Transcription factors: building hubs in the 3D space

References

• Gorkin DU, Leung D, Ren B. The 3D genome in transcriptional regulation and pluripotency. Cell Stem Cell. 2014;14:762–775.
   PubMed Web of Science ®Google Scholar
• Dekker J, Belmont AS, Guttman M, et al. The 4D nucleome project. Nature. 2017;549:219–226.
   PubMed Web of Science ®Google Scholar
• Apostolou E, Ferrari F, Walsh RM, et al. Genome-wide chromatin interactions of the Nanog locus in pluripotency, differentiation, and reprogramming. Cell Stem Cell. 2013;12:699–712.
   PubMed Web of Science ®Google Scholar
• Denholtz M, Bonora G, Chronis C, et al. Long-range chromatin contacts in embryonic stem cells reveal a role for pluripotency factors and polycomb proteins in genome organization. Cell Stem Cell. 2013;13:602–616.
   PubMed Web of Science ®Google Scholar
• Dixon JR, Selvaraj S, Yue F, et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature. 2012;485:376–380.
   PubMed Web of Science ®Google Scholar
• Beagan JA, Gilgenast TG, Kim J, et al. Local genome topology can exhibit an incompletely rewired 3D-folding state during somatic cell reprogramming. Cell Stem Cell. 2016;18:611–624.
   PubMed Web of Science ®Google Scholar
• Di Giammartino DC, Apostolou E. The chromatin signature of pluripotency: establishment and maintenance. Curr Stem Cell Rep. 2016;2:255–262.
   PubMed Web of Science ®Google Scholar
• Li G, Ruan X, Auerbach RK, et al. Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell. 2012;148:84–98.
   PubMed Web of Science ®Google Scholar
• Yao L, Berman BP, Farnham PJ. Demystifying the secret mission of enhancers: linking distal regulatory elements to target genes. Crit Rev Biochem Mol Biol. 2015;50:550–573.
   PubMed Web of Science ®Google Scholar
• Sun F, Chronis C, Kronenberg M, et al. Promoter-enhancer communication occurs primarily within insulated neighborhoods. Mol Cell. 2019;73:250–63 e5.
   PubMed Web of Science ®Google Scholar
• Hnisz D, Day DS, Young RA. Insulated neighborhoods: structural and functional units of mammalian gene control. Cell. 2016;167:1188–1200.
   PubMed Web of Science ®Google Scholar
• Dowen JM, Fan ZP, Hnisz D, et al. Control of cell identity genes occurs in insulated neighborhoods in mammalian chromosomes. Cell. 2014;159:374–387.
   PubMed Web of Science ®Google Scholar
• Nuebler J, Fudenberg G, Imakaev M, et al. Chromatin organization by an interplay of loop extrusion and compartmental segregation. Proc Natl Acad Sci U S A. 2018;115:E6697–E706.
   PubMed Web of Science ®Google Scholar
• Rada-Iglesias A, Grosveld FG, Papantonis A. Forces driving the three-dimensional folding of eukaryotic genomes. Mol Syst Biol. 2018;14:e8214.
   PubMed Web of Science ®Google Scholar
• Beagan JA, Phillips-Cremins JE. On the existence and functionality of topologically associating domains. Nat Genet. 2020;52:8–16.
   PubMed Web of Science ®Google Scholar
• Lieberman-Aiden E, van Berkum NL, Williams L, et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science. 2009;326:289–293.
   PubMed Web of Science ®Google Scholar
• Takebayashi S, Dileep V, Ryba T, et al. Chromatin-interaction compartment switch at developmentally regulated chromosomal domains reveals an unusual principle of chromatin folding. Proc Natl Acad Sci U S A. 2012;109:12574–12579.
   PubMed Web of Science ®Google Scholar
• Dixon JR, Jung I, Selvaraj S, et al. Chromatin architecture reorganization during stem cell differentiation. Nature. 2015;518:331–336.
   PubMed Web of Science ®Google Scholar
• Stadhouders R, Vidal E, Serra F, et al. Transcription factors orchestrate dynamic interplay between genome topology and gene regulation during cell reprogramming. Nat Genet. 2018;50:238–249.
   PubMed Web of Science ®Google Scholar
• Szabo Q, Bantignies F, Cavalli G. Principles of genome folding into topologically associating domains. Sci Adv. 2019;5:eaaw1668.
   PubMed Web of Science ®Google Scholar
• Schoenfelder S, Fraser P. Long-range enhancer-promoter contacts in gene expression control. Nat Rev Genet. 2019;20:437–455.
   PubMed Web of Science ®Google Scholar
• Drissen R, Palstra RJ, Gillemans N, et al. The active spatial organization of the beta-globin locus requires the transcription factor EKLF. Genes Dev. 2004;18:2485–2490.
