Comparison of Hi-C results using in-solution versus in-nucleus ligation
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BACKGROUND: Chromosome conformation capture and various derivative methods such as 4C, 5C and Hi-C have emerged as standard tools to analyze the three-dimensional organization of the genome in the nucleus. These methods employ ligation of diluted cross-linked chromatin complexes, intended to favor proximity-dependent, intra-complex ligation. During development of single-cell Hi-C, we devised an alternative Hi-C protocol with ligation in preserved nuclei rather than in solution. Here we directly compare Hi-C methods employing in-nucleus ligation with the standard in-solution ligation. RESULTS: We show in-nucleus ligation results in consistently lower levels of inter-chromosomal contacts. Through chromatin mixing experiments we show that a significantly large fraction of inter-chromosomal contacts are the result of spurious ligation events formed during in-solution ligation. In-nucleus ligation significantly reduces this source of experimental noise, and results in improved reproducibility between replicates. We also find that in-nucleus ligation eliminates restriction fragment length bias found with in-solution ligation. These improvements result in greater reproducibility of long-range intra-chromosomal and inter-chromosomal contacts, as well as enhanced detection of structural features such as topologically associated domain boundaries. CONCLUSIONS: We conclude that in-nucleus ligation captures chromatin interactions more consistently over a wider range of distances, and significantly reduces both experimental noise and bias. In-nucleus ligation creates higher quality Hi-C libraries while simplifying the experimental procedure. We suggest that the entire range of 3C applications are likely to show similar benefits from in-nucleus ligation.
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Low trans-chromosomal contacts are indicative of high library quality.
“indicative of high library quality13”
From Cell-cycle dynamics of chromosomal organization at single-cell resolution (2017) · cites this paper as [13]
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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
Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y. C., Laslo, P., Cheng, J. X., Murre, C., Singh, H., & Glass, C. K. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.05.004 · Cited by 13,382 · see citing works
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 · 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
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
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 · 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
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 · see citing works
Self-citationIterative correction of Hi-C data reveals hallmarks of chromosome organization
Imakaev, M., Fudenberg, G., McCord, R. P., Naumova, N., Goloborodko, A., Lajoie, B. R., Dekker, J., & Mirny, L. A. (2012) · Nature Methods · doi:10.1038/nmeth.2148 · Cited by 1,423 · 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 · cited 1× · see citing works
“This was done by multiplying the eigenvector by −1 if the Pearson correlation coefficient of the eigenvector and the H3K4me3 histone modification mark ChIPseq [19, 28] profile was negative.”
MethodAnalyzing and minimizing PCR amplification bias in Illumina sequencing libraries
Aird, D., Ross, M. G., Chen, W.-S., Danielsson, M., Fennell, T., Russ, C., Jaffe, D. B., Nusbaum, C., & Gnirke, A. (2011) · Genome Biology · doi:10.1186/gb-2011-12-2-r18 · Cited by 1,174 · see citing works
Exploring the three-dimensional organization of genomes: Interpreting chromatin interaction data
Dekker, J., Marti-Renom, M. A., & Mirny, L. A. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3454 · Cited by 1,068 · see citing works
Comparative Hi-C Reveals that CTCF Underlies Evolution of Chromosomal Domain Architecture
Vietri Rudan, M., Barrington, C., Henderson, S., Ernst, C., Odom, D. T., Tanay, A., & Hadjur, S. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.02.004 · Cited by 680 · see citing works
Yaffe, E., & Tanay, A. (2011) · Nature Genetics · doi:10.1038/ng.947 · Cited by 645 · see citing works
Spatial Organization of the Mouse Genome and Its Role in Recurrent Chromosomal Translocations
