Analysis of hundreds of cis-regulatory landscapes at high resolution in a single, high-throughput experiment
Open accessAbstract
Gene expression during development and differentiation is regulated in a cell- and stage-specific manner by complex networks of intergenic and intragenic cis-regulatory elements whose numbers and representation in the genome far exceed those of structural genes. Using chromosome conformation capture, it is now possible to analyze in detail the interaction between enhancers, silencers, boundary elements and promoters at individual loci, but these techniques are not readily scalable. Here we present a high-throughput approach (Capture-C) to analyze cis interactions, interrogating hundreds of specific interactions at high resolution in a single experiment. We show how this approach will facilitate detailed, genome-wide analysis to elucidate the general principles by which cis-acting sequences control gene expression. In addition, we show how Capture-C will expedite identification of the target genes and functional effects of SNPs that are associated with complex diseases, which most frequently lie in intergenic cis-acting regulatory elements.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The text we found for this paper looks like another document, so the self-check wasn’t run.
Cites
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009) · Genome Biology · doi:10.1186/gb-2009-10-3-r25 · Cited by 21,849 · see citing works
An integrated encyclopedia of DNA elements in the human genome
The ENCODE Project Consortium (2012) · Nature · doi:10.1038/nature11247 · Cited by 18,072 · see citing works
Trapnell, C., Williams, B. A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M. J., Salzberg, S. L., Wold, B. J., & Pachter, L. (2010) · Nature Biotechnology · doi:10.1038/nbt.1621 · Cited by 15,556 · see citing works
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 · see citing works
<tt>BLAT</tt> —The <tt>BLAST</tt> -Like Alignment Tool
Kent, W. J. (2002) · Genome Research · doi:10.1101/gr.229202 · Cited by 8,480 · see citing works
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 · see citing works
Capturing Chromosome Conformation
Dekker, J., Rippe, K., Dekker, M., & Kleckner, N. (2002) · Science · doi:10.1126/science.1067799 · Cited by 3,652 · see citing works
Using RepeatMasker to Identify Repetitive Elements in Genomic Sequences
Tarailo‐Graovac, M., & Chen, N. (2009) · Current Protocols in Bioinformatics · doi:10.1002/0471250953.bi0410s25 · Cited by 3,429 · see citing works
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 · see citing works
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 · see citing works
The 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 · see citing works
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 · see citing works
Chapter 11: Genome-wide association studies
Bush, W. S., & Moore, J. H. (2012) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002822 · Cited by 1,171 · see citing works
An expansive human regulatory lexicon encoded in transcription factor footprints
Neph, S. J., Vierstra, J. D., Stergachis, A. B., Reynolds, A. P., Haugen, E., Vernot, B., Thurman, R. E., John, S., Sandstrom, R. S., Johnson, A., et al. (2012) · Nature · doi:10.1038/nature11212 · Cited by 746 · see citing works
Quantitative analysis of chromosome conformation capture assays (3C-qPCR)
Hagège, H., Klous, P., Braem, C., Splinter, E., Dekker, J., Cathala, G., de Laat, W., & Forné, T. (2007) · Nature Protocols · doi:10.1038/nprot.2007.243 · Cited by 720 · see citing works
Linking disease associations with regulatory information in the human genomePreprint
Schaub, M. A., Boyle, A. P., Kundaje, A. B., Batzoglou, S., & Snyder, M. P. (2012) · Genome Research · doi:10.1101/gr.136127.111 · Cited by 715 · see citing works
Mitoferrin is essential for erythroid iron assimilation
Shaw, G. C., Cope, J. J., Li, L., Corson, K., Hersey, C., Ackermann, G. E., Gwynn, B., Lambert, A. J., Wingert, R. A., Traver, D., et al. (2006) · Nature · doi:10.1038/nature04512 · Cited by 624 · see citing works
Enhancers: five essential questions
Pennacchio, L. A., Bickmore, W. A., Dean, A., Nóbrega, M. A., & Bejerano, G. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3458 · Cited by 584 · see citing works
Robust 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 376 · see citing works
Progress and challenges in genome-wide association studies in humans
Donnelly, P. (2008) · Nature · doi:10.1038/nature07631 · Cited by 358 · see citing works
