Understanding 3D genome organization by multidisciplinary methods.
Journal
Nature reviews. Molecular cell biology
ISSN: 1471-0080
Titre abrégé: Nat Rev Mol Cell Biol
Pays: England
ID NLM: 100962782
Informations de publication
Date de publication:
08 2021
08 2021
Historique:
accepted:
16
03
2021
pubmed:
7
5
2021
medline:
29
9
2021
entrez:
6
5
2021
Statut:
ppublish
Résumé
Understanding how chromatin is folded in the nucleus is fundamental to understanding its function. Although 3D genome organization has been historically difficult to study owing to a lack of relevant methodologies, major technological breakthroughs in genome-wide mapping of chromatin contacts and advances in imaging technologies in the twenty-first century considerably improved our understanding of chromosome conformation and nuclear architecture. In this Review, we discuss methods of 3D genome organization analysis, including sequencing-based techniques, such as Hi-C and its derivatives, Micro-C, DamID and others; microscopy-based techniques, such as super-resolution imaging coupled with fluorescence in situ hybridization (FISH), multiplex FISH, in situ genome sequencing and live microscopy methods; and computational and modelling approaches. We describe the most commonly used techniques and their contribution to our current knowledge of nuclear architecture and, finally, we provide a perspective on up-and-coming methods that open possibilities for future major discoveries.
Identifiants
pubmed: 33953379
doi: 10.1038/s41580-021-00362-w
pii: 10.1038/s41580-021-00362-w
doi:
Substances chimiques
Chromatin
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
511-528Informations de copyright
© 2021. Springer Nature Limited.
Références
Flemming, W. Zellsubstanz, Kern und Zelltheilung (F. C. W. Vogel, 1882).
Heitz, E. Das heterochromatin der moose. Jahrbücher Wissenschaftliche Bot. 69, 762–818 (1928).
Boveri, T. Die Blastomerenkerne von Ascaris megalocephala und die Theorie der Chromosomenindividualität (Engelmann, 1909).
Cremer, T. et al. Analysis of chromosome positions in the interphase nucleus of Chinese hamster cells by laser-UV-microirradiation experiments. Hum. Genet. 62, 201–209 (1982).
pubmed: 7169211
doi: 10.1007/BF00333519
Manuelidis, L. Individual interphase chromosome domains revealed by in situ hybridization. Hum. Genet. 71, 288–293 (1985).
pubmed: 3908288
doi: 10.1007/BF00388453
Schardin, M., Cremer, T., Hager, H. D. & Lang, M. Specific staining of human chromosomes in Chinese hamster × man hybrid cell lines demonstrates interphase chromosome territories. Hum. Genet. 71, 281–287 (1985).
pubmed: 2416668
doi: 10.1007/BF00388452
Cremer, M. et al. Multicolor 3D fluorescence in situ hybridization for imaging interphase chromosomes. Methods Mol. Biol. 463, 205–239 (2012).
doi: 10.1007/978-1-59745-406-3_15
Branco, M. R. & Pombo, A. Intermingling of chromosome territories in interphase suggests role in translocations and transcription-dependent associations. PLoS Biol. 4, e138 (2006).
pubmed: 16623600
pmcid: 1440941
doi: 10.1371/journal.pbio.0040138
Chambeyron, S. & Bickmore, W. A. Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription. Genes Dev. 18, 1119–1130 (2004).
pubmed: 15155579
pmcid: 415637
doi: 10.1101/gad.292104
Ferrai, C. et al. Poised transcription factories prime silent uPA gene prior to activation. PLoS Biol. 8, e1000270 (2010).
pubmed: 20052287
pmcid: 2797137
doi: 10.1371/journal.pbio.1000270
Rosin, L. F., Nguyen, S. C. & Joyce, E. F. Condensin II drives large-scale folding and spatial partitioning of interphase chromosomes in Drosophila nuclei. PLOS Genet. 14, e1007393 (2018).
pubmed: 30001329
pmcid: 6042687
doi: 10.1371/journal.pgen.1007393
Su, J. H., Zheng, P., Kinrot, S. S., Bintu, B. & Zhuang, X. Genome-scale imaging of the 3D organization and transcriptional activity of chromatin. Cell 182, 1641–1659 (2020).
pubmed: 32822575
doi: 10.1016/j.cell.2020.07.032
pmcid: 7851072
Fritz, A. J., Sehgal, N., Pliss, A., Xu, J. & Berezney, R. Chromosome territories and the global regulation of the genome. Genes Chromosom. Cancer 58, 407–426 (2019).
pubmed: 30664301
doi: 10.1002/gcc.22732
Nguyen, H. Q. et al. 3D mapping and accelerated super-resolution imaging of the human genome using in situ sequencing. Nat. Methods 17, 822–832 (2020). This article is the first mention of OligoFISSEQ, showcasing its multiplexing possibilities by imaging 249 loci simultaneously.
pubmed: 32719531
pmcid: 7537785
doi: 10.1038/s41592-020-0890-0
Takei, Y. et al. Integrated spatial genomics reveals global architecture of single nuclei. Nature 590, 344–350 (2021).
pubmed: 33505024
doi: 10.1038/s41586-020-03126-2
pmcid: 7878433
Payne, A. C. et al. In situ genome sequencing resolves DNA sequence and structure in intact biological samples. Science 371, eaay3446 (2020).
pubmed: 33384301
doi: 10.1126/science.aay3446
pmcid: 7962746
Cullen, K. E., Kladde, M. P. & Seyfred, M. A. Interaction between transcription regulatory regions of prolactin chromatin. Science 261, 203–206 (1993).
pubmed: 8327891
doi: 10.1126/science.8327891
Dekker, J., Rippe, K., Dekker, M. & Kleckner, N. Capturing chromosome conformation. Science 295, 1306–1311 (2002).
pubmed: 11847345
doi: 10.1126/science.1067799
Simonis, M. et al. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat. Genet. 38, 1348–1354 (2006).
pubmed: 17033623
doi: 10.1038/ng1896
Dostie, J. et al. Chromosome conformation capture carbon copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res. 16, 1299–1309 (2006).
pubmed: 16954542
pmcid: 1581439
doi: 10.1101/gr.5571506
Schoenfelder, S. et al. The pluripotent regulatory circuitry connecting promoters to their long-range interacting elements. Genome Res. 25, 582–597 (2015).
pubmed: 25752748
pmcid: 4381529
doi: 10.1101/gr.185272.114
Schoenfelder, S. et al. Polycomb repressive complex PRC1 spatially constrains the mouse embryonic stem cell genome. Nat. Genet. 47, 1179–1186 (2015).
pubmed: 26323060
pmcid: 4847639
doi: 10.1038/ng.3393
Mifsud, B. et al. Mapping long-range promoter contacts in human cells with high-resolution capture Hi-C. Nat. Genet. 47, 598–606 (2015).
pubmed: 25938943
doi: 10.1038/ng.3286
Hughes, J. R. et al. Analysis of hundreds of cis-regulatory landscapes at high resolution in a single, high-throughput experiment. Nat. Genet. 46, 205–212 (2014).
pubmed: 24413732
doi: 10.1038/ng.2871
Davies, J. O. J. et al. Multiplexed analysis of chromosome conformation at vastly improved sensitivity. Nat. Methods 13, 74–80 (2015).
pubmed: 26595209
pmcid: 4724891
doi: 10.1038/nmeth.3664
Jäger, R. et al. Capture Hi-C identifies the chromatin interactome of colorectal cancer risk loci. Nat. Commun. 6, 6178 (2015).
pubmed: 25695508
doi: 10.1038/ncomms7178
Lieberman-Aiden, E. et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289–293 (2009).