Zhang, Y., McCord, R. P., Ho, Y.-J., Lajoie, B. R., Hildebrand, D. G., Simon, A. C., Becker, M. S., Alt, F. W., & Dekker, J. (2012) · Cell · doi:10.1016/j.cell.2012.02.002 · Cited by 545 · see citing works
Kalhor, R., Tjong, H., Jayathilaka, N., Alber, F., & Chen, L. (2011) · Nature Biotechnology · doi:10.1038/nbt.2057 · Cited by 532 · 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
Self-citationCohesin-mediated interactions organize chromosomal domain architecture
Sofueva, S., Yaffe, E., Chan, W., Georgopoulou, D., Vietri Rudan, M., Mira‐Bontenbal, H., Pollard, S. M., Schroth, G. P., Tanay, A., & Hadjur, S. (2013) · The EMBO Journal · doi:10.1038/emboj.2013.237 · Cited by 394 · see citing works
The three 'C' s of chromosome conformation capture: controls, controls, controls
Dekker, J. (2005) · Nature Methods · doi:10.1038/nmeth823 · Cited by 347 · see citing works
Whole-genome haplotype reconstruction using proximity-ligation and shotgun sequencing
Selvaraj, S., Dixon, J. R., Bansal, V., & Ren, B. (2013) · Nature Biotechnology · doi:10.1038/nbt.2728 · Cited by 286 · see citing works
Targeted sequencing by proximity ligation for comprehensive variant detection and local haplotyping
de Vree, P. J. P., de Wit, E., Yilmaz, M., van de Heijning, M., Klous, P., Verstegen, M. J. A. M., Wan, Y., Teunissen, H., Krijger, P. H. L., Geeven, G., et al. (2014) · Nature Biotechnology · doi:10.1038/nbt.2959 · Cited by 270 · 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
Self-citationCapture 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
Self-citationComet, I. V., Schuettengruber, B., Sexton, T., & Cavalli, G. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002059108 · Cited by 124 · see citing works
Gavrilov, A. A., Gushchanskaya, E. S., Strelkova, O., Zhironkina, O., Kireev, I. I., Iarovaia, O. V., & Razin, S. V. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt067 · Cited by 87 · see citing works
SnapShot: Chromosome Conformation Capture
Hakim, O., & Misteli, T. (2012) · Cell · doi:10.1016/j.cell.2012.02.019 · Cited by 62 · see citing works
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Research works printed but not linked: 1
- [29]Datasets deposited at Gene Expression Omnibus, GSE70181. http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?token=wtmfywywjrshbip&acc=GSE70181.
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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
Javierre, 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 · see citing works
Self-citationYY1 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 · see citing works
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 · see citing works
Self-citationCell-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 · see citing works
Self-citationHiCUP: pipeline for mapping and processing Hi-C data
Wingett, S., Ewels, P., Furlan-Magaril, M., Nagano, T., Schoenfelder, S., Fraser, P., & Andrews, S. (2015) · F1000Research · doi:10.12688/f1000research.7334.1 · Cited by 724 · see citing works
Self-citationWang, 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
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Jerković, I., & Cavalli, G. (2021) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-021-00362-w · Cited by 389 · see citing works
The second decade of 3C technologies: detailed insights into nuclear organizationPreprint
Denker, A., & de Laat, W. (2016) · Genes & Development · doi:10.1101/gad.281964.116 · Cited by 323 · 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
Lhx2/Ldb1-mediated trans interactions regulate olfactory receptor choice
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Belaghzal, H., Dekker, J., & Gibcus, J. (2016) · bioRxiv · doi:10.1016/j.ymeth.2017.04.004 · Cited by 214 · see citing works
Miguel-Escalada, I., Bonàs‐Guarch, S., Cebola, I., Ponsa-Cobas, J., Mendieta-Esteban, J., Atla, G., Javierre, B. M., Rolando, D., Farabella, I., Morgan, C. C., et al. (2019) · Nature Genetics · doi:10.1038/s41588-019-0457-0 · Cited by 259 · see citing works
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Aymard, F., Aguirrebengoa, M., Guillou, E., Javierre, B. M., Bugler, B., Arnould, C., Rocher, V., Iacovoni, J. S., Biernacka, A., Skrzypczak, M., et al. (2017) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3387 · Cited by 263 · see citing works