Boezen, H. M. (2009) · Proceedings of the American Thoracic Society · doi:10.1513/pats.200907-058dp · Cited by 341 · see citing works
Nichols, J., Evans, E. P., & Smith, A. G. (1990) · Development · doi:10.1242/dev.110.4.1341 · Cited by 334 · see citing works
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 · see citing works
Self-citationThe three-dimensional folding of the α-globin gene domain reveals formation of chromatin globules
Baù, D., Sanyal, A., Lajoie, B. R., Capriotti, E., Byron, M., Lawrence, J. B., Dekker, J., & Martı́-Renom, M. A. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1936 · Cited by 267 · see citing works
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 · see citing works
Self-citationA global role for KLF1 in erythropoiesis revealed by ChIP-seq in primary erythroid cellsPreprint
Tallack, M. R., Whitington, T., Yuen, W. S., Wainwright, E. N., Keys, J. R., Gardiner, B., Nourbakhsh, E., Cloonan, N., Grimmond, S. M., Bailey, T. L., et al. (2010) · Genome Research · doi:10.1101/gr.106575.110 · Cited by 220 · see citing works
Kassouf, M. T., Hughes, J. R., Taylor, S., McGowan, S. J., Soneji, S., Green, A. L., Vyas, P., & Porcher, C. (2010) · Genome Research · doi:10.1101/gr.104935.110 · Cited by 176 · see citing works
Self-citationEnhancers and silencers: an integrated and simple model for their function
Kolovos, P., Knoch, T., Grosveld, F. G., Cook, P. R., & Papantonis, A. (2012) · Epigenetics & Chromatin · doi:10.1186/1756-8935-5-1 · Cited by 173 · see citing works
HIF1α synergizes with glucocorticoids to promote BFU-E progenitor self-renewal
Flygare, J., Rayon-Estrada, V., Shin, C., Gupta, S., & Lodish, H. F. (2010) · Blood · doi:10.1182/blood-2010-07-295550 · Cited by 168 · see citing works
Wallace, H. A. C., Marques-Kranc, F., Richardson, M., Luna-Crespo, F., Sharpe, J. A., Hughes, J. R., Wood, W. G., Higgs, D. R., & Smith, A. J. H. (2007) · Cell · doi:10.1016/j.cell.2006.11.044 · Cited by 164 · see citing works
Self-citationHughes, J. R., Cheng, J., Ventress, N., Prabhakar, S., Clark, K., Anguita, E., Gobbi, M. D., de Jong, P., Rubin, E., & Higgs, D. R. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503401102 · Cited by 146 · see citing works
Self-citationStadhouders, R., Kolovos, P., Brouwer, R. W. W., Zuin, J., van den Heuvel, A., Kockx, C. E. M., Palstra, R.-J. T. S., Wendt, K. S., Grosveld, F. G., van IJcken, W. F. J., et al. (2013) · Nature Protocols · doi:10.1038/nprot.2013.018 · Cited by 141 · see citing works
Using GBrowse 2.0 to visualize and share next-generation sequence data
Stein, L. (2013) · Briefings in Bioinformatics · doi:10.1093/bib/bbt001 · Cited by 115 · see citing works
Lower, K. M., Hughes, J. R., De Gobbi, M., Henderson, S., Viprakasit, V., Fisher, C., Goriely, A., Ayyub, H., Sloane-Stanley, J., Vernimmen, D., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0909331106 · Cited by 92 · see citing works
Self-citationVernimmen, D., Marques-Kranc, F., Sharpe, J. A., Sloane-Stanley, J. A., Wood, W. G., Wallace, H. A. C., Smith, A. J. H., & Higgs, D. R. (2009) · Blood · doi:10.1182/blood-2009-03-213439 · Cited by 89 · see citing works
Self-citationGöttgens, B., Broccardo, C., Sánchez, M. J., Deveaux, S., Murphy, G. J., Göthert, J. R., Kotsopoulou, E., Kinston, S., Delaney, L., Piltz, S., et al. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.5.1870-1883.2004 · Cited by 88 · see citing works
High-resolution circular chromosome conformation capture assay
Göndör, A., Rougier, C., & OHLSSON, R. I. (2008) · Nature Protocols · doi:10.1038/nprot.2007.540 · Cited by 88 · see citing works
3C-based technologies to study the shape of the genome
de Laat, W., & Dekker, J. (2012) · Methods · doi:10.1016/j.ymeth.2012.11.005 · Cited by 84 · see citing works
Methods for Identifying Higher-Order Chromatin Structure
Sajan, S. A., & Hawkins, R. D. (2012) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-090711-163818 · Cited by 76 · see citing works
Horáková, A. H., Moseley, S. C., McLaughlin, C. R., Tremblay, D. C., & Chadwick, B. P. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds270 · Cited by 75 · see citing works
Vavouri, T., McEwen, G. K., Woolfe, A., Gilks, W. R., & Elgar, G. S. (2005) · Trends in Genetics · doi:10.1016/j.tig.2005.10.005 · Cited by 74 · see citing works
Tissue-specific histone modification and transcription factor binding in α globin gene expression
Gobbi, M. D., Anguita, E., Hughes, J. R., Sloane-Stanley, J. A., Sharpe, J. A., Koch, C. M., Dunham, I., Gibbons, R. J., Wood, W. G., & Higgs, D. R. (2007) · Blood · doi:10.1182/blood-2007-06-097964 · Cited by 71 · see citing works