pubmed: 19815776
pmcid: 2858594
doi: 10.1126/science.1181369
Duan, Z. et al. A three-dimensional model of the yeast genome. Nature 465, 363–367 (2010).
pubmed: 20436457
pmcid: 2874121
doi: 10.1038/nature08973
Sati, S. & Cavalli, G. Chromosome conformation capture technologies and their impact in understanding genome function. Chromosoma 126, 33–44 (2017).
pubmed: 27130552
doi: 10.1007/s00412-016-0593-6
Horike, S. I., Cai, S., Miyano, M., Cheng, J. F. & Kohwi-Shigematsu, T. Loss of silent-chromatin looping and impaired imprinting of DLX5 in Rett syndrome. Nat. Genet. 37, 31–40 (2005).
pubmed: 15608638
doi: 10.1038/ng1491
Fullwood, M. J., Wei, C. L., Liu, E. T. & Ruan, Y. Next-generation DNA sequencing of paired-end tags (PET) for transcriptome and genome analyses. Genome Res. 19, 521–532 (2009).
pubmed: 19339662
pmcid: 3807531
doi: 10.1101/gr.074906.107
Mumbach, M. R. et al. HiChIP: efficient and sensitive analysis of protein-directed genome architecture. Nat. Methods 13, 919–922 (2016).
pubmed: 27643841
pmcid: 5501173
doi: 10.1038/nmeth.3999
Fang, R. et al. Mapping of long-range chromatin interactions by proximity ligation-assisted ChIP–seq. Cell Res 26, 1345–1348 (2016).
pubmed: 27886167
pmcid: 5143423
doi: 10.1038/cr.2016.137
Chen, Y. et al. Mapping 3D genome organization relative to nuclear compartments using TSA-seq as a cytological ruler. J. Cell Biol. 217, 4025–4048 (2018). This article introduces TSA-seq, a cytological ruler for nuclear speckles and lamina, which is the first genomics method enabling transforming sequencing reads into physical distances in the nucleus.
pubmed: 30154186
pmcid: 6219710
doi: 10.1083/jcb.201807108
Quinodoz, S. A. et al. Higher-order inter-chromosomal hubs shape 3D genome organization in the nucleus. Cell 174, 744–757 (2018).
pubmed: 29887377
pmcid: 6548320
doi: 10.1016/j.cell.2018.05.024
Arrastia, M. V. et al. A single-cell method to map higher-order 3D genome organization in thousands of individual cells reveals structural heterogeneity in mouse ES cells. Preprint at bioRxiv https://doi.org/10.1101/2020.08.11.242081 (2020).
doi: 10.1101/2020.08.11.242081
Quinodoz, S. A. et al. RNA promotes the formation of spatial compartments in the nucleus. Preprint at bioRxiv https://doi.org/10.1101/2020.08.25.267435 (2020).
doi: 10.1101/2020.08.25.267435
Van Steensel, B. & Henikoff, S. Identification of in vivo DNA targets of chromatin proteins using tethered Dam methyltransferase. Nat. Biotechnol. 14, 424–428 (2000). This article introduces DamID, which is used for spatial positioning of heterochromatin protein 1 on chromatin in vitro and in vivo in D. melanogaster.
doi: 10.1038/74487
Vogel, M. J., Peric-Hupkes, D. & van Steensel, B. Detection of in vivo protein–DNA interactions using DamID in mammalian cells. Nat. Protoc. 2, 1467–1478 (2007).
pubmed: 17545983
doi: 10.1038/nprot.2007.148
Guelen, L. et al. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453, 948–951 (2008).
pubmed: 18463634
doi: 10.1038/nature06947
Beagrie, R. A. et al. Complex multi-enhancer contacts captured by genome architecture mapping. Nature 543, 519–524 (2017). This article introduces the GAM method and the discovery of a richness of multiway contacts in the nucleus.
pubmed: 28273065
pmcid: 5366070
doi: 10.1038/nature21411
Zhang, L. et al. TSA-seq reveals a largely conserved genome organization relative to nuclear speckles with small position changes tightly correlated with gene expression changes. Genome Res. 31, 251–264 (2021).
doi: 10.1101/gr.266239.120
pmcid: 7849416
Szabo, Q. et al. TADs are 3D structural units of higher-order chromosome organization in Drosophila. Sci. Adv. 4, eaar8082 (2018).
pubmed: 29503869
pmcid: 5829972
doi: 10.1126/sciadv.aar8082
Bintu, B. et al. Super-resolution chromatin tracing reveals domains and cooperative interactions in single cells. Science 362, eaau1783 (2018). This study uses high-throughput oligopaint technology to study chromatin dynamics and shows that TADs are highly stochastic in single cells, but predictable at the population level.
pubmed: 30361340
pmcid: 6535145
doi: 10.1126/science.aau1783
Cardozo Gizzi, A. M. et al. Microscopy-based chromosome conformation capture enables simultaneous visualization of genome organization and transcription in intact organisms. Mol. Cell 74, 212–222.e5 (2019). This article presents highly multiplexed sequential oligopaint FISH (RNA and DNA) based on the conjunction of microscopy and microfluidics in D. melanogaster embryos.
pubmed: 30795893
doi: 10.1016/j.molcel.2019.01.011
Nir, G. et al. Walking along chromosomes with super-resolution imaging, contact maps, and integrative modeling. PLoS Genet. 14, e1007872 (2018).
pubmed: 30586358
pmcid: 6324821
doi: 10.1371/journal.pgen.1007872
Mateo, L. J. et al. Visualizing DNA folding and RNA in embryos at single-cell resolution. Nature 568, 49–54 (2019).
pubmed: 30886393
pmcid: 6556380
doi: 10.1038/s41586-019-1035-4
Sawh, A. N. et al. Lamina-dependent stretching and unconventional chromosome compartments in early C. elegans embryos. Mol. Cell 78, 96–111 (2020).
pubmed: 32105612
pmcid: 7263362
doi: 10.1016/j.molcel.2020.02.006
Gu, B. et al. Transcription-coupled changes in nuclear mobility of mammalian cis-regulatory elements. Science 359, 1050–1055 (2018).
pubmed: 29371426
pmcid: 6590518
doi: 10.1126/science.aao3136
Shaban, H. A. & Seeber, A. Monitoring the spatio-temporal organization and dynamics of the genome. Nucleic Acids Res. 48, 3423–3434 (2020).
pubmed: 32123910
pmcid: 7144944
doi: 10.1093/nar/gkaa135
Barth, R., Bystricky, K. & Shaban, H. A. Coupling chromatin structure and dynamics by live super-resolution imaging. Sci. Adv. 6, eaaz2196 (2020).
pubmed: 32937447
pmcid: 7458449
doi: 10.1126/sciadv.aaz2196
Vangala, P. et al. High-resolution mapping of multiway enhancer–promoter interactions regulating pathogen detection. Mol. Cell 80, 359–373 (2020).
pubmed: 32991830
doi: 10.1016/j.molcel.2020.09.005
pmcid: 7572724
Nora, E. P. et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485, 381–385 (2012).
pubmed: 22495304
pmcid: 3555144
doi: 10.1038/nature11049
Sexton, T. et al. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148, 458–472 (2012).
pubmed: 22265598
doi: 10.1016/j.cell.2012.01.010
Dixon, J. R. et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376–380 (2012).
pubmed: 22495300
pmcid: 3356448
doi: 10.1038/nature11082
Kalhor, R. et al. Developmental barcoding of whole mouse via homing CRISPR. Science 361, eaat9804 (2018).
