The DOI matches its Crossref record; 214 of the 218 references it cites were found in a registry or an index.
Long-range enhancer–promoter contacts in gene expression control
Abstract
Spatiotemporal gene expression programmes are orchestrated by transcriptional enhancers, which are key regulatory DNA elements that engage in physical contacts with their target-gene promoters, often bridging considerable genomic distances. Recent progress in genomics, genome editing and microscopy methodologies have enabled the genome-wide mapping of enhancer-promoter contacts and their functional dissection. In this Review, we discuss novel concepts on how enhancer-promoter interactions are established and maintained, how the 3D architecture of mammalian genomes both facilitates and constrains enhancer-promoter contacts, and the role they play in gene expression control during normal development and disease.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“It is clear from both genome-wide profiling and perturbation studies that, of the multitudes of enhancers in a locus, not all of them provide input to every promoter [430, 431].”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [431]
In the citing paper
“Promoter-interacting regions identified using these approaches typically show enrichment for enhancer-associated chromatin marks and disease-associated variants, and in a number of cases their target genes have been validated directly (reviewed in [431]).”
From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [431]
In the citing paper
“During the “search” of a target promoter (regardless of the “searching mechanism”), enhancers meet other genes that, however, are not activated by this enhancer [21,128,129].”
From Enhancer Function in the 3D Genome (2023) · cites this paper as [128]
In the citing paper
“Chromatin loops enable interactions between enhancers and promoters enabling fine control of gene expression, in addition to the regulation mediated by transcription factors and other epigenetic modifications”
From Neuronal DNA double-strand breaks lead to genome structural variations and 3D genome disruption in neurodegeneration (2023) · cites this paper as [27]
Citations
Cites
An integrated encyclopedia of DNA elements in the human genome
The ENCODE Project Consortium (2012) · Nature · doi:10.1038/nature11247 · Cited by 18,072
A 3D Map of the Human Genome at Kilobase Resolution Reveals Principles of Chromatin Looping
Rao, S. S. P., Huntley, M. H., Durand, N. C., Stamenova, E. K., Bochkov, I. D., Robinson, J. T., Sanborn, A. L., Machol, I., Omer, A. D., Lander, E. S., et al. (2014) · Cell · doi:10.1016/j.cell.2014.11.021 · Cited by 9,212
Comprehensive Mapping of Long-Range Interactions Reveals Folding Principles of the Human Genome
Lieberman-Aiden, E., van Berkum, N. L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A., Amit, I., Lajoie, B. R., Sabo, P. J., Dorschner, M. O., et al. (2009) · Science · doi:10.1126/science.1181369 · Cited by 8,898
Topological domains in mammalian genomes identified by analysis of chromatin interactions
Dixon, J. R., Selvaraj, S., Yue, F., Kim, A., Li, Y., Shen, Y., Hu, M., Liu, J. S., & Ren, B. (2012) · Nature · doi:10.1038/nature11082 · Cited by 6,829
Histone H3K27ac separates active from poised enhancers and predicts developmental state
Creyghton, M. P., Cheng, A. W., Welstead, G. G., Kooistra, T., Carey, B. W., Steine, E. J., Hanna, J., Lodato, M. A., Frampton, G. M., Sharp, P. A., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1016071107 · Cited by 4,302
Systematic Localization of Common Disease-Associated Variation in Regulatory DNA
Maurano, M. T., Humbert, R., Rynes, E., Thurman, R. E., Haugen, E., Wang, H., Reynolds, A. P., Sandstrom, R., Qu, H., Brody, J., et al. (2012) · Science · doi:10.1126/science.1222794 · Cited by 3,716
Capturing Chromosome Conformation
Dekker, J., Rippe, K., Dekker, M., & Kleckner, N. (2002) · Science · doi:10.1126/science.1067799 · Cited by 3,652
Spatial partitioning of the regulatory landscape of the X-inactivation centre
Nora, E. P., Lajoie, B. R., Schulz, E. G., Giorgetti, L., Okamoto, I., Servant, N., Piolot, T., van Berkum, N. L., Meisig, J., Sedat, J., et al. (2012) · Nature · doi:10.1038/nature11049 · Cited by 2,895
Coactivator condensation at super-enhancers links phase separation and gene control
Sabari, B. R., Dall’Agnese, A., Boija, A., Klein, I. A., Coffey, E. L., Shrinivas, K., Abraham, B. J., Hannett, N. M., Zamudio, A. V., Manteiga, J. C., et al. (2018) · Science · doi:10.1126/science.aar3958 · Cited by 2,595
A unique chromatin signature uncovers early developmental enhancers in humans
Rada-Iglesias, A., Bajpai, R., Swigut, T., Brugmann, S. A., Flynn, R. A., & Wysocka, J. (2011) · Nature · doi:10.1038/nature09692 · Cited by 2,233
Disruptions of Topological Chromatin Domains Cause Pathogenic Rewiring of Gene-Enhancer Interactions
Lupiáñez, D. G., Kraft, K., Heinrich, V., Krawitz, P., Brancati, F., Klopocki, E., Horn, D., Kayserili, H., Opitz, J. M., Laxova, R., et al. (2015) · Cell · doi:10.1016/j.cell.2015.04.004 · Cited by 2,132
Formation of chromosomal domains by loop extrusion
Fudenberg, G., Imakaev, M., Lu, C., Goloborodko, A., Abdennur, N., & Mirny, L. A. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.085 · Cited by 2,003
Three-dimensional folding and functional organization principles of the Drosophila genome
Sexton, T., Yaffe, E., Kenigsberg, E., Bantignies, F., Leblanc, B., Hoichman, M., Parrinello, H., Tanay, A., & Cavalli, G. (2012) · Cell · doi:10.1016/j.cell.2012.01.010 · Cited by 1,983
Mediator and cohesin connect gene expression and chromatin architecture
Kagey, M. H., Newman, J. J., Bilodeau, S., Zhan, Y., Orlando, D. A., van Berkum, N. L., Ebmeier, C. C., Goossens, J., Rahl, P. B., Levine, S. S., et al. (2010) · Nature · doi:10.1038/nature09380 · Cited by 1,939
Hilton, I. B., D’Ippolito, A. M., Vockley, C. M., Thakore, P. I., Crawford, G. E., Reddy, T. E., & Gersbach, C. A. (2015) · Nature Biotechnology · doi:10.1038/nbt.3199 · Cited by 1,931
Cohesin Loss Eliminates All Loop Domains
Rao, S. S. P., Huang, S.-C., Glenn St Hilaire, B., Engreitz, J. M., Perez, E. M., Kieffer-Kwon, K.-R., Sanborn, A. L., Johnstone, S. E., Bascom, G. D., Bochkov, I. D., et al. (2017) · Cell · doi:10.1016/j.cell.2017.09.026 · Cited by 1,883