Self-citationAmigo, J. D., Yu, M., Troadec, M., Gwynn, B., Cooney, J. D., Lambert, A. J., Chi, N. C., Weiss, M. J., Peters, L. L., Kaplan, J., et al. (2011) · Molecular and Cellular Biology · doi:10.1128/mcb.01010-10 · Cited by 44 · see citing works
Ogilvy, S., Ferreira, R., Piltz, S., Bowen, J. M., Göttgens, B., & Green, A. R. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00931-07 · Cited by 43 · see citing works
Spivak, J. L., Toretti, D., & Dickerman, H. W. (1973) · Blood · doi:10.1182/blood.v42.2.257.257 · Cited by 41 · see citing works
Kang, J. H., Hong, M., Kim, D. W., Park, J., Kang, T., Won, M. H., Baek, N., Moon, B. J., Choi, S. Y., & Kwon, O. (2004) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.2004.04175.x · Cited by 41 · see citing works
Zhou, Z., Li, X., Deng, C., Ney, P. A., Huang, S., & Bungert, J. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.098376 · Cited by 36 · see citing works
Whole exome capture in solution with 3 Gbp of data
Bainbridge, M., Wang, M., Burgess, D. L., Kovar, C., Rodesch, M., D'Ascenzo, M. D., Kitzman, J., Wu, Y.-Q., Newsham, I., Richmond, T., et al. (2010) · Genome Biology · doi:10.1186/gb-2010-11-6-r62 · Cited by 30 · see citing works
Papadopoulos, G. L., Karkoulia, E., Tsamardinos, I., Porcher, C., Ragoussis, J., Bungert, J., & Strouboulis, J. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt167 · Cited by 28 · see citing works
Causes and Consequences of Chromatin Variation between Inbred Mice
Hosseini, M., Goodstadt, L., Hughes, J. R., Kowalczyk, M. S., Gobbi, M. D., Otto, G., Copley, R. R., Mott, R., Higgs, D. R., & Jonathan Flint, C. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003570 · Cited by 19 · see citing works
Self-citationMIG: Multi-Image Genome viewer
McGowan, S. J., Hughes, J. R., Han, Z.-P., & Taylor, S. (2013) · Bioinformatics · doi:10.1093/bioinformatics/btt406 · Cited by 15 · see citing works
Self-citationHigh-resolution analysis of cis -acting regulatory networks at the α-globin locus
Hughes, J. R., Lower, K. M., Dunham, I., Taylor, S., Gobbi, M. D., Sloane-Stanley, J. A., McGowan, S. J., Ragoussis, J., Vernimmen, D., Gibbons, R. J., et al. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2012.0361 · Cited by 13 · see citing works
Self-citationFerreira, R., Spensberger, D., Silber, Y., Dimond, A., Li, J., Green, A. R., & Göttgens, B. (2013) · Molecular and Cellular Biology · doi:10.1128/mcb.01525-12 · Cited by 10 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The Allelic Landscape of Human Blood Cell Trait Variation and Links to Common Complex Disease
Astle, W. J., Elding, H., Jiang, T., Allen, D., Ruklisa, D., Mann, A. L., Mead, D., Bouman, H., Riveros-Mckay, F., Kostadima, M. A., et al. (2016) · Cell · doi:10.1016/j.cell.2016.10.042 · Cited by 1,224 · see citing works
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 · see citing works
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 · see citing works
Long-range enhancer–promoter contacts in gene expression control
Schoenfelder, S., & Fraser, P. (2019) · Nature Reviews Genetics · doi:10.1038/s41576-019-0128-0 · Cited by 1,102 · see citing works
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 · see citing works
The Post-GWAS Era: From Association to Function
Gallagher, M. D., & Chen-Plotkin, A. S. (2018) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2018.04.002 · Cited by 822 · see citing works
the 4D Nucleome Network, Dekker, J., Belmont, A. S., Guttman, M., Leshyk, V. O., Lis, J. T., Lomvardas, S., Mirny, L. A., O’Shea, C. C., Park, P. J., et al. (2017) · Nature · doi:10.1038/nature23884 · Cited by 732 · see citing works
The role of 3D genome organization in development and cell differentiation
Zheng, H., & Xie, W. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0132-4 · Cited by 711 · see citing works
Colocalization of GWAS and eQTL Signals Detects Target Genes
Hormozdiari, F., van de Bunt, M., Segrè, A. V., Li, X., Joo, J. W. J., Bilow, M., Sul, J. H., Sankararaman, S., Pasaniuc, B., & Eskin, E. (2016) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2016.10.003 · Cited by 697 · see citing works
Enhancers as non-coding RNA transcription units: recent insights and future perspectives
Li, W., Notani, D., & Rosenfeld, M. G. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2016.4 · Cited by 710 · see citing works
Önengüt-Gümüşcü, S., Chen, W., Burren, O. S., Cooper, N. J., Quinlan, A. R., Mychaleckyj, J. C., Farber, E., Bonnie, J. K., Szpak, M., Schofield, E. C., et al. (2015) · Nature Genetics · doi:10.1038/ng.3245 · Cited by 675 · see citing works
Non-coding genetic variants in human disease.