pubmed: 30093604
pmcid: 6139672
doi: 10.1126/science.aat9804
Szabo, Q. et al. Regulation of single-cell genome organization into TADs and chromatin nanodomains. Nat. Genet. 52, 1151–1157 (2020). This article is the first description of chromatin nanodomains in mammals using oligopaints in conjunction with SIM.
pubmed: 33077913
pmcid: 7610512
doi: 10.1038/s41588-020-00716-8
Fudenberg, G. et al. Formation of chromosomal domains by loop extrusion. Cell Rep. 15, 2038–2049 (2016).
pubmed: 27210764
pmcid: 4889513
doi: 10.1016/j.celrep.2016.04.085
Wutz, G. et al. Topologically associating domains and chromatin loops depend on cohesin and are regulated by CTCF, WAPL, and PDS5 proteins. EMBO J. 36, 3573–3599 (2017).
pubmed: 29217591
pmcid: 5730888
doi: 10.15252/embj.201798004
Rao, S. S. P. et al. Cohesin loss eliminates all loop domains. Cell 171, 305–320 (2017).
pubmed: 28985562
pmcid: 5846482
doi: 10.1016/j.cell.2017.09.026
Schwarzer, W. et al. Two independent modes of chromatin organization revealed by cohesin removal. Nature 551, 51–56 (2017).
pubmed: 29094699
pmcid: 5687303
doi: 10.1038/nature24281
Guo, Y. et al. CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function. Cell 162, 900–910 (2015).
pubmed: 26276636
pmcid: 4642453
doi: 10.1016/j.cell.2015.07.038
Haarhuis, J. H. I. et al. The cohesin release factor WAPL restricts chromatin loop extension. Cell 169, 693–707 (2017).
pubmed: 28475897
pmcid: 5422210
doi: 10.1016/j.cell.2017.04.013
Nora, E. P. et al. Targeted degradation of CTCF decouples local insulation of chromosome domains from genomic compartmentalization. Cell 169, 930–944 (2017).
pubmed: 28525758
pmcid: 5538188
doi: 10.1016/j.cell.2017.05.004
Bonev, B. et al. Multiscale 3D genome rewiring during mouse article multiscale 3D genome rewiring during mouse neural development. Cell 171, 557–572 (2017).
pubmed: 29053968
pmcid: 5651218
doi: 10.1016/j.cell.2017.09.043
Ulianov, S. V. et al. Active chromatin and transcription play a key role in chromosome partitioning into topologically associating domains. Genome Res. 26, 70–84 (2016).
pubmed: 26518482
pmcid: 4691752
doi: 10.1101/gr.196006.115
Sanborn, A. L. et al. Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. Proc. Natl Acad. Sci. USA 112, 6456–6465 (2015).
doi: 10.1073/pnas.1518552112
Nuebler, J., Fudenberg, G., Imakaev, M., Abdennur, N. & Mirny, L. A. Chromatin organization by an interplay of loop extrusion and compartmental segregation. Proc. Natl Acad. Sci. USA 115, 6697–6706 (2018).
doi: 10.1073/pnas.1717730115
Rowley, M. J. et al. Evolutionarily conserved principles predict 3D chromatin organization. Mol. Cell 67, 837–852 (2017).
pubmed: 28826674
pmcid: 5591081
doi: 10.1016/j.molcel.2017.07.022
Benedetti, F., Racko, D., Dorier, J., Burnier, Y. & Stasiak, A. Transcription-induced supercoiling explains formation of self-interacting chromatin domains in S. pombe. Nucleic Acids Res. 45, 9850–9859 (2017).
pubmed: 28973473
pmcid: 5622301
doi: 10.1093/nar/gkx716
Szabo, Q., Bantignies, F. & Cavalli, G. Principles of genome folding into topologically associating domains. Sci. Adv. 5, eaaw1668 (2019).
pubmed: 30989119
pmcid: 6457944
doi: 10.1126/sciadv.aaw1668
Jerković, I., Szabo, Q., Bantignies, F. & Cavalli, G. Higher-order chromosomal structures mediate genome function. J. Mol. Biol. 432, 676–681 (2020).
pubmed: 31689436
doi: 10.1016/j.jmb.2019.10.014
Oomen, M. E., Hedger, A. K., Watts, J. K. & Dekker, J. Detecting chromatin interactions between and along sister chromatids with SisterC. Nat. Methods 17, 1002–1009 (2020).
pubmed: 32968250
pmcid: 7541687
doi: 10.1038/s41592-020-0930-9
Mitter, M. et al. Conformation of sister chromatids in the replicated human genome. Nature 586, 139–144 (2020).
pubmed: 32968280
pmcid: 7116725
doi: 10.1038/s41586-020-2744-4
AlHaj Abed, J. et al. Highly structured homolog pairing reflects functional organization of the Drosophila genome. Nat. Commun. 10, 1–14 (2019).
doi: 10.1038/s41467-019-12208-3
Franke, M. et al. Formation of new chromatin domains determines pathogenicity of genomic duplications. Nature 538, 265–269 (2016).
pubmed: 27706140
doi: 10.1038/nature19800
Lupiáñez, D. G., Spielmann, M. & Mundlos, S. Breaking TADs: how alterations of chromatin domains result in disease. Trends Genet. 32, 225–237 (2016).
pubmed: 26862051
doi: 10.1016/j.tig.2016.01.003
Despang, A. et al. Functional dissection of the Sox9–Kcnj2 locus identifies nonessential and instructive roles of TAD architecture. Nat. Genet. 51, 1263–1271 (2019).
pubmed: 31358994
doi: 10.1038/s41588-019-0466-z
Andrey, G. & Mundlos, S. The three-dimensional genome: regulating gene expression during pluripotency and development. Development 144, 3646–3658 (2017).
pubmed: 29042476
doi: 10.1242/dev.148304
Weischenfeldt, J. et al. Pan-cancer analysis of somatic copy-number alterations implicates IRS4 and IGF2 in enhancer hijacking. Nat. Genet. 49, 65–74 (2016).
pubmed: 27869826
pmcid: 5791882
doi: 10.1038/ng.3722
Liu, X. S. et al. Rescue of fragile X syndrome neurons by DNA methylation editing of the FMR1 gene. Cell 172, 979–992 (2018).
pubmed: 29456084
pmcid: 6375087
doi: 10.1016/j.cell.2018.01.012
Bruneau, B. G. & Nora, E. P. Chromatin domains go on repeat in disease. Cell 175, 38–40 (2018).
pubmed: 30241613
doi: 10.1016/j.cell.2018.08.068
Akdemir, K. C. et al. Somatic mutation distributions in cancer genomes vary with three-dimensional chromatin structure. Nat. Genet. 52, 1178–1188 (2020).
pubmed: 33020667
doi: 10.1038/s41588-020-0708-0
pmcid: 8350746
Valton, A. L. & Dekker, J. TAD disruption as oncogenic driver. Curr. Opin. Genet. Dev. 36, 34–40 (2016).
pubmed: 27111891
pmcid: 4880504
doi: 10.1016/j.gde.2016.03.008
Rao, S. S. P. et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665–1680 (2014). This paper showcases the first use of the in situ Hi-C protocol and introduces HICCUPS, a contact caller dedicated to chromatin loops.
pubmed: 25497547
pmcid: 5635824
doi: 10.1016/j.cell.2014.11.021
Nagano, T. et al. Comparison of Hi-C results using in-solution versus in-nucleus ligation. Genome Biol. 16, 175 (2015).
pubmed: 26306623
pmcid: 4580221
doi: 10.1186/s13059-015-0753-7
Nagano, T. et al. Single-cell Hi-C reveals cell-to-cell variability in chromosome structure. Nature 502, 59–64 (2013).