Boija, A., Klein, I. A., Sabari, B. R., Dall’Agnese, A., Coffey, E. L., Zamudio, A. V., Li, C. H., Shrinivas, K., Manteiga, J. C., Hannett, N. M., et al. (2018) · Cell · doi:10.1016/j.cell.2018.10.042 · Cited by 1,815
A Phase Separation Model for Transcriptional Control
Hnisz, D., Shrinivas, K., Young, R. A., Chakraborty, A. K., & Sharp, P. A. (2017) · Cell · doi:10.1016/j.cell.2017.02.007 · Cited by 1,753
An oestrogen-receptor-α-bound human chromatin interactome
Fullwood, M. J., Liu, M. H., Pan, Y. F., Liu, J., Han, X., Mohamed, Y. B., Orlov, Y. L., Velkov, S., Ho, A., Poh, H. M., et al. (2009) · Nature · doi:10.1038/nature08497 · Cited by 1,752
Stochastic mRNA Synthesis in Mammalian Cells
Raj, A., Peskin, C. S., Tranchina, D., Vargas, D. Y., & Tyagi, S. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040309 · Cited by 1,737
Sanborn, A. L., Rao, S. S. P., Huang, S.-C., Durand, N. C., Huntley, M. H., Jewett, A. I., Bochkov, I. D., Chinnappan, D., Cutkosky, A., Li, J., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1518552112 · Cited by 1,730
Nora, E. P., Goloborodko, A., Valton, A.-L., Gibcus, J. H., Uebersohn, A., Abdennur, N., Dekker, J., Mirny, L. A., & Bruneau, B. G. (2017) · Cell · doi:10.1016/j.cell.2017.05.004 · Cited by 1,709
Chromatin architecture reorganization during stem cell differentiation
Dixon, J. R., Jung, I., Selvaraj, S., Shen, Y., Antosiewicz-Bourget, J. E., Lee, A. Y., Ye, Z., Kim, A., Rajagopal, N., Xie, W., et al. (2015) · Nature · doi:10.1038/nature14222 · Cited by 1,646
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
Single-cell Hi-C reveals cell-to-cell variability in chromosome structure
Nagano, T., Lubling, Y., Stevens, T. J., Schoenfelder, S., Yaffe, E., Dean, W., Laue, E. D., Tanay, A., & Fraser, P. (2013) · Nature · doi:10.1038/nature12593 · Cited by 1,589
Self-citationThe 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
Mediator and RNA polymerase II clusters associate in transcription-dependent condensates
Cho, W.-K., Spille, J.-H., Hecht, M., Lee, C., Li, C., Grube, V., & Cisse, I. I. (2018) · Science · doi:10.1126/science.aar4199 · Cited by 1,403
Simonis, M., Klous, P., Splinter, E., Moshkin, Y., Willemsen, R., de Wit, E., van Steensel, B., & de Laat, W. (2006) · Nature Genetics · doi:10.1038/ng1896 · Cited by 1,386
A map of the cis-regulatory sequences in the mouse genome
Shen, Y., Yue, F., McCleary, D. F., Ye, Z., Edsall, L., Kuan, S., Wagner, U., Dixon, J., Lee, L., Lobanenkov, V. V., et al. (2012) · Nature · doi:10.1038/nature11243 · Cited by 1,361
Multiscale 3D Genome Rewiring during Mouse Neural Development
Bonev, B., Mendelson Cohen, N., Szabo, Q., Fritsch, L., Papadopoulos, G. L., Lubling, Y., Xu, X., Lv, X., Hugnot, J.-P., Tanay, A., et al. (2017) · Cell · doi:10.1016/j.cell.2017.09.043 · Cited by 1,338
Hi–C: A comprehensive technique to capture the conformation of genomes
Belton, J.-M., McCord, R. P., Gibcus, J. H., Naumova, N., Zhan, Y., & Dekker, J. (2012) · Methods · doi:10.1016/j.ymeth.2012.05.001 · Cited by 1,301
Insulator dysfunction and oncogene activation in IDH mutant gliomas
Flavahan, W. A., Drier, Y., Liau, B. B., Gillespie, S. M., Venteicher, A. S., Stemmer-Rachamimov, A. O., Suvà, M. L., & Bernstein, B. E. (2016) · Nature · doi:10.1038/nature16490 · Cited by 1,288
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
Editing DNA Methylation in the Mammalian Genome
Liu, X. S., Wu, H., Ji, X., Stelzer, Y., Wu, X., Czauderna, S., Shu, J., Dadon, D., Young, R. A., & Jaenisch, R. (2016) · Cell · doi:10.1016/j.cell.2016.08.056 · Cited by 1,224
Obesity-associated variants within FTO form long-range functional connections with IRX3
Smemo, S., Tena, J. J., Kim, K.-H., Gamazon, E. R., Sakabe, N. J., Gómez-Marín, C., Aneas, I., Credidio, F. L., Sobreira, D. R., Wasserman, N. F., et al. (2014) · Nature · doi:10.1038/nature13138 · Cited by 1,219
A high-resolution map of the three-dimensional chromatin interactome in human cells
Jin, F., Li, Y., Dixon, J. R., Selvaraj, S., Ye, Z., Lee, A. Y., Yen, C.-A., Schmitt, A. D., Espinoza, C. A., & Ren, B. (2013) · Nature · doi:10.1038/nature12644 · Cited by 1,208
Two independent modes of chromatin organization revealed by cohesin removal
Schwarzer, W., Abdennur, N., Goloborodko, A., Pekowska, A., Fudenberg, G., Loe-Mie, Y., Fonseca, N. A., Huber, W., Haering, C. H., Mirny, L., et al. (2017) · Nature · doi:10.1038/nature24281 · Cited by 1,196
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
Architectural 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
Organization and function of the 3D genome
Bonev, B., & Cavalli, G. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.112 · Cited by 1,174
Organizational principles of 3D genome architecture
Rowley, M. J., & Corces, V. G. (2018) · Nature Reviews Genetics · doi:10.1038/s41576-018-0060-8 · Cited by 1,171
Lettice, L. A. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg180 · Cited by 1,164
HiChIP: efficient and sensitive analysis of protein-directed genome architecture
Mumbach, M. R., Rubin, A. J., Flynn, R. A., Dai, C., Khavari, P. A., Greenleaf, W. J., & Chang, H. Y. (2016) · Nature Methods · doi:10.1038/nmeth.3999 · Cited by 1,139
Genome-Wide Quantitative Enhancer Activity Maps Identified by STARR-seq
Arnold, C. D., Gerlach, D., Stelzer, C., Boryń, Ł. M., Rath, M., & Stark, A. (2013) · Science · doi:10.1126/science.1232542 · Cited by 1,125
VISTA 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
Active genes dynamically colocalize to shared sites of ongoing transcription
Osborne, C. S., Chakalova, L., Brown, K. E., Carter, D., Horton, A., Debrand, E., Goyenechea, B., Mitchell, J. A., Lopes, S. M. C. D. S., Reik, W., et al. (2004) · Nature Genetics · doi:10.1038/ng1423 · Cited by 1,080
Self-citationJavierre, B. M., Burren, O. S., Wilder, S. P., Kreuzhuber, R., Hill, S. M., Sewitz, S., Cairns, J., Wingett, S. W., Várnai, C., Thiecke, M. J., et al. (2016) · Cell · doi:10.1016/j.cell.2016.09.037 · Cited by 1,046
Self-citationActivation of proto-oncogenes by disruption of chromosome neighborhoods
Hnisz, D., Weintraub, A. S., Day, D. S., Valton, A.-L., Bak, R. O., Li, C. H., Goldmann, J., Lajoie, B. R., Fan, Z. P., Sigova, A. A., et al. (2016) · Science · doi:10.1126/science.aad9024 · Cited by 1,042
Thakore, P. I., D'Ippolito, A. M., Song, L., Safi, A., Shivakumar, N. K., Kabadi, A. M., Reddy, T. E., Crawford, G. E., & Gersbach, C. A. (2015) · Nature Methods · doi:10.1038/nmeth.3630 · Cited by 1,012