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Zhan, Y., Mariani, L., Barozzi, I., Schulz, E. G., Blüthgen, N., Stadler, M. B., Tiana, G., & Giorgetti, L. (2017) · Genome Research · doi:10.1101/gr.212803.116 · Cited by 214 · see citing works
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Meyer, A., Schloissnig, S., Franchini, P., Du, K., Woltering, J. M., Irisarri, I., Wong, W. Y., Nowoshilow, S., Kneitz, S., Kawaguchi, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03198-8 · Cited by 211 · see citing works
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 198 · see citing works
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Zhang, Y., An, L., Xu, J., Zhang, B., Zheng, W. J., Hu, M., Tang, J., & Yue, F. (2018) · Nature Communications · doi:10.1038/s41467-018-03113-2 · Cited by 186 · see citing works
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Harewood, L., Kishore, K., Eldridge, M. D., Wingett, S., Pearson, D., Schoenfelder, S., Collins, V. P., & Fraser, P. (2017) · Genome Biology · doi:10.1186/s13059-017-1253-8 · Cited by 178 · see citing works
Self-citationLu, L., Liu, X., Huang, W., Giusti‐Rodríguez, P., Cui, J., Zhang, S., Xu, W., Wen, Z., Ma, S., Rosen, J. D., et al. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.06.007 · Cited by 170 · see citing works
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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
Kaaij, L. J. T., Mohn, F., van der Weide, R. H., de Wit, E., & Bühler, M. (2019) · Cell · doi:10.1016/j.cell.2019.08.007 · Cited by 133 · see citing works
Nagano, T., Lubling, Y., Yaffe, E., Wingett, S., Dean, W., Tanay, A., & Fraser, P. (2015) · Nature Protocols · doi:10.1038/nprot.2015.127 · Cited by 159 · see citing works
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Zhu, W., Hu, B., Becker, C., Doğan, E. S., Berendzen, K. W., Weigel, D., & Liu, C. (2017) · Genome biology · doi:10.1186/s13059-017-1281-4 · Cited by 112 · see citing works
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Liu, M., Lu, Y., Yang, B., Chen, Y., Radda, J. S. D., Hu, M., Katz, S. G., & Wang, S. (2020) · Nature Communications · doi:10.1038/s41467-020-16732-5 · Cited by 107 · see citing works
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Quigley, I. K., & Kintner, C. R. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006538 · Cited by 97 · see citing works
Yang, M., Vesterlund, M., Siavelis, I., Moura‐Castro, L. H., Castor, A., Fioretos, T., Jafari, R., Lilljebjörn, H., Odom, D. T., Olsson, L., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09469-3 · Cited by 97 · see citing works
Madsen, J. G. S., Madsen, M. S., Rauch, A., Traynor, S., Hauwaert, E. L. V., Haakonsson, A. K., Javierre, B. M., Hyldahl, M., Fraser, P., & Mandrup, S. (2020) · Nature Genetics · doi:10.1038/s41588-020-0709-z · Cited by 94 · see citing works
Self-citationPan, D. Z., Garske, K. M., Alvarez, M., Bhagat, Y. V., Boocock, J., Nikkola, E., Miao, Z., Raulerson, C. K., Cantor, R. M., Civelek, M., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03554-9 · Cited by 93 · see citing works
Liang, Z., Li, G., Wang, Z., Djekidel, M. N., Li, Y., Qian, M., Zhang, M. Q., & Chen, Y. (2017) · Nature Communications · doi:10.1038/s41467-017-01754-3 · Cited by 89 · see citing works
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Qin, Y., Grimm, S. A., Roberts, J. D., Chrysovergis, K., & Wade, P. A. (2020) · Nature Communications · doi:10.1038/s41467-020-14796-x · Cited by 67 · see citing works
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Cresswell, K. G., Stansfield, J. C., & Dozmorov, M. G. (2020) · BMC Bioinformatics · doi:10.1186/s12859-020-03652-w · Cited by 63 · see citing works
The Epstein-Barr Virus Episome Maneuvers between Nuclear Chromatin Compartments during Reactivation
Moquin, S. A., Thomas, S., Whalen, S., Warburton, A., Fernandez, S. G., McBride, A. A., Pollard, K. S., & Miranda, J. L. (2017) · Journal of Virology · doi:10.1128/jvi.01413-17 · Cited by 65 · see citing works
Schoenfelder, S., Mifsud, B., Senner, C. E., Todd, C. D., Chrysanthou, S., Darbo, E., Hemberger, M., & Branco, M. R. (2018) · Nature Communications · doi:10.1038/s41467-018-06666-4 · Cited by 54 · see citing works
Self-citationChromatin architecture reorganization during neuronal cell differentiation in Drosophila genomePreprint
Chathoth, K. T., & Zabet, N. R. (2019) · Genome Research · doi:10.1101/gr.246710.118 · Cited by 54 · see citing works