Zhang, F., & Lupski, J. (2015) · Human Molecular Genetics · doi:10.1093/hmg/ddv259 · Cited by 581 · see citing works
Three-dimensional genome architecture: players and mechanisms
Pombo, A., & Dillon, N. (2015) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3965 · Cited by 571 · see citing works
Wang, Y., Song, F., Zhang, B., Zhang, L., Xu, J., Kuang, D., Li, D., Choudhary, M. N. K., Li, Y., Hu, M., et al. (2018) · Genome biology · doi:10.1186/s13059-018-1519-9 · Cited by 552 · see citing works
HiCRep: assessing the reproducibility of Hi-C data using a stratum-adjusted correlation coefficient
Yang, T., Zhang, F., Yardımcı, G. G., Song, F., Hardison, R. C., Noble, W. S., Yue, F., & Li, Q. (2017) · Genome Research · doi:10.1101/gr.220640.117 · Cited by 533 · see citing works
CTCF and Cohesin in Genome Folding and Transcriptional Gene Regulation
Merkenschlager, M., & Nora, E. P. (2016) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-083115-022339 · Cited by 505 · see citing works
Methods for mapping 3D chromosome architecture
Kempfer, R., & Pombo, A. (2019) · Nature Reviews Genetics · doi:10.1038/s41576-019-0195-2 · Cited by 502 · see citing works
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 · see citing works
Role of non-coding sequence variants in cancer
Khurana, E., Fu, Y., Chakravarty, D., Demichelis, F., Rubin, M. A., & Gerstein, M. (2016) · Nature Reviews Genetics · doi:10.1038/nrg.2015.17 · Cited by 448 · see citing works
The 3D genome in transcriptional regulation and pluripotency
Gorkin, D. U., Leung, D., & Ren, B. (2014) · Cell Stem Cell · doi:10.1016/j.stem.2014.05.017 · Cited by 391 · see citing works
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 · see citing works
Understanding 3D genome organization by multidisciplinary methods
Jerković, I., & Cavalli, G. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00362-w · Cited by 389 · see citing works
The Three-Dimensional Organization of Mammalian Genomes
Yu, M., & Ren, B. (2017) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100616-060531 · Cited by 366 · see citing works
Cis-regulatory sequences in plants: Their importance, discovery, and future challenges
Schmitz, R. J., Grotewold, E., & Stam, M. E. (2021) · The Plant Cell · doi:10.1093/plcell/koab281 · Cited by 358 · see citing works
The second decade of 3C technologies: detailed insights into nuclear organizationPreprint
Denker, A., & de Laat, W. L. (2016) · Genes & Development · doi:10.1101/gad.281964.116 · Cited by 346 · see citing works
Tak, Y. G., & Farnham, P. (2015) · Epigenetics & Chromatin · doi:10.1186/s13072-015-0050-4 · Cited by 342 · see citing works
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 · see citing works
Regulation of disease-associated gene expression in the 3D genome
Krijger, P. H. L., & de Laat, W. L. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.138 · Cited by 316 · see citing works
The relationship between genome structure and function
Oudelaar, A. M., & Higgs, D. R. (2021) · Nature Reviews Genetics · doi:10.1038/s41576-020-00303-x · Cited by 304 · see citing works
Self-citationBelaghzal, H., Dekker, J., & Gibcus, J. H. (2017) · Methods · doi:10.1016/j.ymeth.2017.04.004 · Cited by 316 · see citing works
In Situ Capture of Chromatin Interactions by Biotinylated dCas9
Liu, X., Zhang, Y., Chen, Y., Li, M., Zhou, F., Li, K., Cao, H., Ni, M., Liu, Y., Gu, Z., et al. (2017) · Cell · doi:10.1016/j.cell.2017.08.003 · Cited by 309 · see citing works
Multiplexed analysis of chromosome conformation at vastly improved sensitivity
Davies, J. O. J., Telenius, J. M., McGowan, S. J., Roberts, N. A., Taylor, S., Higgs, D. R., & Hughes, J. R. (2016) · Nature Methods · doi:10.1038/nmeth.3664 · Cited by 268 · see citing works
Self-citationChromatin structure dynamics during the mitosis-to-G1 phase transition
Zhang, H., Emerson, D. J., Gilgenast, T. G., Titus, K. R., Lan, Y., Huang, P., Zhang, D., Wang, H., Keller, C. A., Giardine, B., et al. (2019) · Nature · doi:10.1038/s41586-019-1778-y · Cited by 271 · see citing works
Recent evidence that TADs and chromatin loops are dynamic structures