The Xist lncRNA Exploits Three-Dimensional Genome Architecture to Spread Across the X Chromosome
Engreitz, J., Pandya‐Jones, A., McDonel, P. E., Shishkin, A., Sirokman, K., Surka, C., Kadri, S., Xing, J. C., Goren, A., Lander, E. S., et al. (2013) · Science · doi:10.1126/science.1237973 · Cited by 1,008
YY1 Is a Structural Regulator of Enhancer-Promoter Loops
Weintraub, A. S., Li, C. H., Zamudio, A. V., Sigova, A. A., Hannett, N. M., Day, D. S., Abraham, B. J., Cohen, M. A., Nabet, B., Buckley, D. L., et al. (2017) · Cell · doi:10.1016/j.cell.2017.11.008 · Cited by 992
Mapping long-range promoter contacts in human cells with high-resolution capture Hi-C
Mifsud, B., Tavares-Cadete, F., Young, A. N., Sugar, R., Schoenfelder, S., Ferreira, L., Wingett, S. W., Andrews, S., Grey, W., Ewels, P. A., et al. (2015) · Nature Genetics · doi:10.1038/ng.3286 · Cited by 990
Self-citationCTCF-Mediated Human 3D Genome Architecture Reveals Chromatin Topology for Transcription
Tang, Z., Luo, O. J., Li, X., Zheng, M., Zhu, J. J., Szalaj, P., Trzaskoma, P., Magalska, A., Wlodarczyk, J., Ruszczycki, B., et al. (2015) · Cell · doi:10.1016/j.cell.2015.11.024 · Cited by 982
Super-resolution chromatin tracing reveals domains and cooperative interactions in single cells
Bintu, B., Mateo, L. J., Su, J.-H., Sinnott-Armstrong, N. A., Parker, M., Kinrot, S., Yamaya, K., Boettiger, A. N., & Zhuang, X. (2018) · Science · doi:10.1126/science.aau1783 · Cited by 976
Imaging dynamic and selective low-complexity domain interactions that control gene transcription
Chong, S., Dugast-Darzacq, C., Liu, Z., Dong, P., Dailey, G. M., Cattoglio, C., Heckert, A., Banala, S., Lavis, L., Darzacq, X., et al. (2018) · Science · doi:10.1126/science.aar2555 · Cited by 966
CRISPR Inversion of CTCF Sites Alters Genome Topology and Enhancer/Promoter Function
Guo, Y., Xu, Q., Canzio, D., Shou, J., Li, J., Gorkin, D. U., Jung, I., Wu, H., Zhai, Y., Tang, Y., et al. (2015) · Cell · doi:10.1016/j.cell.2015.07.038 · Cited by 958
Zhao, Z., Tavoosidana, G., Sjölinder, M., Göndör, A., Mariano, P., Wang, S., Kanduri, C., Lezcano, M., Sandhu, K. S., Singh, U., et al. (2006) · Nature Genetics · doi:10.1038/ng1891 · Cited by 957
Ever-Changing Landscapes: Transcriptional Enhancers in Development and Evolution
Long, H. K., Prescott, S. L., & Wysocka, J. (2016) · Cell · doi:10.1016/j.cell.2016.09.018 · Cited by 945
Cohesins Functionally Associate with CTCF on Mammalian Chromosome Arms
Parelho, V., Hadjur, S., Spivakov, M., Leleu, M., Sauer, S., Gregson, H. C., Jarmuz, A., Canzonetta, C., Webster, Z., Nesterova, T., et al. (2008) · Cell · doi:10.1016/j.cell.2008.01.011 · Cited by 900
BCL11A enhancer dissection by Cas9-mediated in situ saturating mutagenesis
Canver, M. C., Smith, E. C., Sher, F., Pinello, L., Sanjana, N. E., Shalem, O., Chen, D. D., Schupp, P. G., Vinjamur, D. S., Garcia, S. P., et al. (2015) · Nature · doi:10.1038/nature15521 · Cited by 886
Control of cell identity genes occurs in insulated neighborhoods in mammalian chromosomes
Dowen, J. M., Fan, Z. P., Hnisz, D., Ren, G., Abraham, B. J., Zhang, L. N., Weintraub, A. S., Schuijers, J., Lee, T. I., Zhao, K., et al. (2014) · Cell · doi:10.1016/j.cell.2014.09.030 · Cited by 884
Super-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
Wutz, G., Várnai, C., Nagasaka, K., Cisneros, D. A., Stocsits, R. R., Tang, W., Schoenfelder, S., Jessberger, G., Muhar, M., Hossain, M. J., et al. (2017) · The EMBO Journal · doi:10.15252/embj.201798004 · Cited by 864
Self-citationActivating RNAs associate with Mediator to enhance chromatin architecture and transcription
Lai, F., Ørom, U. A., Cesaroni, M., Beringer, M., Taatjes, D. J., Blobel, G. A., & Shiekhattar, R. (2013) · Nature · doi:10.1038/nature11884 · Cited by 857
Nasmyth, K. (2001) · Annual Review of Genetics · doi:10.1146/annurev.genet.35.102401.091334 · Cited by 805
Cell-cycle dynamics of chromosomal organization at single-cell resolution
Nagano, T., Lubling, Y., Várnai, C., Dudley, C., Leung, W., Baran, Y., Mendelson Cohen, N., Wingett, S., Fraser, P., & Tanay, A. (2017) · Nature · doi:10.1038/nature23001 · Cited by 794
Self-citationThe cohesin release factor WAPL restricts chromatin loop extension
Haarhuis, J. H. I., van der Weide, R. H., Blomen, V. A., Yáñez-Cuna, J. O., Amendola, M., van Ruiten, M. S., Krijger, P. H. L., Teunissen, H., Medema, R. H., van Steensel, B., et al. (2017) · Cell · doi:10.1016/j.cell.2017.04.013 · Cited by 793
Schoenfelder, S., Sexton, T., Chakalova, L., Cope, N. F., Horton, A., Andrews, S., Kurukuti, S., Mitchell, J. A., Umlauf, D., Dimitrova, D. S., et al. (2009) · Nature Genetics · doi:10.1038/ng.496 · Cited by 735
Self-citationDeng, W., Lee, J., Wang, H., Miller, J., Reik, A., Gregory, P. D., Dean, A., & Blobel, G. A. (2012) · Cell · doi:10.1016/j.cell.2012.03.051 · Cited by 734
Genome Architecture: Domain Organization of Interphase Chromosomes
Bickmore, W. A., & van Steensel, B. (2013) · Cell · doi:10.1016/j.cell.2013.02.001 · Cited by 725
Enhancer Control of Transcriptional Bursting
Fukaya, T., Lim, B., & Levine, M. (2016) · Cell · doi:10.1016/j.cell.2016.05.025 · Cited by 721
Complex multi-enhancer contacts captured by genome architecture mapping
Beagrie, R. A., Scialdone, A., Schueler, M., Kraemer, D. C. A., Chotalia, M., Xie, S. Q., Barbieri, M., de Santiago, I., Lavitas, L.-M., Branco, M. R., et al. (2017) · Nature · doi:10.1038/nature21411 · Cited by 715
Transcriptional Pulsing of a Developmental Gene
Chubb, J. R., Trcek, T., Shenoy, S. M., & Singer, R. H. (2006) · Current Biology · doi:10.1016/j.cub.2006.03.092 · Cited by 714
A Single Oncogenic Enhancer Rearrangement Causes Concomitant EVI1 and GATA2 Deregulation in Leukemia
Gröschel, S., Sanders, M. A., Hoogenboezem, R., de Wit, E., Bouwman, B. A. M., Erpelinck, C., van der Velden, V. H. J., Havermans, M., Avellino, R., van Lom, K., et al. (2014) · Cell · doi:10.1016/j.cell.2014.02.019 · Cited by 687
Formation of new chromatin domains determines pathogenicity of genomic duplications
Franke, M., Ibrahim, D. M., Andrey, G., Schwarzer, W., Heinrich, V., Schöpflin, R., Kraft, K., Kempfer, R., Jerković, I., Chan, W.-L., et al. (2016) · Nature · doi:10.1038/nature19800 · Cited by 673
Long-range chromatin regulatory interactions in vivo