Three-dimensional organization and dynamics of the genome
Szałaj, P., & Plewczyński, D. (2018) · Cell Biology and Toxicology · doi:10.1007/s10565-018-9428-y · Cited by 54 · see citing works
NF-kappaB-dependent lymphoid enhancer co-option promotes renal carcinoma metastasis
Rodrigues, P., Patel, S. A., Harewood, L., Olan, I., Vojtasova, E., Syafruddin, S. E., Zaini, M. N., Richardson, E., Burge, J., Warren, A., et al. (2018) · Cancer Discovery · doi:10.1158/2159-8290.cd-17-1211 · Cited by 45 · see citing works
Global in situ profiling of RNA-RNA spatial interactions with RIC-seq
Cao, C., Cai, Z., Ye, R., Su, R., Hu, N., Zhao, H., & Xue, Y. (2021) · Nature Protocols · doi:10.1038/s41596-021-00524-2 · Cited by 51 · see citing works
Multiscale 3D genome reorganization during skeletal muscle stem cell lineage progression and aging
Zhao, Y. F., Ding, Y., He, L., Zhou, Q., Chen, X., Li, Y., Alfonsi, M. V., Wu, Z., Sun, H., & Wang, H. (2023) · Science Advances · doi:10.1126/sciadv.abo1360 · Cited by 49 · see citing works
PAR-TERRA directs homologous sex chromosome pairing
Chu, H.-P. C., Froberg, J. E., Kesner, B., Oh, H. J., Ji, F., Sadreyev, R. I., Pinter, S. F., & Lee, J. T. (2017) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.3432 · Cited by 51 · see citing works
Genome-Wide Analysis of the Arabidopsis Replication Timing Program
Concia, L., Brooks, A. M., Wheeler, E., Zynda, G. J., Wear, E. E., LeBlanc, C., Song, J., Lee, T.-J., Pascuzzi, P. E., Martienssen, R. A., et al. (2018) · PLANT PHYSIOLOGY · doi:10.1104/pp.17.01537 · Cited by 49 · see citing works
CTCF maintains regulatory homeostasis of cancer pathways
Aitken, S. J., Ibarra-Soria, X., Kentepozidou, E., Flicek, P., Feig, C., Marioni, J. C., & Odom, D. T. (2018) · Genome biology · doi:10.1186/s13059-018-1484-3 · Cited by 47 · see citing works
The macro and micro of chromosome conformation capture
Goel, V. Y., & Hansen, A. S. (2020) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.395 · Cited by 46 · see citing works
Zhang, N., Mendieta-Esteban, J., Magli, A., Lilja, K. C., Perlingeiro, R., Martí-Renom, M., Tsirigos, A., & Dynlacht, B. (2020) · Nature Communications · doi:10.1038/s41467-020-19999-w · Cited by 38 · see citing works
Chromatin interactome mapping at 139 independent breast cancer risk signals
Beesley, J., Sivakumaran, H., Marjaneh, M. M., Lima, L. G., Hillman, K. M., Kaufmann, S., Tuano, N., Hussein, N., Ham, S., Mukhopadhyay, P., et al. (2020) · Genome biology · doi:10.1186/s13059-019-1877-y · Cited by 43 · see citing works
Sim3C: simulation of Hi-C and Meta3C proximity ligation sequencing technologies
DeMaere, M. Z., & Darling, A. E. (2017) · GigaScience · doi:10.1093/gigascience/gix103 · Cited by 41 · see citing works
Analysis of the structural variability of topologically associated domains as revealed by Hi-C
Sauerwald, N., Singhal, A., & Kingsford, C. (2019) · NAR Genomics and Bioinformatics · doi:10.1093/nargab/lqz008 · Cited by 40 · see citing works
Downes, D. J., Beagrie, R. A., Gosden, M. E., Telenius, J. M., Carpenter, S. J., Nußbaum, L., Ornellas, S. D., Sergeant, M. J., Eijsbouts, C. Q., Schweßinger, R., et al. (2021) · Nature Communications · doi:10.1038/s41467-020-20809-6 · Cited by 43 · see citing works
QuASAR: Quality Assessment of Spatial Arrangement Reproducibility in Hi-C DataPreprint
Sauria, M. E. G., & Taylor, J. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/204438 · Cited by 40 · see citing works
MDM2 facilitates adipocyte differentiation through CRTC-mediated activation of STAT3
Hallenborg, P., Siersbæk, M. S., Barrio‐Hernandez, I., Nielsen, R., Kristiansen, K., Mandrup, S., Grøntved, L., & Blagoev, B. (2016) · Cell Death and Disease · doi:10.1038/cddis.2016.188 · Cited by 38 · see citing works
Groves, I. J., Drane, E., Michalski, M., Monahan, J., Scarpini, C. G., Smith, S. P., Bussotti, G., Várnai, C., Schoenfelder, S., Fraser, P., et al. (2021) · PLoS Pathogens · doi:10.1371/journal.ppat.1009875 · Cited by 37 · see citing works
Self-citationmiRNA-independent function of long noncoding pri-miRNA loci
He, D. X., Wu, D., Müller, S., Wang, L., Saha, P., Ahanger, S. H., Liu, S. J., Cui, M., Hong, S. J., Jain, M., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2017562118 · Cited by 34 · see citing works
Practical Analysis of Hi-C Data: Generating A/B Compartment Profiles.
