) · PLoS Genetics · doi:10.1371/journal.pgen.1001023 · Cited by 260
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Kurotaki, D., Osato, N., Nishiyama, A., Yamamoto, M., Ban, T., Sato, H., Nakabayashi, J., Umehara, M., Miyake, N., Matsumoto, N., et al. (2013) · Blood · doi:10.1182/blood-2012-06-437863 · Cited by 252
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Bennett, R. L., & Licht, J. D. (2017) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010716-105106 · Cited by 254
A Role for Noncoding Variation in Schizophrenia
Roussos, P., Mitchell, A. C., Voloudakis, G., Fullard, J. F., Pothula, V. M., Tsang, J., Stahl, E. A., Georgakopoulos, A., Ruderfer, D. M., Charney, A., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.10.015 · Cited by 251
Boyle, P., Clement, K., Gu, H., Smith, Z. D., Ziller, M. J., Fostel, J., Holmes, L., Meldrim, J., Kelley, F., Gnirke, A., et al. (2012) · Genome biology · doi:10.1186/gb-2012-13-10-r92 · Cited by 257
Mimura, I., Nangaku, M., Kanki, Y., Tsutsumi, S., Inoue, T., Kohro, T., Yamamoto, S., Fujita, T., Shimamura, T., Suehiro, J.-I., et al. (2012) · Molecular and Cellular Biology · doi:10.1128/mcb.06643-11 · Cited by 251
Lindholm, M. E., Marabita, F., Gómez-Cabrero, D., Rundqvist, H., Ekström, T. J., Tegner, J. N., & Sundberg, C. J. (2014) · Epigenetics · doi:10.4161/15592294.2014.982445 · Cited by 261
The Dynamic Epigenetic Landscape of the Retina During Development, Reprogramming, and Tumorigenesis
Aldiri, I., Xu, B., Wang, L., Chen, X. '., Hiler, D. J., Griffiths, L. M., Valentine, M. B., Shirinifard, A., Thiagarajan, S., Sablauer, A., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.022 · Cited by 252
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Yu, B., Zhang, K., Milner, J. J., Toma, C., Chen, R., Scott-Browne, J. P., Pereira, R. M., Crotty, S., Chang, J. T., Pipkin, M. E., et al. (2017) · Nature Immunology · doi:10.1038/ni.3706 · Cited by 248
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Li, K., Liu, Y., Cao, H., Zhang, Y., Gu, Z., Liu, X., Yu, A., Kaphle, P., Dickerson, K. E., Ni, M., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-14362-5 · Cited by 257
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DNA methylation status predicts cell type‐specific enhancer activity
Wiench, M., John, S., Baek, S., Johnson, T. A., Sung, M., Escobar, T., Simmons, C. A., Pearce, K. H., Biddie, S. C., Sabo, P. J., et al. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.210 · Cited by 245
Xie, J.-J., Jiang, Y.-Y., Jiang, Y. Y., Li, C., Lim, M. C., An, Ö., Mayakonda, A., Ding, L., Long, L., Sun, C., et al. (2018) · Gastroenterology · doi:10.1053/j.gastro.2018.02.018 · Cited by 247
RetractedDiscriminative prediction of mammalian enhancers from DNA sequencePreprint
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Fischer, J., Paret, C., Malki, K. E., Alt, F., Wingerter, A., Neu, M. A., Kron, B., Russo, A., Lehmann, N., Roth, L., et al. (2017) · Journal of Immunotherapy · doi:10.1097/cji.0000000000000169 · Cited by 255
Predicting cell-type–specific gene expression from regions of open chromatinPreprint
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Enhancer priming by H3K4 methyltransferase MLL4 controls cell fate transition
Wang, C., Lee, J.-E., Lai, B., Macfarlan, T. S., Xu, S., Zhuang, L., Liu, C., Peng, W., & Ge, K. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1606857113 · Cited by 242
Wang, S., Tang, Z., Chen, C.-W. D., Shimada, M., Koche, R. P., Wang, L.-H., Nakadai, T., Chramiec, A. G., Krivtsov, A. V., Armstrong, S. A., et al. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.06.028 · Cited by 249
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Finding distal regulatory elements in the human genome
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Local, A., Huang, H., de Albuquerque, C. P., Singh, N., Lee, A. Y., Wang, W., Wang, C., Hsia, J. E., Shiau, A. K., Ge, K., et al. (2017) · Nature Genetics · doi:10.1038/s41588-017-0015-6 · Cited by 245
Self-citationRevilla‐i‐Domingo, R., Bilić, I., Vilagos, B., Tagoh, H., Ebert, A., Tamir, I., Smeenk, L., Trupke, J., Sommer, A., Jaritz, M., et al. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.155 · Cited by 246
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Euskirchen, G. M., Auerbach, R. K., Davidov, E., Gianoulis, T. A., Zhong, G., Rozowsky, J. S., Bhardwaj, N., Gerstein, M., & Snyder, M. P. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002008 · Cited by 233