Carter, D., Chakalova, L., Osborne, C. S., Dai, Y.-F., & Fraser, P. (2002) · Nature Genetics · doi:10.1038/ng1051 · Cited by 663
Self-citationFunctional annotation of native enhancers with a Cas9–histone demethylase fusion
Kearns, N. A., Pham, H., Tabak, B., Genga, R. M., Silverstein, N. J., Garber, M., & Maehr, R. (2015) · Nature Methods · doi:10.1038/nmeth.3325 · Cited by 656
An Erythroid Enhancer of BCL11A Subject to Genetic Variation Determines Fetal Hemoglobin Level
Bauer, D. E., Kamran, S. C., Lessard, S., Xu, J., Fujiwara, Y., Lin, C., Shao, Z., Canver, M. C., Smith, E. C., Pinello, L., et al. (2013) · Science · doi:10.1126/science.1242088 · Cited by 653
Topological organization of multichromosomal regions by the long intergenic noncoding RNA Firre
Hacisuleyman, E., Goff, L. A., Trapnell, C., Williams, A., Henao‐Mejia, J., Sun, L., McClanahan, P. D., Hendrickson, D. G., Sauvageau, M., Kelley, D. R., et al. (2014) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2764 · Cited by 644
Systematic mapping of functional enhancer–promoter connections with CRISPR interference
Fulco, C. P., Munschauer, M., Anyoha, R., Munson, G., Grossman, S. R., Perez, E. M., Kane, M., Cleary, B., Lander, E. S., & Engreitz, J. M. (2016) · Science · doi:10.1126/science.aag2445 · Cited by 643
Enhancer redundancy provides phenotypic robustness in mammalian development
Osterwalder, M., Barozzi, I., Tissières, V., Fukuda-Yuzawa, Y., Mannion, B. J., Afzal, S. Y., Lee, E. A., Zhu, Y., Plajzer-Frick, I., Pickle, C. S., et al. (2018) · Nature · doi:10.1038/nature25461 · Cited by 642
CTCF Binding Polarity Determines Chromatin Looping
de Wit, E., Vos, E. S. M., Holwerda, S. J. B., Valdes-Quezada, C., Verstegen, M. J. A. M., Teunissen, H., Splinter, E., Wijchers, P. J., Krijger, P. H. L., & de Laat, W. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.09.023 · Cited by 641
Developmental enhancers and chromosome topology
Furlong, E. E. M., & Levine, M. (2018) · Science · doi:10.1126/science.aau0320 · Cited by 641
A Genome-wide Framework for Mapping Gene Regulation via Cellular Genetic Screens
Gasperini, M., Hill, A. J., McFaline-Figueroa, J. L., Martin, B., Kim, S., Zhang, M. D., Jackson, D., Leith, A., Schreiber, J., Noble, W. S., et al. (2019) · Cell · doi:10.1016/j.cell.2018.11.029 · Cited by 613
Three-dimensional genome architecture: players and mechanisms
Pombo, A., & Dillon, N. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3965 · Cited by 603
Epigenetic signatures distinguish multiple classes of enhancers with distinct cellular functions
Zentner, G. E., Tesar, P. J., & Scacheri, P. C. (2011) · Genome Research · doi:10.1101/gr.122382.111 · Cited by 564
Murrell, A., Heeson, S., & Reik, W. (2004) · Nature Genetics · doi:10.1038/ng1402 · Cited by 556
eRNAs Are Required for p53-Dependent Enhancer Activity and Gene Transcription
Melo, C. A., Drost, J., Wijchers, P. J., van de Werken, H., de Wit, E., Vrielink, J. A. F. O., Elkon, R., Melo, S. A., Léveillé, N., Kalluri, R., et al. (2013) · Molecular Cell · doi:10.1016/j.molcel.2012.11.021 · Cited by 544
Enhancer loops appear stable during development and are associated with paused polymerase
Ghavi-Helm, Y., Klein, F. A., Pakozdi, T., Ciglar, L., Noordermeer, D., Huber, W., & Furlong, E. E. M. (2014) · Nature · doi:10.1038/nature13417 · Cited by 536
CTCF 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
Polycomb group proteins: navigators of lineage pathways led astray in cancer
Bracken, A. P., & Helin, K. (2009) · Nature Reviews Cancer · doi:10.1038/nrc2736 · Cited by 523
Topology of mammalian developmental enhancers and their regulatory landscapes
de Laat, W., & Duboule, D. (2013) · Nature · doi:10.1038/nature12753 · Cited by 521
Kurukuti, S., Tiwari, V. K., Tavoosidana, G., Pugacheva, E., Murrell, A., Zhao, Z., Lobanenkov, V., Reik, W., & Ohlsson, R. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600326103 · Cited by 511
Phenotypic robustness conferred by apparently redundant transcriptional enhancers
Frankel, N., Davis, G. K., Vargas, D., Wang, S., Payre, F., & Stern, D. L. (2010) · Nature · doi:10.1038/nature09158 · Cited by 510
Parkinson-associated risk variant in distal enhancer of α-synuclein modulates target gene expression
Soldner, F., Stelzer, Y., Shivalila, C., Abraham, B. J., Latourelle, J. C., Barrasa, M. I., Goldmann, J. E., Myers, R. H., Young, R. A., & Jaenisch, R. (2016) · Nature · doi:10.1038/nature17939 · Cited by 507
Transcription factor trapping by RNA in gene regulatory elements
Sigova, A. A., Abraham, B. J., Ji, X., Molinie, B., Hannett, N. M., Guo, Y. E., Jangi, M., Giallourakis, C. C., Sharp, P. A., & Young, R. A. (2015) · Science · doi:10.1126/science.aad3346 · Cited by 492
Mumbach, M. R., Satpathy, A. T., Boyle, E. A., Dai, C., Gowen, B. G., Cho, S. W., Nguyen, M. L., Rubin, A. J., Granja, J. M., Kazane, K. R., et al. (2017) · Nature Genetics · doi:10.1038/ng.3963 · Cited by 490
Roelfsema, J. H., White, S. J., Ariyürek, Y., Bartholdi, D., Niedrist, D., Papadia, F., Bacino, C. A., den Dunnen, J. T., van Ommen, G. B., Breuning, M. H., et al. (2005) · The American Journal of Human Genetics · doi:10.1086/429130 · Cited by 487
Dynamic interplay between enhancer–promoter topology and gene activity
Chen, H., Levo, M., Barinov, L., Fujioka, M., Jaynes, J. B., & Gregor, T. (2018) · Nature Genetics · doi:10.1038/s41588-018-0175-z · Cited by 483
A Regulatory Archipelago Controls Hox Genes Transcription in Digits
Montavon, T., Soshnikova, N., Mascrez, B., Joye, E., Thevenet, L., Splinter, E., de Laat, W., Spitz, F., & Duboule, D. (2011) · Cell · doi:10.1016/j.cell.2011.10.023 · Cited by 477
Shadow enhancers as a source of evolutionary novelty
Hong, J.-W., Hendrix, D. A., & Levine, M. S. (2008) · Science · doi:10.1126/science.1160631 · Cited by 474
Enhancer–core-promoter specificity separates developmental and housekeeping gene regulation
Zabidi, M. A., Arnold, C. D., Schernhuber, K., Pagani, M., Rath, M., Frank, O., & Stark, A. (2015) · Nature · doi:10.1038/nature13994 · Cited by 471
Cohesin is positioned in mammalian genomes by transcription, CTCF and Wapl
Busslinger, G. A., Stocsits, R. R., van der Lelij, P., Axelsson, E., Tedeschi, A., Galjart, N., & Peters, J.-M. (2017) · Nature · doi:10.1038/nature22063 · Cited by 468