pubmed: 24067610
doi: 10.1038/nature12593
Ma, W. et al. Fine-scale chromatin interaction maps reveal the cis-regulatory landscape of human lincRNA genes. Nat. Methods 12, 71–78 (2014).
pubmed: 25437436
pmcid: 4281301
doi: 10.1038/nmeth.3205
Ramani, V. et al. Mapping 3D genome architecture through in situ DNase Hi-C. Nat. Protoc. 11, 2104–2121 (2016).
pubmed: 27685100
pmcid: 5547819
doi: 10.1038/nprot.2016.126
Deng, X. et al. Bipartite structure of the inactive mouse X chromosome. Genome Biol. 16, 152 (2015).
pubmed: 26248554
pmcid: 4539712
doi: 10.1186/s13059-015-0728-8
Hsieh, T. H. S. et al. Mapping nucleosome resolution chromosome folding in yeast by Micro-C. Cell 162, 108–119 (2015).
pubmed: 26119342
pmcid: 4509605
doi: 10.1016/j.cell.2015.05.048
Hsieh, T.-H. S. et al. Resolving the 3D landscape of transcription-linked mammalian chromatin folding. Mol. Cell 78, 539–553 (2020). This article presents high-resolution Micro-C performed in mouse embryonic stem cells with concomitant analysis of nucleosome positioning.
pubmed: 32213323
pmcid: 7703524
doi: 10.1016/j.molcel.2020.03.002
Krietenstein, N. et al. Ultrastructural details of mammalian chromosome architecture. Mol. Cell 78, 554–565 (2020). This article presents high-resolution Micro-C performed in human embryonic stem cells and fibroblasts with concomitant analysis of nucleosome positioning.
pubmed: 32213324
pmcid: 7222625
doi: 10.1016/j.molcel.2020.03.003
Goel, V. Y. & Hansen, A. S. The macro and micro of chromosome conformation capture. WIREs Dev. Biol. https://doi.org/10.1002/wdev.395 (2020).
doi: 10.1002/wdev.395
Akgol Oksuz, B. et al. Systematic evaluation of chromosome conformation capture assays. Preprint at bioRxiv https://doi.org/10.1101/2020.12.26.424448 (2020).
doi: 10.1101/2020.12.26.424448
Baranello, L., Kouzine, F., Sanford, S. & Levens, D. ChIP bias as a function of cross-linking time. Chromosom. Res. 24, 175–181 (2016).
doi: 10.1007/s10577-015-9509-1
Gavrilov, A., Razin, S. V. & Cavalli, G. In vivo formaldehyde cross-linking: it is time for black box analysis. Brief. Funct. Genomics 14, 163–165 (2015).
pubmed: 25241225
doi: 10.1093/bfgp/elu037
Kempfer, R. & Pombo, A. Methods for mapping 3D chromosome architecture. Nat. Rev. Genet. 21, 207–226 (2020).
pubmed: 31848476
doi: 10.1038/s41576-019-0195-2
Fullwood, M. J. & Ruan, Y. ChIP-based methods for the identification of long-range chromatin interactions. J. Cell. Biochem. 107, 30–39 (2009).
pubmed: 19247990
pmcid: 2748757
doi: 10.1002/jcb.22116
Kind, J. et al. Genome-wide maps of nuclear lamina interactions in single human cells. Cell 163, 134–147 (2015).
pubmed: 26365489
pmcid: 4583798
doi: 10.1016/j.cell.2015.08.040
Redolfi, J. et al. DamC reveals principles of chromatin folding in vivo without crosslinking and ligation. Nat. Struct. Mol. Biol. 26, 471–480 (2019).
pubmed: 31133702
pmcid: 6561777
doi: 10.1038/s41594-019-0231-0
Li, X. et al. Long-read ChIA-PET for base-pair-resolution mapping of haplotype-specific chromatin interactions. Nat. Protoc. 12, 899–915 (2017).
pubmed: 28358394
pmcid: 5537732
doi: 10.1038/nprot.2017.012
Andrey, G. et al. Characterization of hundreds of regulatory landscapes in developing limbs reveals two regimes of chromatin folding. Genome Res. 27, 223–233 (2017).
pubmed: 27923844
pmcid: 5287228
doi: 10.1101/gr.213066.116
Rooijers, K. et al. Simultaneous quantification of protein–DNA contacts and transcriptomes in single cells. Nat. Biotechnol. 37, 766–772 (2019).
pubmed: 31209373
pmcid: 6609448
doi: 10.1038/s41587-019-0150-y
Sahl, S. J., Hell, S. W. & Jakobs, S. Fluorescence nanoscopy in cell biology. Nat. Rev. Mol. Cell Biol. 18, 685–701 (2017).
pubmed: 28875992
doi: 10.1038/nrm.2017.71
Liu, Z., Lavis, L. D. & Betzig, E. Imaging live-cell dynamics and structure at the single-molecule level. Mol. Cell 58, 644–659 (2015).
pubmed: 26000849
doi: 10.1016/j.molcel.2015.02.033
Heintzmann, R. & Cremer, C. G. Laterally modulated excitation microscopy: improvement of resolution by using a diffraction grating. Proc. SPIE 3568, 185–196 (1999).
doi: 10.1117/12.336833
Gustafsson, M. G. L. Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J. Microsc. 198, 82–87 (2000).
pubmed: 10810003
doi: 10.1046/j.1365-2818.2000.00710.x
Gustafsson, M. G. L. et al. Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys. J. 94, 4957–4970 (2008).
pubmed: 18326650
pmcid: 2397368
doi: 10.1529/biophysj.107.120345
Schermelleh, L. et al. Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 320, 1332–1336 (2008).
pubmed: 18535242
pmcid: 2916659
doi: 10.1126/science.1156947
Miron, E. et al. Chromatin arranges in chains of mesoscale domains with nanoscale functional topography independent of cohesin. Sci. Adv. 6, eaba8811 (2020).
pubmed: 32967822
pmcid: 7531892
doi: 10.1126/sciadv.aba8811
Rust, M. J., Bates, M. & Zhuang, X. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 3, 793–795 (2006).
pubmed: 16896339
pmcid: 2700296
doi: 10.1038/nmeth929
Betzig, E. et al. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313, 1642–1645 (2006).
pubmed: 16902090
doi: 10.1126/science.1127344
Hess, S. T., Girirajan, T. P. K. & Mason, M. D. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys. J. 91, 4258–4272 (2006).
pubmed: 16980368
pmcid: 1635685
doi: 10.1529/biophysj.106.091116
Huang, B., Babcock, H. & Zhuang, X. Breaking the diffraction barrier: super-resolution imaging of cells. Cell 143, 1047–1058 (2010).
pubmed: 21168201
pmcid: 3272504
doi: 10.1016/j.cell.2010.12.002
Ricci, M. A., Manzo, C., Lakadamyali, M. & Cosma, M. P. Chromatin fibers are formed by heterogeneous groups of nucleosomes in vivo. Cell 160, 1145–1158 (2015).
pubmed: 25768910
doi: 10.1016/j.cell.2015.01.054
Nozaki, T. et al. Dynamic organization of chromatin domains revealed by super-resolution live-cell imaging. Mol. Cell 67, 282–293 (2017).
pubmed: 28712725
doi: 10.1016/j.molcel.2017.06.018
Hell, S. W. & Wichmann, J. Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt. Lett. 19, 780–782 (1994).
pubmed: 19844443
doi: 10.1364/OL.19.000780
Klar, T. A., Jakobs, S., Dyba, M., Egner, A. & Hell, S. W. Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission. Proc. Natl Acad. Sci. USA 97, 8206–8210 (2000).