Hansen, A. S., Cattoglio, C., Darzacq, X., & Tjian, R. (2018) · Nucleus · doi:10.1080/19491034.2017.1389365 · Cited by 266 · see citing works
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 254 · see citing works
Barutcu, A. R., Lajoie, B. R., McCord, R. P., Tye, C. E., Hong, D., Messier, T. L., Browne, G., van Wijnen, A. J., Lian, J. B., Stein, J. L., et al. (2015) · Genome Biology · doi:10.1186/s13059-015-0768-0 · Cited by 250 · see citing works
PRC1 catalytic activity is central to polycomb system function
Blackledge, N. P., Fursova, N. A., Kelley, J. R., Huseyin, M. K., Feldmann, A., & Klose, R. J. (2020) · Molecular Cell · doi:10.1016/j.molcel.2019.12.001 · Cited by 243 · see citing works
Enhancer redundancy in development and disease
Kvon, E. Z., Waymack, R., Gad, M., & Wunderlich, Z. (2021) · Nature Reviews Genetics · doi:10.1038/s41576-020-00311-x · Cited by 226 · see citing works
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 229 · see citing works
An Overview of Genome Organization and How We Got There: from FISH to Hi-C
Fraser, J., Williamson, I., Bickmore, W. A., & Dostie, J. (2015) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00006-15 · Cited by 218 · see citing works
Transcription in Living Cells: Molecular Mechanisms of Bursting
Rodriguez, J., & Larson, D. R. (2020) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-011520-105250 · Cited by 224 · see citing works
Symmons, 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 · see citing works
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 210 · see citing works
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 · see citing works
Self-citationEnhancer 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 · see citing works
4C-seq from beginning to end: A detailed protocol for sample preparation and data analysis
Krijger, P. H. L., Geeven, G., Bianchi, V., Hilvering, C. R. E., & de Laat, W. L. (2019) · Methods · doi:10.1016/j.ymeth.2019.07.014 · Cited by 201 · see citing works
diffHic: a Bioconductor package to detect differential genomic interactions in Hi-C data
Lun, A. T. L., & Smyth, G. K. (2015) · BMC Bioinformatics · doi:10.1186/s12859-015-0683-0 · Cited by 199 · see citing works
McCord, R. P., Kaplan, N., & Giorgetti, L. (2020) · Molecular Cell · doi:10.1016/j.molcel.2019.12.021 · Cited by 204 · see citing works
Super-enhancers include classical enhancers and facilitators to fully activate gene expression
Blayney, J. W., Francis, H., Rampasekova, A., Camellato, B., Mitchell, L., Stolper, R., Cornell, L., Babbs, C., Boeke, J. D., Higgs, D. R., et al. (2023) · Cell · doi:10.1016/j.cell.2023.11.030 · Cited by 196 · see citing works
Self-citationSingle-allele chromatin interactions identify regulatory hubs in dynamic compartmentalized domains
Oudelaar, A. M., Davies, J. O. J., Hanssen, L. L. P., Telenius, J. M., Schwessinger, R., Liu, Y., Brown, J. M., Downes, D. J., Chiariello, A. M., Bianco, S., et al. (2018) · Nature Genetics · doi:10.1038/s41588-018-0253-2 · Cited by 196 · see citing works
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 190 · see citing works
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 · see citing works
Polymer Simulations of Heteromorphic Chromatin Predict the 3D Folding of Complex Genomic Loci
Buckle, A., Brackley, C. A., Boyle, S., Marenduzzo, D., & Gilbert, N. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.09.016 · Cited by 172 · see citing works
Cohesin Disrupts Polycomb-Dependent Chromosome Interactions in Embryonic Stem Cells
Rhodes, J. D. P., Feldmann, A., Hernández-Rodríguez, B., Díaz, N., Brown, J. M., Fursova, N. A., Blackledge, N. P., Prathapan, P., Dobrinic, P., Huseyin, M. K., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2019.12.057 · Cited by 187 · see citing works
Fine-scale chromatin interaction maps reveal the cis-regulatory landscape of human lincRNA genes
Ma, W., Ay, F., Lee, C., Gülsoy, G., Deng, X., Cook, S. M., Hesson, J., Cavanaugh, C., Ware, C. B., Krumm, A., et al. (2014) · Nature Methods · doi:10.1038/nmeth.3205 · Cited by 186 · see citing works
Defining genome architecture at base-pair resolution