Miura, H., Poonperm, R., Takahashi, S., & Hiratani, I. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-8766-5_16 · Cited by 31 · see citing works
Iteratively improving Hi-C experiments one step at a time
Golloshi, R., Sanders, J. T., & McCord, R. P. (2018) · Methods · doi:10.1016/j.ymeth.2018.04.033 · Cited by 28 · see citing works
Niu, L., Shen, W., Huang, Y., He, N., Zhang, Y., Sun, J., Wan, J., Jiang, D., Yang, M., Tse, Y. C., et al. (2019) · Communications Biology · doi:10.1038/s42003-019-0519-y · Cited by 30 · see citing works
Johanson, T. M., Coughlan, H. D., Lun, A. T. L., Bediaga, N. G., Naselli, G., Garnham, A. L., Harrison, L. C., Smyth, G. K., & Allan, R. S. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007431 · Cited by 29 · see citing works
Ultraconserved Elements Occupy Specific Arenas of Three-Dimensional Mammalian Genome Organization
McCole, R. B., Erceg, J., Saylor, W., & Wu, C.-T. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.06.031 · Cited by 29 · see citing works
Identification of physical interactions between genomic regions by enCh IP ‐Seq
Fujita, T., Yuno, M., Suzuki, Y., Sugano, S., & Fujii, H. (2017) · Genes to Cells · doi:10.1111/gtc.12492 · Cited by 28 · see citing works
Sanders, J. T., Golloshi, R., Das, P., Xu, Y., Terry, P. H., Nash, D. G., Dekker, J., & McCord, R. P. (2022) · Scientific Reports · doi:10.1038/s41598-022-08602-5 · Cited by 26 · see citing works
Measuring the reproducibility and quality of Hi-C dataPreprint
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. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/188755 · Cited by 28 · see citing works
C-TALE, a new cost-effective method for targeted enrichment of Hi-C/3C-seq libraries
Golov, A. K., Ulianov, S. V., Luzhin, A. V., Kalabusheva, E. P., Kantidze, O. L., Flyamer, I. M., Razin, S. V., & Gavrilov, A. A. (2019) · Methods · doi:10.1016/j.ymeth.2019.06.022 · Cited by 27 · see citing works
Liu, C. (2017) · Methods in molecular biology · doi:10.1007/978-1-4939-7125-1_11 · Cited by 25 · see citing works
Garske, K. M., Pan, D. Z., Miao, Z., Bhagat, Y. V., Comenho, C., Robles, C. R., Benhammou, J. N., Alvarez, M., Ko, A., Ye, C., et al. (2019) · Nature Metabolism · doi:10.1038/s42255-019-0071-6 · Cited by 22 · see citing works
Rodríguez, S., Scadden, A. W., Reckard, A. T., Shtanko, Y., Hull-Crew, C., & Klocko, A. D. (2022) · G3 Genes Genomes Genetics · doi:10.1093/g3journal/jkac053 · Cited by 16 · see citing works
Huang, H., Liu, J., Li, M., Guo, H., Zhu, J., Zhu, L., Wu, S., Mo, K., Huang, Y., Tan, J., et al. (2022) · Science Advances · doi:10.1126/sciadv.abo5668 · Cited by 17 · see citing works
Capturing Three-Dimensional Genome Organization in Individual Cells by Single-Cell Hi-C
Nagano, T., Wingett, S., & Fraser, P. (2017) · Methods in molecular biology · doi:10.1007/978-1-4939-7231-9_6 · Cited by 17 · see citing works
Self-citationInter-chromosomal contacts demarcate genome topology along a spatial gradient
Mokhtaridoost, M., Chalmers, J. J., Soleimanpoor, M., McMurray, B. J., Lato, D. F., Nguyen, S. C., Musienko, V., Nash, J. O., Espeso‐Gil, S., Ahmed, S., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-53983-y · Cited by 17 · see citing works
BAT Hi-C maps global chromatin interactions in an efficient and economical way.