pubmed: 10899992
pmcid: 26924
doi: 10.1073/pnas.97.15.8206
Hofmann, M., Eggeling, C., Jakobs, S. & Hell, S. W. Breaking the diffraction barrier in fluorescence microscopy at low light intensities by using reversibly photoswitchable proteins. Proc. Natl Acad. Sci. USA 102, 17565–17569 (2005).
pubmed: 16314572
pmcid: 1308899
doi: 10.1073/pnas.0506010102
Gwosch, C. K. et al. MINFLUX nanoscopy delivers multicolor nanometer 3D-resolution in (living) cells. Nat. Methods 17, 217–224 (2020).
pubmed: 31932776
doi: 10.1038/s41592-019-0688-0
Beliveau, B. J. et al. Versatile design and synthesis platform for visualizing genomes with Oligopaint FISH probes. Proc. Natl Acad. Sci. USA 109, 21301–21306 (2012).
pubmed: 23236188
pmcid: 3535588
doi: 10.1073/pnas.1213818110
Wang, S. et al. Spatial organization of chromatin domains and compartments in single chromosomes. Science 353, 598–602 (2016).
pubmed: 27445307
pmcid: 4991974
doi: 10.1126/science.aaf8084
Ou, H. D. et al. ChromEMT: visualizing 3D chromatin structure and compaction in interphase and mitotic cells. Science 357, eaag0025 (2017).
pubmed: 28751582
pmcid: 5646685
doi: 10.1126/science.aag0025
Yaffe, E. & Tanay, A. Probabilistic modeling of Hi-C contact maps eliminates systematic biases to characterize global chromosomal architecture. Nat. Genet. 43, 1059–1065 (2011).
pubmed: 22001755
doi: 10.1038/ng.947
Imakaev, M. et al. Iterative correction of Hi-C data reveals hallmarks of chromosome organization. Nat. Methods 9, 999–1003 (2012).
pubmed: 22941365
pmcid: 3816492
doi: 10.1038/nmeth.2148
Ryba, T. et al. Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. Genome Res. 20, 761–770 (2010).
pubmed: 20430782
pmcid: 2877573
doi: 10.1101/gr.099655.109
Di Pierro, M., Cheng, R. R., Aiden, E. L., Wolynes, P. G. & Onuchic, J. N. De novo prediction of human chromosome structures: epigenetic marking patterns encode genome architecture. Proc. Natl Acad. Sci. USA 114, 12126–12131 (2017).
pubmed: 29087948
pmcid: 5699090
doi: 10.1073/pnas.1714980114
Lin, D., Bonora, G., Yardimci, G. G. & Noble, W. S. Computational methods for analyzing and modeling genome structure and organization. Wiley Interdiscip. Rev. Syst. Biol. Med. 11, e1435 (2019).
pubmed: 30022617
doi: 10.1002/wsbm.1435
Kalhor, R., Tjong, H., Jayathilaka, N., Alber, F. & Chen, L. Genome architectures revealed by tethered chromosome conformation capture and population-based modeling. Nat. Biotechnol. 30, 90–98 (2012).
doi: 10.1038/nbt.2057
Crane, E. et al. Condensin-driven remodelling of X chromosome topology during dosage compensation. Nature 523, 240–244 (2015).
pubmed: 26030525
pmcid: 4498965
doi: 10.1038/nature14450
Shin, H. et al. TopDom: an efficient and deterministic method for identifying topological domains in genomes. Nucleic Acids Res. 44, e70 (2015). This article presents one of the most reliable and popular TAD callers.
pubmed: 26704975
pmcid: 4838359
doi: 10.1093/nar/gkv1505
Malik, L. & Patro, R. Rich chromatin structure prediction from Hi-C data. IEEE/ACM Trans. Comput. Biol. Bioinform. 16, 1448–1458 (2019).
pubmed: 29994683
doi: 10.1109/TCBB.2018.2851200
Haddad, N., Vaillant, C. & Jost, D. IC-Finder: inferring robustly the hierarchical organization of chromatin folding. Nucleic Acids Res. 45, 81 (2017).
Soler-Vila, P., Cuscó, P., Farabella, I., Di Stefano, M. & Marti-Renom, M. A. Hierarchical chromatin organization detected by TADpole. Nucleic Acids Res. 48, e39 (2020). This paper presents one of the most recently developed TAD callers and is extremely valuable for its benchmarking quality and for multiple TAD caller comparisons.
pubmed: 32083658
pmcid: 7144900
doi: 10.1093/nar/gkaa087
Norton, H. K. et al. Detecting hierarchical genome folding with network modularity. Nat. Methods 15, 119–122 (2018).
pubmed: 29334377
pmcid: 6029251
doi: 10.1038/nmeth.4560
Moller, J. & de Pablo, J. J. Bottom-up meets top-down: the crossroads of multiscale chromatin modeling. Biophys. J. 118, 2057–2065 (2020).
pubmed: 32320675
pmcid: 7203006
doi: 10.1016/j.bpj.2020.03.014
Bendandi, A., Dante, S., Zia, S. R., Diaspro, A. & Rocchia, W. Chromatin compaction multiscale modeling: a complex synergy between theory, simulation, and experiment. Front. Mol. Biosci. 7, 15 (2020).
pubmed: 32158765
pmcid: 7051991
doi: 10.3389/fmolb.2020.00015
Zufferey, M., Tavernari, D., Oricchio, E. & Ciriello, G. Comparison of computational methods for the identification of topologically associating domains. Genome Biol. 19, 217 (2018).
pubmed: 30526631
pmcid: 6288901
doi: 10.1186/s13059-018-1596-9
Forcato, M. et al. Comparison of computational methods for Hi-C data analysis. Nat. Methods 14, 679–685 (2017).
pubmed: 28604721
pmcid: 5493985
doi: 10.1038/nmeth.4325
Ay, F., Bailey, T. L. & Noble, W. S. Statistical confidence estimation for Hi-C data reveals regulatory chromatin contacts. Genome Res. 24, 999–1011 (2014).
pubmed: 24501021
pmcid: 4032863
doi: 10.1101/gr.160374.113
Carty, M. et al. An integrated model for detecting significant chromatin interactions from high-resolution Hi-C data. Nat. Commun. 8, 1–10 (2017).
doi: 10.1038/ncomms15454
Pal, K., Forcato, M. & Ferrari, F. Hi-C analysis: from data generation to integration. Biophys. Rev. 11, 67–78 (2019).
pubmed: 30570701
doi: 10.1007/s12551-018-0489-1
Dozmorov, M., Sirusb & Benfeitas, R. Hi-C data analysis tools and papers. GitHub https://github.com/mdozmorov/HiC_tools/blob/master/README.md (2021).