Peng, H., Badat, M., Hanssen, L. L. P., Hentges, L. D., Crump, N. T., Downes, D. J., Jeziorska, D. M., Oudelaar, A. M., Schweßinger, R., Taylor, S., et al. (2021) · Nature · doi:10.1038/s41586-021-03639-4 · Cited by 176 · see citing works
Self-citationChromosome conformation capture technologies and their impact in understanding genome function
Sati, S., & Cavalli, G. (2016) · Chromosoma · doi:10.1007/s00412-016-0593-6 · Cited by 181 · see citing works
van de Bunt, M., Fox, J. E. M., Dai, X.-Q., Barrett, A., Grey, C. L., Li, L., Bennett, A. J., Johnson, P. R. V., Rajotte, R. V., Gaulton, K. J., et al. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005694 · Cited by 174 · see citing works
Loss of Extreme Long-Range Enhancers in Human Neural Crest Drives a Craniofacial Disorder
Long, H. K., Osterwalder, M., Welsh, I. C., Hansen, K. L., Davies, J. O. J., Liu, Y. E., Koska, M., Adams, A. T., Aho, R., Arora, N., et al. (2020) · Cell stem cell · doi:10.1016/j.stem.2020.09.001 · Cited by 160 · see citing works
Self-citationA supervised learning framework for chromatin loop detection in genome-wide contact maps
Salameh, T. J., Wang, X., Song, F., Zhang, B., Wright, S. M., Khunsriraksakul, C., Ruan, Y., & Yue, F. (2020) · Nature Communications · doi:10.1038/s41467-020-17239-9 · Cited by 165 · see citing works
VHL Deficiency Drives Enhancer Activation of Oncogenes in Clear Cell Renal Cell Carcinoma
Yao, X., Tan, J. Y., Lim, K. J., Koh, J., Ooi, W. F., Li, Z., Huang, D., Xing, M., Chan, Y. S., Qu, J. Z., et al. (2017) · Cancer Discovery · doi:10.1158/2159-8290.cd-17-0375 · Cited by 166 · see citing works
Self-citationMeasuring the reproducibility and quality of Hi-C data
Yardımcı, G. G., Özadam, H., Sauria, M. E. G., Ursu, O., Yan, K., Yang, T., Chakraborty, A., Kaul, A., Lajoie, B. R., Song, F., et al. (2019) · Genome biology · doi:10.1186/s13059-019-1658-7 · Cited by 171 · see citing works
Gómez-Marín, C., Tena, J. J., Acemel, R. D., López-Mayorga, M., Naranjo, S., de la Calle-Mustienes, E., Maeso, I., Beccari, L., Aneas, I., Vielmas, E., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1505463112 · Cited by 159 · see citing works
Chesi, A., Wagley, Y., Johnson, M. E., Manduchi, E., Su, C., Lu, S., Leonard, M. E., Hodge, K. M., Pippin, J. A., Hankenson, K. D., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09302-x · Cited by 158 · see citing works
How best to identify chromosomal interactions: a comparison of approaches
Davies, J. O. J., Oudelaar, A. M., Higgs, D. R., & Hughes, J. R. (2017) · Nature Methods · doi:10.1038/nmeth.4146 · Cited by 148 · see citing works
Self-citationDOT1L inhibition reveals a distinct subset of enhancers dependent on H3K79 methylation
Godfrey, L., Crump, N. T., Thorne, R., Lau, I., Repapi, E., Dimou, D., Smith, A., Harman, J. R., Telenius, J. M., Oudelaar, A. M., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-10844-3 · Cited by 146 · see citing works
Self-citationPlant Enhancers: A Call for Discovery
Weber, B., Zicola, J., Oka, R., & Stam, M. E. (2016) · Trends in Plant Science · doi:10.1016/j.tplants.2016.07.013 · Cited by 140 · see citing works
HOTTIP-dependent R-loop formation regulates CTCF boundary activity and TAD integrity in leukemia
Luo, H., Zhu, G., Eshelman, M. A., Fung, T. K., Lai, Q., Wang, F., Zeisig, B. B., Lesperance, J., Ma, X., Shi, C., et al. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.01.014 · Cited by 145 · see citing works
Reconstruction of the Global Neural Crest Gene Regulatory Network In Vivo
Williams, R. M., Candido-Ferreira, I., Repapi, E., Gavriouchkina, D., Senanayake, U., Ling, I. T. C., Telenius, J., Taylor, S., Hughes, J., & Sauka-Spengler, T. (2019) · Developmental Cell · doi:10.1016/j.devcel.2019.10.003 · Cited by 122 · see citing works
Self-citationThe BET Protein BRD2 Cooperates with CTCF to Enforce Transcriptional and Architectural Boundaries
Hsu, S. C., Gilgenast, T. G., Bartman, C., Edwards, C. R., Stonestrom, A. J., Huang, P., Emerson, D. J., Evans, P., Werner, M. T., Keller, C. A., et al. (2017) · Molecular Cell · doi:10.1016/j.molcel.2017.02.027 · Cited by 138 · see citing works
Sub-nucleosomal Genome Structure Reveals Distinct Nucleosome Folding Motifs