Hughes, J. R., Roberts, N., McGowan, S., Hay, D., Giannoulatou, E., Lynch, M., De Gobbi, M., Taylor, S., Gibbons, R., & Higgs, D. R. (2014) · Nature Genetics · doi:10.1038/ng.2871 · Cited by 461
The pluripotent regulatory circuitry connecting promoters to their long-range interacting elements
Schoenfelder, S., Furlan-Magaril, M., Mifsud, B., Tavares-Cadete, F., Sugar, R., Javierre, B.-M., Nagano, T., Katsman, Y., Sakthidevi, M., Wingett, S. W., et al. (2015) · Genome Research · doi:10.1101/gr.185272.114 · Cited by 460
Self-citationFunctional and topological characteristics of mammalian regulatory domains
Symmons, O., Uslu, V. V., Tsujimura, T., Ruf, S., Nassari, S., Schwarzer, W., Ettwiller, L., & Spitz, F. (2014) · Genome Research · doi:10.1101/gr.163519.113 · Cited by 455
Transcription Elongation Can Affect Genome 3D Structure
Heinz, S., Texari, L., Hayes, M. G. B., Urbanowski, M., Chang, M. W., Givarkes, N., Rialdi, A., White, K. M., Albrecht, R. A., Pache, L., et al. (2018) · Cell · doi:10.1016/j.cell.2018.07.047 · Cited by 453
Gupta, R. M., Hadaya, J., Trehan, A., Zekavat, S. M., Roselli, C., Klarin, D., Emdin, C. A., Hilvering, C. R. E., Bianchi, V., Mueller, C., et al. (2017) · Cell · doi:10.1016/j.cell.2017.06.049 · Cited by 450
Highly conserved non-coding elements on either side of SOX9 associated with Pierre Robin sequence
Benko, S., Fantes, J. A., Amiel, J., Kleinjan, D., Thomas, S., Ramsay, J. K., Jamshidi, N., Essafi, A., Heaney, S. J. H., Gordon, C. T., et al. (2009) · Nature Genetics · doi:10.1038/ng.329 · Cited by 447
Klann, T. S., Black, J. B., Chellappan, M., Safi, A., Song, L., Hilton, I. B., Crawford, G. E., Reddy, T. E., & Gersbach, C. A. (2017) · Nature Biotechnology · doi:10.1038/nbt.3853 · Cited by 447
Reactivation of developmentally silenced globin genes by forced chromatin looping
Deng, W., Rupon, J. W., Krivega, I., Breda, L., Motta, I., Jahn, K. S., Reik, A., Gregory, P. D., Rivella, S., Dean, A., et al. (2014) · Cell · doi:10.1016/j.cell.2014.05.050 · Cited by 443
Insulated Neighborhoods: Structural and Functional Units of Mammalian Gene Control
Hnisz, D., Day, D. S., & Young, R. A. (2016) · Cell · doi:10.1016/j.cell.2016.10.024 · Cited by 420
CHiCAGO: robust detection of DNA looping interactions in Capture Hi-C data
Cairns, J., Freire-Pritchett, P., Wingett, S. W., Várnai, C., Dimond, A., Plagnol, V., Zerbino, D., Schoenfelder, S., Javierre, B.-M., Osborne, C., et al. (2016) · Genome Biology · doi:10.1186/s13059-016-0992-2 · Cited by 417
Self-citationSagai, T., Hosoya, M., Mizushina, Y., Tamura, M., & Shiroishi, T. (2005) · Development · doi:10.1242/dev.01613 · Cited by 413
Herranz, D., Ambesi-Impiombato, A., Palomero, T., Schnell, S. A., Belver, L., Wendorff, A. A., Xu, L., Castillo-Martin, M., Llobet-Navás, D., Cordon-Cardo, C., et al. (2014) · Nature Medicine · doi:10.1038/nm.3665 · Cited by 405
Functional genetic screens for enhancer elements in the human genome using CRISPR-Cas9
Korkmaz, G., Lopes, R., Ugalde, A. P., Nevedomskaya, E., Han, R., Myacheva, K., Zwart, W. T., Elkon, R., & Agami, R. (2016) · Nature Biotechnology · doi:10.1038/nbt.3450 · Cited by 405
3D Chromosome Regulatory Landscape of Human Pluripotent Cells
Ji, X., Dadon, D. B., Powell, B. E., Fan, Z. P., Borges-Rivera, D., Shachar, S., Weintraub, A. S., Hnisz, D., Pegoraro, G., Lee, T. I., et al. (2016) · Cell Stem Cell · doi:10.1016/j.stem.2015.11.007 · Cited by 400
Polycomb 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
Self-citationRobust 4C-seq data analysis to screen for regulatory DNA interactions
van de Werken, H. J. G., Landan, G., Holwerda, S. J. B., Hoichman, M., Klous, P., Chachik, R., Splinter, E., Valdes‐Quezada, C., Öz, Y., Bouwman, B. A. M., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2173 · Cited by 391
A CTCF-independent role for cohesin in tissue-specific transcriptionPreprint
Schmidt, D., Schwalie, P. C., Ross-Innes, C. S., Hurtado, A., Brown, G. D., Carroll, J. S., Flicek, P., & Odom, D. T. (2010) · Genome Research · doi:10.1101/gr.100479.109 · Cited by 370
Transcription-coupled changes in nuclear mobility of mammalian cis-regulatory elements
Gu, B., Swigut, T., Spencley, A., Bauer, M. R., Chung, M., Meyer, T., & Wysocka, J. (2018) · Science · doi:10.1126/science.aao3136 · Cited by 363
Progressive Loss of Function in a Limb Enhancer during Snake Evolution
Kvon, E. Z., Kamneva, O. K., Melo, U. S., Barozzi, I., Osterwalder, M., Mannion, B. J., Tissières, V., Pickle, C. S., Plajzer-Frick, I., Lee, E. A., et al. (2016) · Cell · doi:10.1016/j.cell.2016.09.028 · Cited by 353
The active spatial organization of the β-globin locus requires the transcription factor EKLF
Drissen, R., Palstra, R.-J., Gillemans, N., Splinter, E., Grosveld, F., Philipsen, S., & de Laat, W. (2004) · Genes & Development · doi:10.1101/gad.317004 · Cited by 352
Enhancer Regulation of Transcriptional Bursting Parameters Revealed by Forced Chromatin Looping
Bartman, C. R., Hsu, S. C., Hsiung, C. C.-S., Raj, A., & Blobel, G. A. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.03.007 · Cited by 345
Genome-wide mapping and analysis of chromosome architecture
Schmitt, A. D., Hu, M., & Ren, B. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.104 · Cited by 344
Chromatin Position Effects Assayed by Thousands of Reporters Integrated in Parallel
Akhtar, W., de Jong, J., Pindyurin, A. V., Pagie, L., Meuleman, W. R. A., de Ridder, J., Berns, A. J. M., Wessels, L. F. A., van Lohuizen, M., & van Steensel, B. (2013) · Cell · doi:10.1016/j.cell.2013.07.018 · Cited by 338
Saha, S., Weber, C. A., Nousch, M., Adame-Arana, O., Hoege, C., Hein, M. Y., Nishimura, E. O., Mahamid, J., Jahnel, M., Jawerth, L. M., et al. (2016) · Cell · doi:10.1016/j.cell.2016.08.006 · Cited by 335
Transcription of the non-coding RNA upperhand controls Hand2 expression and heart development
Anderson, K. M., Anderson, D. M., McAnally, J., Shelton, J. M., Bassel‐Duby, R., & Olson, E. N. (2016) · Nature · doi:10.1038/nature20128 · Cited by 334
A Myc enhancer cluster regulates normal and leukaemic haematopoietic stem cell hierarchies
Bahr, C., von Paleske, L., Uslu, V. V., Remeseiro, S., Takayama, N., Ng, S. W., Murison, A., Langenfeld, K., Petretich, M., Scognamiglio, R., et al. (2018) · Nature · doi:10.1038/nature25193 · Cited by 328
Enhancer biology and enhanceropathies
Smith, E. R., & Shilatifard, A. (2014) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2784 · Cited by 326