Huang, J., Jiang, Y.-P., Zheng, H., & Ji, X. (2019) · Methods · doi:10.1016/j.ymeth.2019.08.004 · Cited by 15 · see citing works
Chandradoss, K. R., Guthikonda, P. K., Kethavath, S., Dass, M., Singh, H., Nayak, R., Kurukuti, S., & Sandhu, K. S. (2020) · BMC Genomics · doi:10.1186/s12864-020-6580-6 · Cited by 16 · see citing works
Xiao, Y., Jiao, S., He, M., Lin, D., Zuo, H., Han, J., Sun, Y., Cao, G., Chen, Z., & Liu, H. (2022) · International Journal of Oral Science · doi:10.1038/s41368-022-00194-0 · Cited by 15 · see citing works
Liu, X., Sun, Q., Wang, Q., Hu, C., Chen, X., Li, H., Czajkowsky, D. M., & Shao, Z. (2021) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2020.06.017 · Cited by 16 · see citing works
Cell type-specific interchromosomal interactions as a mechanism for transcriptional diversityPreprint
Horta, A., Monahan, K., Bashkirova, E., & Lomvardas, S. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/287532 · Cited by 14 · see citing works
Chromatin‐Associated RNA Sequencing (ChAR‐seq)
Jukam, D., Limouse, C., Smith, O. K., Risca, V. I., Bell, J. C., & Straight, A. F. (2019) · Current Protocols in Molecular Biology · doi:10.1002/cpmb.87 · Cited by 13 · see citing works
Technologies to study spatial genome organization: beyond 3C
Übelmesser, N., & Papantonis, A. (2019) · Briefings in Functional Genomics · doi:10.1093/bfgp/elz019 · Cited by 13 · see citing works
Golov, A. K., Abashkin, D. A., Kondratyev, N. V., Razin, S. V., Gavrilov, A. A., & Голимбет, В. Е. (2020) · Scientific Reports · doi:10.1038/s41598-020-72496-4 · Cited by 13 · see citing works
- Authors
- Nagano, T., Várnai, C., Schoenfelder, S., Javierre, B.-M., Wingett, S. W., & Fraser, P.
- Affiliations
- Babraham Institute (GB)
- Corresponding author
- Nagano, Takashi
- Fraser, Peter
- ORCID
- Venue
- Genome Biology
- Published
- 2015-08-26
- Volume
- 16
- Issue
- 1
- Pages
- 175-175
- ISSN
- 1465-6906 (ISSN-L)
- 1474-760X
- PMC
- PMC4580221
- OpenAlex
- W2116261028
- Cited by
- 166
- References
- 26
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 8 · 2023: 8 · 2022: 11 · 2021: 20 · 2020: 17 · 2019: 23 · 2018: 25 · 2017: 27 · 2016: 12 · 2015: 5
- FWCI
- 9.99
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Genome biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion, cc-by)
- Apollo (University of Cambridge) (submittedVersion, cc-by)
- Apollo (cc-by)
- Funders
- European Research Council (111608)
- BBSRC (BBS/E/B/000C0405)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genomic variations and chromosomal abnormalities
- Keywords
- Hi-C, chromosome conformation capture, 3D genome organization, topologically associating domains, single-cell Hi-C
- MeSH terms
- Animals, Cell Nucleus, Cells, Cultured, Chromatin, Humans, Mice, Inbred C57BL, Genomics, Mice
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