Ohno, M., Ando, T., Priest, D. G., Kumar, V., Yoshida, Y., & Taniguchi, Y. (2019) · Cell · doi:10.1016/j.cell.2018.12.014 · Cited by 141 · see citing works
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 131 · see citing works
Andrey, G., Schöpflin, R., Jerković, I., Heinrich, V., Ibrahim, D. M., Paliou, C., Hochradel, M., Timmermann, B., Haas, S. A., Vingron, M., et al. (2016) · Genome Research · doi:10.1101/gr.213066.116 · Cited by 122 · see citing works
The three-dimensional genome: regulating gene expression during pluripotency and development
Andrey, G., & Mundlos, S. (2017) · Development · doi:10.1242/dev.148304 · Cited by 129 · see citing works
The chromosome folding problem and how cells solve it
Dekker, J., & Mirny, L. A. (2024) · Cell · doi:10.1016/j.cell.2024.10.026 · Cited by 112 · see citing works
The Mediator complex regulates enhancer-promoter interactions
Ramasamy, S., Aljahani, A., Karpińska, M. A., Cao, T. B. N., Velychko, T., Cruz, J. N., Lidschreiber, M., & Oudelaar, A. M. (2023) · Nature Structural & Molecular Biology · doi:10.1038/s41594-023-01027-2 · Cited by 132 · see citing works
Chromatin conformation analysis of primary patient tissue using a low input Hi-C method
Díaz, N., Kruse, K., Erdmann, T., Staiger, A. M., Ott, G., Lenz, G., & Vaquerizas, J. M. (2018) · Nature Communications · doi:10.1038/s41467-018-06961-0 · Cited by 121 · see citing works
Dynamics of the 4D Genome during in Vivo Lineage Specification and Differentiation
Oudelaar, A. M., Beagrie, R. A., Gosden, M., de Ornellas, S., Georgiades, E., Kerry, J., Hidalgo, D., Carrelha, J., Shivalingam, A., El-Sagheer, A. H., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-16598-7 · Cited by 119 · see citing works
Self-citationBrackley, C. A., Brown, J. M., Waithe, D., Babbs, C., Davies, J. O. J., Hughes, J. R., Buckle, V. J., & Marenduzzo, D. (2016) · Genome biology · doi:10.1186/s13059-016-0909-0 · Cited by 110 · see citing works
Self-citationA hyperactive transcriptional state marks genome reactivation at the mitosis–G1 transitionPreprint
Hsiung, C. C. ‐., Bartman, C., Huang, P., Ginart, P., Stonestrom, A. J., Keller, C. A., Face, C. J., Jahn, K. S., Evans, P., Sankaranarayanan, L., et al. (2016) · Genes & Development · doi:10.1101/gad.280859.116 · Cited by 105 · see citing works
4DGenome: a comprehensive database of chromatin interactions
Teng, L., He, B., Wang, J., & Tan, K. (2016) · Bioinformatics · doi:10.1093/bioinformatics/btw375 · Cited by 114 · see citing works
Enhancer deregulation in cancer and other diseases
Herz, H. (2016) · BioEssays · doi:10.1002/bies.201600106 · Cited by 107 · see citing works
Promoter Capture Hi-C: High-resolution, Genome-wide Profiling of Promoter Interactions
Schoenfelder, S., Javierre, B. M., Furlan-Magaril, M., Wingett, S., & Fraser, P. (2018) · Journal of Visualized Experiments · doi:10.3791/57320 · Cited by 114 · see citing works
A Dementia-Associated Risk Variant near TMEM106B Alters Chromatin Architecture and Gene Expression
Gallagher, M. D., Posavi, M., Huang, P., Unger, T. L., Berlyand, Y., Gruenewald, A. L., Chesi, A., Manduchi, E., Wells, A. D., Grant, S. F. A., et al. (2017) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2017.09.004 · Cited by 109 · see citing works
peakC: a flexible, non-parametric peak calling package for 4C and Capture-C data
Geeven, G., Teunissen, H., de Laat, W. L., & de Wit, E. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky443 · Cited by 102 · see citing works
The Ftx Noncoding Locus Controls X Chromosome Inactivation Independently of Its RNA Products
Furlan, G., Hernandez, N. G., Huret, C., Galupa, R., van Bemmel, J. G., Romito, A., Heard, É., Morey, C., & Rougeulle, C. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.03.024 · Cited by 106 · see citing works
Huang, P., Zhang, P., Xu, S.-G., Wang, H., Zhang, X., & Zhang, H. (2019) · Nanoscale · doi:10.1039/c9nr08890c · Cited by 107 · see citing works
4DGenome: a comprehensive database of chromatin interactions
Teng, L., He, B., Wang, J., & Tan, K. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btv158 · Cited by 107 · see citing works
Spurious transcription factor binding: Non‐functional or genetically redundant?