Ragoczy, T., Bender, M. A., Telling, A., Byron, R., & Groudine, M. T. (2006) · Genes & Development · doi:10.1101/gad.1419506 · Cited by 326
Isoda, T., Moore, A. J., He, Z., Chandra, V. K., Aida, M., Denholtz, M., van Hamburg, J. P., Fisch, K. M., Chang, A. N., Fahl, S. P., et al. (2017) · Cell · doi:10.1016/j.cell.2017.09.001 · Cited by 323
Genetic Control of Chromatin States in Humans Involves Local and Distal Chromosomal Interactions
Grubert, F., Zaugg, J. B., Kasowski, M., Ursu, O., Spacek, D. V., Martin, A. R., Greenside, P., Srivas, R., Phanstiel, D. H., Pekowska, A., et al. (2015) · Cell · doi:10.1016/j.cell.2015.07.048 · Cited by 319
LHX2- and LDB1-mediated trans interactions regulate olfactory receptor choice
Monahan, K. D., Horta, A., & Lomvardas, S. (2019) · Nature · doi:10.1038/s41586-018-0845-0 · Cited by 318
Dily, F. L., Baù, D., Pohl, A., Vicent, G. P., Serra, F., Soronellas, D., Castellano, G., Wright, R. H. G., Ballaré, C., Filion, G. J. P., et al. (2014) · Genes & Development · doi:10.1101/gad.241422.114 · Cited by 314
YY1 and CTCF orchestrate a 3D chromatin looping switch during early neural lineage commitment
Beagan, J. A., Duong, M. T., Titus, K. R., Zhou, L., Cao, Z., Ma, J., Lachanski, C. V., Gillis, D. R., & Phillips-Cremins, J. E. (2017) · Genome Research · doi:10.1101/gr.215160.116 · Cited by 299
Effect of natural genetic variation on enhancer selection and function
Heinz, S., Romanoski, C. E., Benner, C., Allison, K. A., Kaikkonen, M. U., Orozco, L. D., & Glass, C. K. (2013) · Nature · doi:10.1038/nature12615 · Cited by 298
Discovery of stimulation-responsive immune enhancers with CRISPR activation
Simeonov, D. R., Gowen, B. G., Boontanrart, M., Roth, T. L., Gagnon, J. D., Mumbach, M. R., Satpathy, A. T., Lee, Y., Bray, N. L., Chan, A. Y., et al. (2017) · Nature · doi:10.1038/nature23875 · Cited by 297
Rubin, A. J., Barajas, B. C., Furlan-Magaril, M., Lopez-Pajares, V., Mumbach, M. R., Howard, I., Kim, D. S., Boxer, L. D., Cairns, J., Spivakov, M., et al. (2017) · Nature Genetics · doi:10.1038/ng.3935 · Cited by 293
Self-citationHigh-resolution interrogation of functional elements in the noncoding genome
Sanjana, N. E., Wright, J. B., Zheng, K., Shalem, O., Fontanillas, P., Joung, J., Cheng, C. S., Regev, A., & Zhang, F. (2016) · Science · doi:10.1126/science.aaf7613 · Cited by 290
Genome-wide characterization of mammalian promoters with distal enhancer functions
Dao, L. T. M., Galindo-Albarrán, A. O., Castro-Mondragon, J. A., Andrieu-Soler, C., Medina-Rivera, A., Souaid, C., Charbonnier, G., Griffon, A., Vanhille, L., Stephen, T., et al. (2017) · Nature Genetics · doi:10.1038/ng.3884 · Cited by 281
Manipulation of nuclear architecture through CRISPR-mediated chromosomal looping
Morgan, S. L., Mariano, N. C., Bermudez, A., Arruda, N. L., Wu, F., Luo, Y., Shankar, G., Jia, L., Chen, H., Hu, J.-F., et al. (2017) · Nature Communications · doi:10.1038/ncomms15993 · Cited by 279
Denholtz, M., Bonora, G., Chronis, C., Splinter, E., de Laat, W., Ernst, J., Pellegrini, M., & Plath, K. (2013) · Cell Stem Cell · doi:10.1016/j.stem.2013.08.013 · Cited by 274
Amano, T., Sagai, T., Tanabe, H., Mizushina, Y., Nakazawa, H., & Shiroishi, T. (2009) · Developmental Cell · doi:10.1016/j.devcel.2008.11.011 · Cited by 268
Enhancer Function: Mechanistic and Genome-Wide Insights Come Together
Plank, J. L., & Dean, A. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.06.015 · Cited by 263
Unbiased analysis of potential targets of breast cancer susceptibility loci by Capture Hi-CPreprint
Dryden, N. H., Broome, L. R., Dudbridge, F., Johnson, N., Orr, N., Schoenfelder, S., Nagano, T., Andrews, S., Wingett, S., Kozarewa, I., et al. (2014) · Genome Research · doi:10.1101/gr.175034.114 · Cited by 261
Self-citationA tiling-deletion-based genetic screen for cis-regulatory element identification in mammalian cells
Diao, Y., Fang, R., Li, B., Meng, Z., Yu, J., Qiu, Y., Lin, K. C., Huang, H., Liu, T., Marina, R. J., et al. (2017) · Nature Methods · doi:10.1038/nmeth.4264 · Cited by 259
Beyond Oil and Water—Phase Transitions in Cells
Hyman, A. A., & Simons, K. (2012) · Science · doi:10.1126/science.1223728 · Cited by 251
Vernimmen, D., Gobbi, M. D., Sloane‐Stanley, J. A., Wood, W. G., & Higgs, D. R. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601654 · Cited by 244
Dynamic Rewiring of Promoter-Anchored Chromatin Loops during Adipocyte Differentiation
Siersbæk, R., Madsen, J. G. S., Javierre, B. M., Nielsen, R., Bagge, E. K., Cairns, J., Wingett, S. W., Traynor, S., Spivakov, M., Fraser, P., et al. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.04.010 · Cited by 243
Self-citationApostolou, E., & Thanos, D. (2008) · Cell · doi:10.1016/j.cell.2008.05.052 · Cited by 242
Histone H3 globular domain acetylation identifies a new class of enhancers
Pradeepa, M. M., Grimes, G. R., Kumar, Y., Olley, G., Taylor, G. C. A., Schneider, R., & Bickmore, W. A. (2016) · Nature Genetics · doi:10.1038/ng.3550 · Cited by 240
Cruz-Molina, S., Respuela, P., Tebartz, C., Kolovos, P., Nikolic, M., Fueyo, R., van Ijcken, W. F. J., Grosveld, F., Frommolt, P., Bazzi, H., et al. (2017) · Cell Stem Cell · doi:10.1016/j.stem.2017.02.004 · Cited by 240
Williamson, I., Berlivet, S., Eskeland, R., Boyle, S., Illingworth, R. S., Paquette, D., Dostie, J., & Bickmore, W. A. (2014) · Genes & Development · doi:10.1101/gad.251694.114 · Cited by 239
Jeong, Y., El-Jaick, K. B., Roessler, E., Muenke, M., & Epstein, D. J. (2006) · Development · doi:10.1242/dev.02239 · Cited by 238
High-throughput mapping of regulatory DNA
Rajagopal, N., Srinivasan, S., Kooshesh, K., Guo, Y., Edwards, M. D., Banerjee, B., Syed, T., Emons, B. J. M., Gifford, D. K., & Sherwood, R. I. (2016) · Nature Biotechnology · doi:10.1038/nbt.3468 · Cited by 238
Sex reversal following deletion of a single distal enhancer of Sox9
Gonen, N., Futtner, C. R., Wood, S., Garcia-Moreno, S. A., Salamone, I. M., Samson, S. C., Sekido, R., Poulat, F., Maatouk, D. M., & Lovell-Badge, R. (2018) · Science · doi:10.1126/science.aas9408 · Cited by 235
Functional Dissection of the Enhancer Repertoire in Human Embryonic Stem Cells
Barakat, T. S., Halbritter, F., Zhang, M., Rendeiro, A. F., Perenthaler, E., Bock, C., & Chambers, I. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.06.014 · Cited by 227