Roayaei Ardakany, A., Gezer, H. T., Lonardi, S. & Ay, F. Mustache: multi-scale detection of chromatin loops from Hi-C and Micro-C maps using scale-space representation. Genome Biol. 21, 256 (2020).
pubmed: 32998764
pmcid: 7528378
doi: 10.1186/s13059-020-02167-0
Jordan Rowley, M. et al. Analysis of Hi-C data using SIP effectively identifies loops in organisms from C. elegans to mammals. Genome Res. 30, 447–458 (2020).
pubmed: 32127418
doi: 10.1101/gr.257832.119
Ay, F. & Noble, W. S. Analysis methods for studying the 3D architecture of the genome. Genome Biol. 16, 183 (2015).
pubmed: 26328929
pmcid: 4556012
doi: 10.1186/s13059-015-0745-7
Nikumbh, S. & Pfeifer, N. Genetic sequence-based prediction of long-range chromatin interactions suggests a potential role of short tandem repeat sequences in genome organization. BMC Bioinformatics 18, 218 (2017).
pubmed: 28420341
pmcid: 5395875
doi: 10.1186/s12859-017-1624-x
Rhie, S. K. et al. Using 3D epigenomic maps of primary olfactory neuronal cells from living individuals to understand gene regulation. Sci. Adv. 4, eaav8550 (2018).
pubmed: 30555922
pmcid: 6292713
doi: 10.1126/sciadv.aav8550
Hafez, D. et al. McEnhancer: predicting gene expression via semi-supervised assignment of enhancers to target genes. Genome Biol. 18, 199 (2017).
pubmed: 29070071
pmcid: 5657048
doi: 10.1186/s13059-017-1316-x
Di Iulio, J. et al. The human noncoding genome defined by genetic diversity. Nat. Genet. 50, 333–337 (2018).
pubmed: 29483654
doi: 10.1038/s41588-018-0062-7
Javierre, B. M. et al. Lineage-specific genome architecture links enhancers and non-coding disease variants to target gene promoters. Cell 167, 1369–1384 (2016).
pubmed: 27863249
pmcid: 5123897
doi: 10.1016/j.cell.2016.09.037
Mitchelmore, J., Grinberg, N. F., Wallace, C. & Spivakov, M. Functional effects of variation in transcription factor binding highlight long-range gene regulation by epromoters. Nucleic Acids Res. 48, 2866–2879 (2020).
pubmed: 32112106
pmcid: 7102942
doi: 10.1093/nar/gkaa123
Malysheva, V., Mendoza-Parra, M. A., Blum, M., Spivakov, M. & Gronemeyer, H. Gene regulatory network reconstruction incorporating 3D chromosomal architecture reveals key transcription factors and DNA elements driving neural lineage commitment. Preprint at bioRxiv https://doi.org/10.1101/303842 (2019).
doi: 10.1101/303842
Madrid-Mencía, M., Raineri, E., Cao, T. B. N. & Pancaldi, V. Using GARDEN-NET and ChAseR to explore human haematopoietic 3D chromatin interaction networks. Nucleic Acids Res. 48, 4066–4080 (2020).
pubmed: 32182345
pmcid: 7192625
doi: 10.1093/nar/gkaa159
Zhang, Y. et al. Enhancing Hi-C data resolution with deep convolutional neural network HiCPlus. Nat. Commun. 9, 1–9 (2018).
Oluwadare, O., Highsmith, M. & Cheng, J. An overview of methods for reconstructing 3-D chromosome and genome structures from Hi-C data. Biol. Proced. Online 21, 1–20 (2019).
doi: 10.1186/s12575-019-0094-0
Marti-Renom, M. A. et al. Challenges and guidelines toward 4D nucleome data and model standards. Nat. Genet. 50, 1352–1358 (2018).
pubmed: 30262815
doi: 10.1038/s41588-018-0236-3
MacPherson, Q., Beltran, B. & Spakowitz, A. J. Bottom-up modeling of chromatin segregation due to epigenetic modifications. Proc. Natl Acad. Sci. USA 115, 12739–12744 (2018).
pubmed: 30478042
pmcid: 6294944
doi: 10.1073/pnas.1812268115
Bianco, S., Chiariello, A. M., Annunziatella, C., Esposito, A. & Nicodemi, M. Predicting chromatin architecture from models of polymer physics. Chromosome Res. 25, 25–34 (2017).
pubmed: 28070687
doi: 10.1007/s10577-016-9545-5
Mirny, L. A. The fractal globule as a model of chromatin architecture in the cell. Chromosom. Res. 19, 37–51 (2011).
doi: 10.1007/s10577-010-9177-0
Barbieri, M. et al. A model of the large-scale organization of chromatin. Biochem. Soc. Trans. 41, 508–512 (2013).
pubmed: 23514144
doi: 10.1042/BST20120238
Jost, D., Carrivain, P., Cavalli, G. & Vaillant, C. Modeling epigenome folding: formation and dynamics of topologically associated chromatin domains. Nucleic Acids Res. 42, 9553–9561 (2014).
pubmed: 25092923
pmcid: 4150797
doi: 10.1093/nar/gku698
Jost, D. & Vaillant, C. Epigenomics in 3D: importance of long-range spreading and specific interactions in epigenomic maintenance. Nucleic Acids Res. 46, 2252–2264 (2018).
pubmed: 29365171
pmcid: 5861409
doi: 10.1093/nar/gky009
Barbieri, M. et al. Active and poised promoter states drive folding of the extended HoxB locus in mouse embryonic stem cells. Nat. Struct. Mol. Biol. 24, 515–524 (2017).
pubmed: 28436944
doi: 10.1038/nsmb.3402
Falk, M. et al. Heterochromatin drives compartmentalization of inverted and conventional nuclei. Nature 570, 395–399 (2019).
pubmed: 31168090
pmcid: 7206897
doi: 10.1038/s41586-019-1275-3
Oliveira Junior, A. B., Contessoto, V. G., Mello, M. F. & Onuchic, J. N. A scalable computational approach for simulating complexes of multiple chromosomes. J. Mol. Biol. 433, 166700 (2020).
pubmed: 33160979
doi: 10.1016/j.jmb.2020.10.034
Ghosh, S. K. & Jost, D. How epigenome drives chromatin folding and dynamics, insights from efficient coarse-grained models of chromosomes. PLoS Comput. Biol. 14, e1006159 (2018).
pubmed: 29813054
pmcid: 6003694
doi: 10.1371/journal.pcbi.1006159
Giorgetti, L. et al. Predictive polymer modeling reveals coupled fluctuations in chromosome conformation and transcription. Cell 157, 950–963 (2014).
pubmed: 24813616
pmcid: 4427251
doi: 10.1016/j.cell.2014.03.025
Bianco, S. et al. Polymer physics predicts the effects of structural variants on chromatin architecture. Nat. Genet. 50, 662–667 (2018).
pubmed: 29662163
doi: 10.1038/s41588-018-0098-8
Contessoto, V. G. et al. The Nucleome Data Bank: web-based resources to simulate and analyze the three-dimensional genome. Nucleic Acids Res. 49, 172–182 (2020).
doi: 10.1093/nar/gkaa818
Rousseau, M., Fraser, J., Ferraiuolo, M. A., Dostie, J. & Blanchette, M. Three-dimensional modeling of chromatin structure from interaction frequency data using Markov chain Monte Carlo sampling. BMC Bioinformatics 12, 414 (2011).
pubmed: 22026390
pmcid: 3245522
doi: 10.1186/1471-2105-12-414
Baú, D. et al. The three-dimensional folding of the α-globin gene domain reveals formation of chromatin globules. Nat. Struct. Mol. Biol. 18, 107–115 (2011).
pubmed: 21131981
doi: 10.1038/nsmb.1936
Trussart, M. et al. Defined chromosome structure in the genome-reduced bacterium Mycoplasma pneumoniae. Nat. Commun. 8, 14665 (2017).
pubmed: 28272414
pmcid: 5344976
doi: 10.1038/ncomms14665
Zhu, G. et al. Reconstructing spatial organizations of chromosomes through manifold learning. Nucleic Acids Res. 46, e50 (2018).
pubmed: 29408992
pmcid: 5934626
doi: 10.1093/nar/gky065
Paulsen, J. et al. Long-range interactions between topologically associating domains shape the four-dimensional genome during differentiation. Nat. Genet. 51, 835–843 (2019).