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Scruggs, B. S., Gilchrist, D. A., Nechaev, S., Muse, G. W., Burkholder, A., Fargo, D. C., & Adelman, K. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.04.006 · Cited by 232
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Li, X.-Y., Thomas, S., Sabo, P. J., Eisen, M. B., Stamatoyannopoulos, J. A., & Biggin, M. D. (2011) · Genome Biology · doi:10.1186/gb-2011-12-4-r34 · Cited by 217
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Sequence and chromatin determinants of cell-type–specific transcription factor bindingPreprint
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van Nuland, R., Smits, A. H., Pallaki, P., Jansen, P. W. T. C., Vermeulen, M., & Timmers, H. T. M. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.01742-12 · Cited by 223
Solouki, A. M., Verhoeven, V. J. M., van Duijn, C. M., Verkerk, A. J. M. H., Ikram, M. K., Hysi, P. G., Despriet, D. D. G., van Koolwijk, L. M. E., Ho, L., Ramdas, W. D., et al. (2010) · Nature Genetics · doi:10.1038/ng.663 · Cited by 215
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Levo, M., & Segal, E. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3684 · Cited by 215
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Hu, X., Huang, X., Yang, Y., Sun, Y., Zhao, Y., Zhang, Z., Qiu, D., Wu, Y., Wu, G., & Lei, L. (2024) · Nucleic Acids Research · doi:10.1093/nar/gkae183 · Cited by 213
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Andersson, R., Sandelin, A., & Danko, C. G. (2015) · Trends in Genetics · doi:10.1016/j.tig.2015.05.007 · Cited by 225
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Smale, S. T., Tarakhovsky, A., & Natoli, G. (2014) · Annual Review of Immunology · doi:10.1146/annurev-immunol-031210-101303 · Cited by 213
Barozzi, I., Simonatto, M., Bonifacio, S., Yang, L., Rohs, R., Ghisletti, S., & Natoli, G. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.04.006 · Cited by 209
Establishment of regions of genomic activity during the Drosophila maternal to zygotic transition
Li, X., Harrison, M. M., Villalta, J. E., Kaplan, T., & Eisen, M. B. (2014) · eLife · doi:10.7554/elife.03737 · Cited by 218
Lefterova, M. I., Steger, D. J., Zhuo, D. X., Qatanani, M., Mullican, S. E., Tuteja, G., Manduchi, E., Grant, G. R., & Lazar, M. A. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.01651-09 · Cited by 213
Evolution of transcription factor binding in metazoans — mechanisms and functional implications
Villar, D., Flicek, P., & Odom, D. T. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3481 · Cited by 217
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Comai, G., & Tajbakhsh, S. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-405943-6.00001-4 · Cited by 213
Catarino, R. R., & Stark, A. (2018) · Genes & Development · doi:10.1101/gad.310367.117 · Cited by 215
Self-citationVerzi, M. P., Shin, H., He, H. H., Sulahian, R., Meyer, C. A., Montgomery, R. K., Fleet, J. C., Brown, M. A., Liu, X. S., & Shivdasani, R. A. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.10.006 · Cited by 211
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Martynoga, B., Mateo, J. L., Zhou, B., Andersen, J., Achimastou, A., Urbán, N., van den Berg, D. L. C., Georgopoulou, D., Hadjur, S., Wittbrodt, J., et al. (2013) · Genes & Development · doi:10.1101/gad.216804.113 · Cited by 215
Zhao, B., Zou, J., Wang, H., Johannsen, E., Peng, C.-W., Quackenbush, J. F., Mar, J. C., Morton, C. C., Freedman, M. L., Blacklow, S. C., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1108892108 · Cited by 205
Transcription-associated histone modifications and cryptic transcription
Smolle, M., & Workman, J. L. (2012) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2012.08.008 · Cited by 215
Disrupted Intricacy of Histone H3K4 Methylation in Neurodevelopmental Disorders
Vallianatos, C. N., & Iwase, S. (2015) · Epigenomics · doi:10.2217/epi.15.1 · Cited by 204
Lee, J., Park, Y.-K., Park, S., Jang, Y., Waring, N. A., Dey, A., Ozato, K., Lai, B., Peng, W., & Ge, K. (2017) · Nature Communications · doi:10.1038/s41467-017-02403-5 · Cited by 209
Du, L., Lin, L., Li, Q., Liu, K., Huang, Y., Wang, X., Cao, K., Chen, X., Cao, W., Li, F., et al. (2019) · Cell Metabolism · doi:10.1016/j.cmet.2019.01.006 · Cited by 203