Enhancer hubs and loop collisions identified from single-allele topologies
Allahyar, A., Vermeulen, C., Bouwman, B. A. M., Krijger, P. H. L., Verstegen, M. J. A. M., Geeven, G., van Kranenburg, M., Pieterse, M., Straver, R., Haarhuis, J. H. I., et al. (2018) · Nature Genetics · doi:10.1038/s41588-018-0161-5 · Cited by 227
A unified architecture of transcriptional regulatory elements
Andersson, R., Sandelin, A., & Danko, C. G. (2015) · Trends in Genetics · doi:10.1016/j.tig.2015.05.007 · Cited by 225
Transcription factories are nuclear subcompartments that remain in the absence of transcriptionPreprint
Mitchell, J. A., & Fraser, P. (2008) · Genes & Development · doi:10.1101/gad.454008 · Cited by 225
Self-citationSymmons, O., Pan, L., Remeseiro, S., Aktas, T., Klein, F., Huber, W., & Spitz, F. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.10.015 · Cited by 222
Hanssen, L. L. P., Kassouf, M. T., Oudelaar, A. M., Biggs, D., Preece, C., Downes, D. J., Gosden, M., Sharpe, J. A., Sloane-Stanley, J. A., Hughes, J. R., et al. (2017) · Nature Cell Biology · doi:10.1038/ncb3573 · Cited by 219
Capture Hi-C identifies the chromatin interactome of colorectal cancer risk loci
Jäger, R., Migliorini, G., Henrion, M., Kandaswamy, R., Speedy, H. E., Heindl, A., Whiffin, N., Carnicer, M. J., Broome, L. R., Dryden, N. H., et al. (2015) · Nature Communications · doi:10.1038/ncomms7178 · Cited by 216
Self-citationChromosomal Contact Permits Transcription between Coregulated Genes
Fanucchi, S., Shibayama, Y., Burd, S. C., Weinberg, M. S., & Mhlanga, M. M. (2013) · Cell · doi:10.1016/j.cell.2013.09.051 · Cited by 216
Population Variation and Genetic Control of Modular Chromatin Architecture in Humans
Waszak, S. M., Delaneau, O., Gschwind, A. R., Kilpinen, H., Raghav, S. K., Witwicki, R. M., Orioli, A., Wiederkehr, M., Panousis, N. I., Yurovsky, A., et al. (2015) · Cell · doi:10.1016/j.cell.2015.08.001 · Cited by 214
Enhancer Interaction Networks as a Means for Singular Olfactory Receptor Expression
Markenscoff-Papadimitriou, E., Allen, W. E., Colquitt, B. M., Goh, T., Murphy, K. K., Monahan, K., Mosley, C. P., Ahituv, N., & Lomvardas, S. (2014) · Cell · doi:10.1016/j.cell.2014.09.033 · Cited by 214
Martin, P., McGovern, A., Orozco, G., Duffus, K., Yarwood, A., Schoenfelder, S., Cooper, N. J., Barton, A., Wallace, C., Fraser, P., et al. (2015) · Nature Communications · doi:10.1038/ncomms10069 · Cited by 213
Self-citationCuartero, S., Weiss, F. D., Dharmalingam, G., Guo, Y., Ing-Simmons, E., Masella, S., Robles-Rebollo, I., Xiao, X., Wang, Y.-F., Barozzi, I., et al. (2018) · Nature Immunology · doi:10.1038/s41590-018-0184-1 · Cited by 210
Joshi, O., Wang, S.-Y., Kuznetsova, T., Atlasi, Y., Peng, T., Fabre, P. J., Habibi, E., Shaik, J., Saeed, S., Handoko, L., et al. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.11.010 · Cited by 208
Moorthy, S. D., Davidson, S., Shchuka, V. M., Singh, G., Malek-Gilani, N., Langroudi, L., Martchenko, A., So, V., Macpherson, N. N., & Mitchell, J. A. (2016) · Genome Research · doi:10.1101/gr.210930.116 · Cited by 202
Bhatia, S., Bengani, H., Fish, M., Brown, A., Divizia, M. T., de Marco, R., Damante, G., Grainger, R., van Heyningen, V., & Kleinjan, D. A. (2013) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2013.10.028 · Cited by 196
Rev-erbα Dynamically Modulates Chromatin Looping to Control Circadian Gene Transcription
Kim, Y. H., Marhon, S. A., Zhang, Y.-X., Steger, D. J., Won, K.-J., & Lazar, M. (2018) · Science · doi:10.1126/science.aao6891 · Cited by 195
A Sox2 distal enhancer cluster regulates embryonic stem cell differentiation potential
Zhou, H. Y., Katsman, Y., Dhaliwal, N. K., Davidson, S., Macpherson, N. N., Sakthidevi, M., Collura, F., & Mitchell, J. A. (2014) · Genes & Development · doi:10.1101/gad.248526.114 · Cited by 192
A Muscle-Specific Enhancer RNA Mediates Cohesin Recruitment and Regulates Transcription In trans
Tsai, P.-F., Dell’Orso, S., Rodriguez, J., Vivanco, K. O., Ko, K.-D., Jiang, K., Juan, A. H., Sarshad, A. A., Vian, L., Tran, M. D., et al. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.06.008 · Cited by 190
Locus-Specific Targeting to the X Chromosome Revealed by the RNA Interactome of CTCF
Kung, J. T., Kesner, B., An, J. Y., Ahn, J. Y., Cifuentes‐Rojas, C., Colognori, D., Jeon, Y., Szántó, A., Rosario, B. C. D., Pinter, S. F., et al. (2015) · Molecular Cell · doi:10.1016/j.molcel.2014.12.006 · Cited by 180
Lettice, L. A., Hill, A. E., Devenney, P. S., & Hill, R. E. (2007) · Human Molecular Genetics · doi:10.1093/hmg/ddm370 · Cited by 179
Spatial enhancer clustering and regulation of enhancer-proximal genes by cohesin
Ing-Simmons, E., Seitan, V. C., Faure, A. J., Flicek, P., Carroll, T., Dekker, J., Fisher, A. G., Lenhard, B., & Merkenschlager, M. (2015) · Genome Research · doi:10.1101/gr.184986.114 · Cited by 167
Global reorganisation of cis-regulatory units upon lineage commitment of human embryonic stem cells
Freire-Pritchett, P., Schoenfelder, S., Várnai, C., Wingett, S. W., Cairns, J., Collier, A. J., García-Vílchez, R., Furlan-Magaril, M., Osborne, C. S., Fraser, P., et al. (2017) · eLife · doi:10.7554/elife.21926 · Cited by 161
Self-citationVariegated gene expression caused by cell-specific long-range DNA interactions
Noordermeer, D., de Wit, E., Klous, P., van de Werken, H. J. G., Simonis, M., Lopez-Jones, M., Eussen, B., de Klein, A., Singer, R. H., & de Laat, W. L. (2011) · Nature Cell Biology · doi:10.1038/ncb2278 · Cited by 159
Genome-wide mapping of promoter-anchored interactions with close to single-enhancer resolution
Sahlén, P., Abdullayev, I., Ramsköld, D., Matskova, L. V., Rilakovic, N., Lötstedt, B., Albert, T. J., Lundeberg, J., & Sandberg, R. (2015) · Genome biology · doi:10.1186/s13059-015-0727-9 · Cited by 139
BRD4 interacts with NIPBL and BRD4 is mutated in a Cornelia de Lange–like syndrome
Study, D. D. D., Olley, G., Ansari, M., Bengani, H., Grimes, G. R., Rhodes, J., von Kriegsheim, A., Blatnik, A., Stewart, F. J., Wakeling, E. L., et al. (2018) · Nature Genetics · doi:10.1038/s41588-018-0042-y · Cited by 136
LADL: light-activated dynamic looping for endogenous gene expression control
Kim, J. H., Rege, M., Valeri, J., Dunagin, M. C., Metzger, A., Titus, K. R., Gilgenast, T. G., Gong, W., Beagan, J. A., Raj, A., et al. (2019) · Nature Methods · doi:10.1038/s41592-019-0436-5 · Cited by 135