Spivakov, M. (2014) · BioEssays · doi:10.1002/bies.201400036 · Cited by 96 · see citing works
Mettananda, S., Fisher, C. A., Hay, D., Badat, M., Quek, L. S., Clark, K., Hublitz, P., Downes, D. J., Kerry, J., Gosden, M. E., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00479-7 · Cited by 104 · see citing works
Self-citationThe impact of chromosomal rearrangements on regulation of gene expression
Harewood, L., & Fraser, P. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddu278 · Cited by 100 · see citing works
UMI-4C for quantitative and targeted chromosomal contact profiling
Schwartzman, O., Mukamel, Z., Elkayam, N. O., Olivares‐Chauvet, P., Lubling, Y., Landan, G., Izraeli, S., & Tanay, A. (2016) · Nature Methods · doi:10.1038/nmeth.3922 · Cited by 94 · see citing works
3C and 3C-based techniques: the powerful tools for spatial genome organization deciphering
Han, J., Zhang, Z., & Wang, K. (2018) · Molecular Cytogenetics · doi:10.1186/s13039-018-0368-2 · Cited by 97 · see citing works
Hi-C analysis: from data generation to integration
Pal, K., Forcato, M., & Ferrari, F. (2018) · Biophysical Reviews · doi:10.1007/s12551-018-0489-1 · Cited by 97 · see citing works
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 · see citing works
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 91 · see citing works
Trac-looping measures genome structure and chromatin accessibility
Lai, B., Tang, Q., Jin, W., Hu, G., Wangsa, D., Cui, K., Stanton, B. Z., Ren, G., Ding, Y., Zhao, M., et al. (2018) · Nature Methods · doi:10.1038/s41592-018-0107-y · Cited by 85 · see citing works
4C-ker: A Method to Reproducibly Identify Genome-Wide Interactions Captured by 4C-Seq Experiments
Raviram, R., Rocha, P. P., Müller, C. L., Miraldi, E. R., Badri, S., Fu, Y., Swanzey, E., Proudhon, C., Snetkova, V., Bonneau, R., et al. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004780 · Cited by 89 · see citing works
HSP90: Enabler of Cancer Adaptation
Jaeger, A. M., & Whitesell, L. J. (2018) · Annual Review of Cancer Biology · doi:10.1146/annurev-cancerbio-030518-055533 · Cited by 91 · see citing works
Oudelaar, A. M., Harrold, C. L., Hanssen, L. L. P., Telenius, J. M., Higgs, D. R., & Hughes, J. R. (2019) · Nature Communications · doi:10.1038/s41467-019-13404-x · Cited by 80 · see citing works
Self-citation
- Authors
- Hughes, J. R., Roberts, N., McGowan, S., Hay, D., Giannoulatou, E., Lynch, M., De Gobbi, M., Taylor, S., Gibbons, R., & Higgs, D. R.
- Affiliations
- University of Oxford (GB)
- Corresponding author
- Hughes, Jim R
- Higgs, Douglas R
- ORCID
- Venue
- Nature Genetics
- Published
- 2014-01-12
- Volume
- 46
- Issue
- 2
- Pages
- 205-212
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- OpenAlex
- W1974223852
- Cited by
- 461
- References
- 53
- Citations by year
- 2026: 11 · 2025: 11 · 2024: 29 · 2023: 38 · 2022: 31 · 2021: 50 · 2020: 53 · 2019: 50 · 2018: 48 · 2017: 40 · 2016: 43 · 2015: 38 · 2014: 18
- FWCI
- 17.49
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- other-oa
- www.springer.com/tdm (tdm)
- Locations
- Nature Genetics (publishedVersion)
- PubMed (publishedVersion)
- Oxford University Research Archive (ORA) (University of Oxford) (acceptedVersion)
- Institutional Research Information System University of Turin (University of Turin) (submittedVersion, other-oa)
- Funders
- Wellcome Trust (91070, 090532, 090532/Z/09/Z, 090532/Z/09/, 090532/Z)
- Medical Research Council (G0900747 91070, 090532/Z09/Z)
- 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 › Genetics › Genetic Associations and Epidemiology
- Keywords
- cis-regulatory elements, chromosome conformation capture, enhancers, silencers, boundary elements, promoter, gene expression regulation, single nucleotide polymorphisms, complex disease genetics, target gene identification
- MeSH terms
- Animals, Base Sequence, Female, Humans, Molecular Sequence Data, Gene Library, Sequence Analysis, DNA, Gene Expression Regulation, Developmental, Polymorphism, Single Nucleotide, Genetic Diseases, Inborn, Chromatin Immunoprecipitation, Regulatory Elements, Transcriptional, Mice, High-Throughput Screening Assays
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