pubmed: 31011212
doi: 10.1038/s41588-019-0392-0
Lesne, A., Riposo, J., Roger, P., Cournac, A. & Mozziconacci, J. 3D genome reconstruction from chromosomal contacts. Nat. Methods 11, 1141–1143 (2014).
pubmed: 25240436
doi: 10.1038/nmeth.3104
Trieu, T., Oluwadare, O. & Cheng, J. Hierarchical reconstruction of high-resolution 3D models of large chromosomes. Sci. Rep. 9, 1–12 (2019).
doi: 10.1038/s41598-019-41369-w
Tan, L., Xing, D., Chang, C.-H. H., Li, H. & Xie, X. S. Three-dimensional genome structures of single diploid human cells. Science 361, 924–928 (2018).
pubmed: 30166492
pmcid: 6360088
doi: 10.1126/science.aat5641
Di Stefano, M. et al. Transcriptional activation during cell reprogramming correlates with the formation of 3D open chromatin hubs. Nat. Commun. 11, 1–12 (2020).
doi: 10.1038/s41467-020-16396-1
Li, Q. et al. The three-dimensional genome organization of Drosophila melanogaster through data integration. Genome Biol. 18, 145 (2017).
pubmed: 28760140
pmcid: 5576134
doi: 10.1186/s13059-017-1264-5
Hua, N. et al. Producing genome structure populations with the dynamic and automated PGS software. Nat. Protoc. 13, 915–926 (2018).
pubmed: 29622804
pmcid: 6043163
doi: 10.1038/nprot.2018.008
Whalen, S., Truty, R. M. & Pollard, K. S. Enhancer–promoter interactions are encoded by complex genomic signatures on looping chromatin. Nat. Genet. 48, 488–496 (2016).
pubmed: 27064255
pmcid: 4910881
doi: 10.1038/ng.3539
Li, W., Wong, W. H. & Jiang, R. DeepTACT: predicting 3D chromatin contacts via bootstrapping deep learning. Nucleic Acids Res. 47, e60 (2019).
pubmed: 30869141
pmcid: 6547469
doi: 10.1093/nar/gkz167
Fudenberg, G., Kelley, D. R. & Pollard, K. S. Predicting 3D genome folding from DNA sequence with Akita. Nat. Methods 17, 1111–1117 (2020). This is the first computational modelling paper describing modelling of chromatin conformation solely from the DNA.
pubmed: 33046897
pmcid: 8211359
doi: 10.1038/s41592-020-0958-x
Schwessinger, R. et al. DeepC: predicting 3D genome folding using megabase-scale transfer learning. Nat. Methods 17, 1118–1124 (2020). This article presents one of the first computational tools to model chromatin conformation solely from the DNA sequence. However, unlike Akita, it requires training on the epigenetics data.
pubmed: 33046896
pmcid: 7610627
doi: 10.1038/s41592-020-0960-3
Zhang, S., Chasman, D., Knaack, S. & Roy, S. In silico prediction of high-resolution Hi-C interaction matrices. Nat. Commun. 10, 1–18 (2019).
doi: 10.1038/s41467-019-13423-8
Belokopytova, P. S., Nuriddinov, M. A., Mozheiko, E. A., Fishman, D. & Fishman, V. Quantitative prediction of enhancer–promoter interactions. Genome Res. 30, 72–84 (2020).
pubmed: 31804952
pmcid: 6961579
doi: 10.1101/gr.249367.119
Qi, Y. et al. Data-driven polymer model for mechanistic exploration of diploid genome organization. Biophys. J. 119, 1905–1916 (2020).
pubmed: 33086041
doi: 10.1016/j.bpj.2020.09.009
pmcid: 7677132
de Luca, K. L. & Kind, J. in Methods in Molecular Biology Vol. 2157 159–172 (Humana, 2021).
Li, G. et al. Joint profiling of DNA methylation and chromatin architecture in single cells. Nat. Methods 16, 991–993 (2019).
pubmed: 31384045
pmcid: 6765429
doi: 10.1038/s41592-019-0502-z
Zheng, M. et al. Multiplex chromatin interactions with single-molecule precision. Nature 566, 558–562 (2019).
pubmed: 30778195
pmcid: 7001875
doi: 10.1038/s41586-019-0949-1
Ramani, V. et al. Massively multiplex single-cell Hi-C. Nat. Methods 14, 263–266 (2017).
pubmed: 28135255
pmcid: 5330809
doi: 10.1038/nmeth.4155
You, Q. et al. Direct DNA crosslinking with CAP-C uncovers transcription-dependent chromatin organization at high resolution. Nat. Biotechnol. 39, 225–235 (2020).
pubmed: 32839564
doi: 10.1038/s41587-020-0643-8
pmcid: 8274026
Girelli, G. et al. GPSeq reveals the radial organization of chromatin in the cell nucleus. Nat. Biotechnol. 38, 1184–1193 (2020).
pubmed: 32451505
pmcid: 7610410
doi: 10.1038/s41587-020-0519-y
Wang, Y. et al. SPIN reveals genome-wide landscape of nuclear compartmentalization. Genome Biol. 22, 36 (2021). This article presents the first tool that combines nuclear architecture (positioning) data from TSA-seq and DamID in order to compute spatial compartmentalization of chromatin in respect to the lamina or nuclear bodies such as nuclear speckles.
pubmed: 33446254
pmcid: 7809771
doi: 10.1186/s13059-020-02253-3
Kubalová, I. et al. Prospects and limitations of expansion microscopy in chromatin ultrastructure determination. Chromosom. Res. 28, 355–368 (2020).
doi: 10.1007/s10577-020-09637-y
Shi, X. et al. Label-retention expansion microscopy. Preprint at bioRxiv https://doi.org/10.1101/687954 (2021).
doi: 10.1101/687954
pubmed: 34845456
pmcid: 8629199
Wassie, A. T., Zhao, Y. & Boyden, E. S. Expansion microscopy: principles and uses in biological research. Nat. Methods 16, 33–41 (2019).
pubmed: 30573813
doi: 10.1038/s41592-018-0219-4
Alon, S. et al. Expansion sequencing: spatially precise in situ transcriptomics in intact biological systems. Science 371, eaax2656 (2021).
pubmed: 33509999
pmcid: 7900882
doi: 10.1126/science.aax2656
Robinett, C. C. et al. In vivo localization of DNA sequences and visualization of large-scale chromatin organization using lac operator/repressor recognition. J. Cell Biol. 135, 1685–1700 (1996).
pubmed: 8991083
doi: 10.1083/jcb.135.6.1685
Belmont, A. S. & Straight, A. F. In vivo visualization of chromosomes using lac operator-repressor binding. Trends Cell Biol. 8, 121–124 (1998).
pubmed: 9695822
doi: 10.1016/S0962-8924(97)01211-7
Lucas, J. S., Zhang, Y., Dudko, O. K. & Murre, C. 3D trajectories adopted by coding and regulatory DNA elements: first-passage times for genomic interactions. Cell 158, 339–352 (2014).
pubmed: 24998931
pmcid: 4113018
doi: 10.1016/j.cell.2014.05.036
Chen, H. et al. Dynamic interplay between enhancer–promoter topology and gene activity. Nat. Genet. 50, 1296–1303 (2018).
pubmed: 30038397
pmcid: 6119122
doi: 10.1038/s41588-018-0175-z
Maass, P. G. et al. Spatiotemporal allele organization by allele-specific CRISPR live-cell imaging (SNP-CLING). Nat. Struct. Mol. Biol. 25, 176–184 (2018).
pubmed: 29343869
pmcid: 5805655
doi: 10.1038/s41594-017-0015-3
Wang, H. et al. CRISPR-mediated live imaging of genome editing and transcription. Science 365, 1301–1305 (2019).