On the Molecular Etiology of Cornelia de Lange Syndrome
Dorsett, D., & Krantz, I. D. (2008) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2008.03450.x · Cited by 134
Long-range enhancers regulating Myc expression are required for normal facial morphogenesis
Uslu, V. V., Petretich, M., Ruf, S., Langenfeld, K., Fonseca, N. A., Marioni, J. C., & Spitz, F. (2014) · Nature Genetics · doi:10.1038/ng.2971 · Cited by 133
Shh and ZRS enhancer colocalisation is specific to the zone of polarising activity
Williamson, I., Lettice, L. A., Hill, R. E., & Bickmore, W. A. (2016) · Development · doi:10.1242/dev.139188 · Cited by 124
A new class of temporarily phenotypic enhancers identified by CRISPR/Cas9-mediated genetic screening
Diao, Y., Li, B., Meng, Z., Jung, I., Lee, A. Y., Dixon, J., Maliskova, L., Guan, K.-L., Shen, Y., & Ren, B. (2016) · Genome Research · doi:10.1101/gr.197152.115 · Cited by 122
Novo, C. L., Javierre, B.-M., Cairns, J., Segonds-Pichon, A., Wingett, S. W., Freire-Pritchett, P., Furlan-Magaril, M., Schoenfelder, S., Fraser, P., & Rugg-Gunn, P. J. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.02.040 · Cited by 119
Self-citationDavison, L. J., Wallace, C., Cooper, J. D., Cope, N. F., Wilson, N. K., Smyth, D. J., Howson, J. M. M., Saleh, N. M., Aljeffery, A., Angus, K. L., et al. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr468 · Cited by 107
Self-citationA cluster of three long-range enhancers directs regionalShhexpression in the epithelial linings
Sagai, T., Amano, T., Tamura, M., Mizushina, Y., Sumiyama, K., & Shiroishi, T. (2009) · Development · doi:10.1242/dev.032714 · Cited by 105
Active RNA Polymerases: Mobile or Immobile Molecular Machines?
Papantonis, A., Larkin, J. D., Wada, Y., Ohta, Y., Ihara, S., Kodama, T., & Cook, P. R. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000419 · Cited by 102
Clock-dependent chromatin topology modulates circadian transcription and behaviorPreprint
Mermet, J., Yeung, J., Hurni, C., Mauvoisin, D., Gustafson, K., Jouffe, C., Nicolas, D., Emmenegger, Y., Gobet, C., Franken, P., et al. (2018) · Genes & Development · doi:10.1101/gad.312397.118 · Cited by 101
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
Regulation of Neuroregeneration by Long Noncoding RNAs
Perry, R. B., Hezroni, H., Goldrich, M. J., & Ulitsky, I. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.09.021 · Cited by 95
McGovern, A., Schoenfelder, S., Martin, P., Massey, J., Duffus, K., Plant, D., Yarwood, A., Pratt, A. G., Anderson, A. E., Isaacs, J. D., et al. (2016) · Genome biology · doi:10.1186/s13059-016-1078-x · Cited by 91
Self-citationInterchromosomal Communication Coordinates Intrinsically Stochastic Expression Between Alleles
Johnston, R. J., & Desplan, C. (2014) · Science · doi:10.1126/science.1243039 · Cited by 89
Caputo, L., Witzel, H. R., Kolovos, P., Cheedipudi, S. M., Looso, M., Mylona, A., van IJcken, W. F. J., Laugwitz, K., Evans, S. Μ., Braun, T. W., et al. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.08.007 · Cited by 88
Function-based identification of mammalian enhancers using site-specific integration
Dickel, D. E., Zhu, Y., Nord, A. S., Wylie, J. N., Akiyama, J. A., Afzal, V., Plajzer-Frick, I., Kirkpatrick, A. M., Göttgens, B., Bruneau, B. G., et al. (2014) · Nature Methods · doi:10.1038/nmeth.2886 · Cited by 87
Gonen, N., Quinn, A., O’Neill, H. C., Koopman, P. A., & Lovell-Badge, R. H. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006520 · Cited by 85
Cajigas, I., Chakraborty, A., Swyter, K. R., Luo, H., Bastidas, M., Nigro, M., Morris, E. R., Chen, S., VanGompel, M. J. W., Leib, D., et al. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.07.024 · Cited by 82
Cited by
Sorted by citations
Chromatin Potential Identified by Shared Single-Cell Profiling of RNA and Chromatin
Ma, S., Zhang, B., LaFave, L. M., Earl, A. S., Chiang, Z., Hu, Y., Ding, J., Brack, A., Kartha, V. K., Tay, T., et al. (2020) · Cell · doi:10.1016/j.cell.2020.09.056 · Cited by 1,146
Determinants of enhancer and promoter activities of regulatory elements
Andersson, R., & Sandelin, A. (2020) · Nature Reviews Genetics · doi:10.1038/s41576-019-0173-8 · Cited by 713
Hasan, N., Choudhary, S., Naaz, N., Sharma, N., & Laskar, R. A. (2021) · Journal of Genetic Engineering and Biotechnology · doi:10.1186/s43141-021-00231-1 · Cited by 582
“The promoter regions that facilitate the transcription of a gene are located too close to a particular gene [54]; along these lines, they can be utilized to be specify the profiling of the genome of the investigated organism.”
BackgroundRoles of transposable elements in the regulation of mammalian transcription
Fueyo, R., Judd, J., Feschotte, C., & Wysocka, J. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00457-y · Cited by 451
Advances in Targeting ‘Undruggable’ transcription Factors With Small Molecules
Henley, M. J., & Koehler, A. N. (2021) · Nature Reviews Drug Discovery · doi:10.1038/s41573-021-00199-0 · Cited by 409
Metadata
- Authors
- Schoenfelder, S., & Fraser, P.
- Affiliations
- Babraham Institute (GB)
- Florida State University (US)
- Corresponding author
- Schoenfelder, Stefan
- Venue
- Nature Reviews Genetics
- Published
- 2019-05-13
- Volume
- 20
- Issue
- 8
- Pages
- 437-455
- ISSN
- 1471-0056 (ISSN-L)
- 1471-0064
- OpenAlex
- W2945038365
- Semantic Scholar
- d851d5037a1a04033beae17bfcd824e8c27b304e
- Cited by
- 1,102
- References
- 218
- Citations by year
- 2026: 118 · 2025: 144 · 2024: 162 · 2023: 170 · 2022: 163 · 2021: 184 · 2020: 127 · 2019: 32
- FWCI
- 11.70
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature Reviews Genetics (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Medical Research Council (MR/L007150/1, MR/T016787/1)
- Biotechnology and Biological Sciences Research Council (BB/J004480/1)
- National Heart, Lung, and Blood Institute (U01HL129971)
- Topics
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Keywords
- enhancer-promoter interactions, enhancers, 3D genome organization, chromatin looping, gene expression regulation, developmental gene regulation, disease
- MeSH terms
- Gene Editing, Animals, Enhancer Elements, Genetic, Humans, Mammals, Promoter Regions, Genetic, Gene Expression, Genome, Genomics
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review