Maintaining Cell Identity through Global Control of Genomic Organization
Natoli, G. (2010) · Immunity · doi:10.1016/j.immuni.2010.07.006 · Cited by 208
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Ma, Z., Swigut, T., Valouev, A., Rada-Iglesias, Á., & Wysocka, J. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2000 · Cited by 203
Mechanisms of specificity in neuronal activity-regulated gene transcription
Lyons, M. R., & West, A. E. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.05.003 · Cited by 209
Epigenetic mechanisms in diabetic vascular complications
Reddy, M. A., & Natarajan, R. D. (2011) · Cardiovascular Research · doi:10.1093/cvr/cvr024 · Cited by 202
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Yan, J., Chen, S.-A. A., Local, A., Liu, T., Qiu, Y., Lee, A. Y., Jung, I., Preißl, S., Rivera, C. M., Wang, C., et al. (2018) · Cell Research · doi:10.1038/cr.2018.1 · Cited by 198
Self-citationSpatially resolved epigenomic profiling of single cells in complex tissues
Lu, T., Ang, C. E., & Zhuang, X. (2022) · Cell · doi:10.1016/j.cell.2022.09.035 · Cited by 197
Xu, J., Shao, Z., Glass, K., Bauer, D. E., Pinello, L., Handel, B. V., Hou, S., Stamatoyannopoulos, J. A., Mikkola, H. K. A., Yuan, G., et al. (2012) · Developmental Cell · doi:10.1016/j.devcel.2012.09.003 · Cited by 207
Lodato, M. A., Ng, C., Wamstad, J. A., Cheng, A. W., Thai, K. K., Fraenkel, E., Jaenisch, R., & Boyer, L. A. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003288 · Cited by 201
Interferon stimulation creates chromatin marks and establishes transcriptional memory
Kamada, R., Yang, W., Zhang, Y., Patel, M. C., Yang, Y., Ouda, R., Dey, A., Wakabayashi, Y., Sakaguchi, K., Fujita, T., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1720930115 · Cited by 206
Histone H3 lysine K4 methylation and its role in learning and memory
Collins, B. E., Greer, C. B., Coleman, B. C., & Sweatt, J. D. (2019) · Epigenetics & Chromatin · doi:10.1186/s13072-018-0251-8 · Cited by 209
ZNF143 provides sequence specificity to secure chromatin interactions at gene promoters
Bailey, S. D., Zhang, X., Desai, K., Aid, M., Corradin, O., Cowper-Sal·lari, R., Akhtar-Zaidi, B., Scacheri, P. C., Haibe-Kains, B., & Lupien, M. (2015) · Nature Communications · doi:10.1038/ncomms7186 · Cited by 194
Self-citationStitzel, M. L., Sethupathy, P., Pearson, D. S., Chines, P. S., Song, L., Erdos, M. R., Welch, R., Parker, S. C. J., Boyle, A. P., Scott, L. J., et al. (2010) · Cell Metabolism · doi:10.1016/j.cmet.2010.09.012 · Cited by 193
Self-citation
Metadata
- Authors
- 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., Ching, K. A., Antosiewicz-Bourget, J. E., Liu, H., Zhang, X., Green, R. D., Lobanenkov, V. V., Stewart, R., Thomson, J. A., Crawford, G. E., Kellis, M., & Ren, B.
- Affiliations
- Ludwig Cancer Research (BE)
- MIT Computer Science and Artificial Intelligence Laboratory (US)
- Broad Institute (US)
- National Institute of Allergy and Infectious Diseases (US)
- Morgridge Institute for Research (US)
- University of Wisconsin–Madison (US)
- Duke University (US)
- Corresponding author
- Ren, Bing
- ORCID
- Venue
- Nature
- Published
- 2009-03-18
- Volume
- 459
- Issue
- 7243
- Pages
- 108-112
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC2910248
- OpenAlex
- W2123564569
- Cited by
- 2,533
- References
- 27
- Citations by year
- 2026: 56 · 2025: 101 · 2024: 115 · 2023: 122 · 2022: 101 · 2021: 126 · 2020: 171 · 2019: 150 · 2018: 163 · 2017: 154 · 2016: 164 · 2015: 183 · 2014: 193 · 2013: 204 · 2012: 188
- FWCI
- 71.06
- 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)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-sa)
- PubMed Central
- Funders
- National Institutes of Health
- National Human Genome Research Institute (U01HG003151, R01HG004037)
- 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 › Chromatin Remodeling and Cancer
- Keywords
- histone modifications, enhancers, cell type-specific gene expression, promoter, insulators, CTCF binding, chromatin state, cis-regulatory elements, human cell lines, ChIP-chip
- MeSH terms
- Binding Sites, Cell Line, Cell Physiological Phenomena, Chromatin, Gene Expression Regulation, HeLa Cells, Histones, Humans, Promoter Regions, Genetic, Transcription Factors, Genome, Human, K562 Cells
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