pubmed: 31488703
doi: 10.1126/science.aax7852
Geng, Y. & Pertsinidis, A. CAS-LiveFISH: simple and versatile imaging of genomic loci in live mammalian cells and early pre-implantation embryos. Preprint at bioRxiv https://doi.org/10.1101/2020.08.25.265306 (2020).
doi: 10.1101/2020.08.25.265306
pubmed: 32935102
pmcid: 7491516
Neguembor, M. V. et al. (Po)STAC (polycistronic SunTAg modified CRISPR) enables live-cell and fixed-cell super-resolution imaging of multiple genes. Nucleic Acids Res. 46, e30 (2018).
pubmed: 29294098
doi: 10.1093/nar/gkx1271
Chu, L. et al. The 3D topography of mitotic chromosomes. Mol. Cell 79, 902–916.e6 (2020).
pubmed: 32768407
doi: 10.1016/j.molcel.2020.07.002
Liu, X. et al. In situ capture of chromatin interactions by biotinylated dCas9. Cell 170, 1028–1043 (2017).
pubmed: 28841410
pmcid: 6857456
doi: 10.1016/j.cell.2017.08.003
Tsui, C. et al. dCas9-targeted locus-specific protein isolation method identifies histone gene regulators. Proc. Natl Acad. Sci. USA 115, 2734–2741 (2018).
doi: 10.1073/pnas.1718844115
Myers, S. A. et al. Discovery of proteins associated with a predefined genomic locus via dCas9–APEX-mediated proximity labeling. Nat. Methods 15, 437–439 (2018).
pubmed: 29735997
pmcid: 6202184
doi: 10.1038/s41592-018-0007-1
de Wit, E. et al. CTCF binding polarity determines chromatin looping. Mol. Cell 60, 676–684 (2015).
pubmed: 26527277
doi: 10.1016/j.molcel.2015.09.023
Gómez-Marín, C. et al. Evolutionary comparison reveals that diverging CTCF sites are signatures of ancestral topological associating domains borders. Proc. Natl Acad. Sci. USA 112, 7542–7547 (2015).
pubmed: 26034287
pmcid: 4475986
doi: 10.1073/pnas.1505463112
Bantignies, F. et al. Polycomb-dependent regulatory contacts between distant hox loci in Drosophila. Cell 144, 214–226 (2011).
pubmed: 21241892
doi: 10.1016/j.cell.2010.12.026
Monahan, K., Horta, A. & Lomvardas, S. LHX2- and LDB1-mediated trans interactions regulate olfactory receptor choice. Nature 565, 448–453 (2019).
pubmed: 30626972
pmcid: 6436840
doi: 10.1038/s41586-018-0845-0
Phillips-Cremins, J. E. et al. Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 153, 1281–1295 (2013).
pubmed: 23706625
pmcid: 3712340
doi: 10.1016/j.cell.2013.04.053
Bhattacharyya, S., Chandra, V., Vijayanand, P. & Ay, F. Identification of significant chromatin contacts from HiChIP data by FitHiChIP. Nat. Commun. 10, 1–14 (2019).
doi: 10.1038/s41467-019-11950-y
Takei, Y. et al. Global architecture of the nucleus in single cells by DNA seqFISH+ and multiplexed immunofluorescence. Preprint at bioRxiv https://doi.org/10.1101/2020.11.29.403055 (2020).
doi: 10.1101/2020.11.29.403055
Tolhuis, B., Palstra, R. J., Splinter, E., Grosveld, F. & de Laat, W. Looping and interaction between hypersensitive sites in the active β-globin locus. Mol. Cell 10, 1453–1465 (2002).
pubmed: 12504019
doi: 10.1016/S1097-2765(02)00781-5
Palstra, R. J. et al. The β-globin nuclear compartment in development and erythroid differentiation. Nat. Genet. 35, 190–194 (2003).
pubmed: 14517543
doi: 10.1038/ng1244
Splinter, E. et al. CTCF mediates long-range chromatin looping and local histone modification in the β-globin locus. Genes Dev. 20, 2349–2354 (2006).
pubmed: 16951251
pmcid: 1560409
doi: 10.1101/gad.399506
Vakoc, C. R. et al. Proximity among distant regulatory elements at the β-globin locus requires GATA-1 and FOG-1. Mol. Cell 17, 453–462 (2005).
pubmed: 15694345
doi: 10.1016/j.molcel.2004.12.028
Splinter, E. & De Laat, W. The complex transcription regulatory landscape of our genome: control in three dimensions. EMBO J. 30, 4345–4355 (2011).
pubmed: 21952046
pmcid: 3230377
doi: 10.1038/emboj.2011.344
Zhao, Z. et al. Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions. Nat. Genet. 38, 1341–1347 (2006).
pubmed: 17033624
doi: 10.1038/ng1891
Andrey, G. et al. A switch between topological domains underlies HoxD genes collinearity in mouse limbs. Science 340, 1234167 (2013).
pubmed: 23744951
doi: 10.1126/science.1234167
Ghavi-Helm, Y. et al. Enhancer loops appear stable during development and are associated with paused polymerase. Nature 512, 96–100 (2014).
pubmed: 25043061
doi: 10.1038/nature13417
Apostolou, E. et al. Genome-wide chromatin interactions of the nanog locus in pluripotency, differentiation, and reprogramming. Cell Stem Cell 12, 699–712 (2013).
pubmed: 23665121
pmcid: 3725985
doi: 10.1016/j.stem.2013.04.013
Van De Werken, H. J. G. et al. in Methods in Enzymology Vol. 513 (eds Wu, C. & Allis, D) 89–112 (Academic, 2012).
Bonev, B. & Cavalli, G. Organization and function of the 3D genome. Nat. Rev. Genet. 17, 661–678 (2016).
pubmed: 27739532
doi: 10.1038/nrg.2016.112
Y, G. H. et al. Highly rearranged chromosomes reveal uncoupling between genome topology and gene expression. Nat. Genet. 51, 1272–1282 (2019).
doi: 10.1038/s41588-019-0462-3
Lupiáñez, D. G. et al. Disruptions of topological chromatin domains cause pathogenic rewiring of gene–enhancer interactions. Cell 161, 1012–1025 (2015).
pubmed: 25959774
pmcid: 4791538
doi: 10.1016/j.cell.2015.04.004
Ogiyama, Y., Schuettengruber, B., Papadopoulos, G. L., Chang, J.-M. & Cavalli, G. Polycomb-dependent chromatin looping contributes to gene silencing during Drosophila development. Mol. Cell 71, 73–88 (2018).
pubmed: 30008320
doi: 10.1016/j.molcel.2018.05.032
Flavahan, W. A. et al. Altered chromosomal topology drives oncogenic programs in SDH-deficient GISTs. Nature 575, 229–233 (2019).
pubmed: 31666694
pmcid: 6913936
doi: 10.1038/s41586-019-1668-3
Tarjan, D. R., Flavahan, W. A. & Bernstein, B. E. Epigenome editing strategies for the functional annotation of CTCF insulators. Nat. Commun. 10, 4258 (2019).
pubmed: 31534142
pmcid: 6751197
doi: 10.1038/s41467-019-12166-w
Kim, J. H. et al. LADL: light-activated dynamic looping for endogenous gene expression control. Nat. Methods 16, 633–639 (2019).
pubmed: 31235883
pmcid: 6599567
doi: 10.1038/s41592-019-0436-5
Wang, H. et al. CRISPR-mediated programmable 3D genome positioning and nuclear organization. Cell 175, 1405–1417 (2018).
pubmed: 30318144
pmcid: 6239909
doi: 10.1016/j.cell.2018.09.013