   PubMed Web of Science ®Google Scholar
• Robson MI, Ringel AR, Mundlos S. Regulatory landscaping: how enhancer-promoter communication is sculpted in 3D. Mol Cell. 2019;74:1110–1122.
   PubMed Web of Science ®Google Scholar
• Apostolou E, Thanos D. Virus infection induces NF-kappaB-dependent interchromosomal associations mediating monoallelic IFN-beta gene expression. Cell. 2008;134:85–96.
   PubMed Web of Science ®Google Scholar
• Wei Z, Gao F, Kim S, et al. Klf4 organizes long-range chromosomal interactions with the oct4 locus in reprogramming and pluripotency. Cell Stem Cell. 2013;13:36–47.
   PubMedGoogle Scholar
• Markenscoff-Papadimitriou E, Allen WE, Colquitt BM, et al. Enhancer interaction networks as a means for singular olfactory receptor expression. Cell. 2014;159:543–557.
   PubMed Web of Science ®Google Scholar
• Lomvardas S, Barnea G, Pisapia DJ, et al. Interchromosomal interactions and olfactory receptor choice. Cell. 2006;126:403–413.
   PubMed Web of Science ®Google Scholar
• Schoenfelder S, Sexton T, Chakalova L, et al. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat Genet. 2010;42:53–61.
   PubMed Web of Science ®Google Scholar
• Noordermeer D, Leleu M, Splinter E, et al. The dynamic architecture of hox gene clusters. Science. 2011;334:222–225.
   PubMed Web of Science ®Google Scholar
• Rao SS, Huntley MH, Durand NC, et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell. 2014;159:1665–1680.
   PubMed Web of Science ®Google Scholar
• Bonev B, Mendelson Cohen N, Szabo Q, et al. Multiscale 3D genome rewiring during mouse neural development. Cell. 2017;171:557–72 e24.
   PubMed Web of Science ®Google Scholar
• Gasperini M, Hill AJ, McFaline-Figueroa JL, et al. A genome-wide framework for mapping gene regulation via cellular genetic screens. Cell. 2019;176:1516.
   PubMed Web of Science ®Google Scholar
• Di Giammartino DC, Kloetgen A, Polyzos A, et al. KLF4 is involved in the organization and regulation of pluripotency-associated three-dimensional enhancer networks. Nat Cell Biol. 2019;21:1179–1190.
   PubMed Web of Science ®Google Scholar
• Li G, Cai L, Chang H, et al. Chromatin interaction analysis with paired-end tag (ChIA-PET) sequencing technology and application. BMC Genomics. 2014;15(Suppl 12):S11.
   PubMedGoogle Scholar
• Fang R, Yu M, Li G, et al. Mapping of long-range chromatin interactions by proximity ligation-assisted ChIP-seq. Cell Res. 2016;26:1345–1348.
   PubMed Web of Science ®Google Scholar
• Mumbach MR, Satpathy AT, Boyle EA, et al. Enhancer connectome in primary human cells identifies target genes of disease-associated DNA elements. Nat Genet. 2017;49:1602–1612.
   PubMed Web of Science ®Google Scholar
• Davies JO, Telenius JM, McGowan SJ, et al. Multiplexed analysis of chromosome conformation at vastly improved sensitivity. Nat Methods. 2016;13:74–80.
   PubMed Web of Science ®Google Scholar
• Petrovic J, Zhou Y, Fasolino M, et al. Oncogenic notch promotes long-range regulatory interactions within hyperconnected 3D cliques. Mol Cell. 2019;73:1174–90 e12.
   PubMed Web of Science ®Google Scholar
• Weintraub AS, Li CH, Zamudio AV, et al. YY1 is a structural regulator of enhancer-promoter loops. Cell. 2017;171:1573–88 e28.
   PubMed Web of Science ®Google Scholar
• Ji X, Dadon DB, Powell BE, et al. 3D chromosome regulatory landscape of human pluripotent cells. Cell Stem Cell. 2016;18:262–275.
   PubMed Web of Science ®Google Scholar
• Song M, Pebworth M-P, Yang X, et al. 3D epigenomic characterization reveals insights into gene regulation and lineage specification during corticogenesis. bioRxiv. 2020. 2020.02.24.963652.
   Google Scholar
• Whyte WA, Orlando DA, Hnisz D, et al. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell. 2013;153:307–319.
   PubMed Web of Science ®Google Scholar
• Schmitt AD, Hu M, Jung I, et al. A compendium of chromatin contact maps reveals spatially active regions in the human genome. Cell Rep. 2016;17(8):2042–2059.
   PubMed Web of Science ®Google Scholar
• Vian L, Pekowska A, Rao SSP, et al. The energetics and physiological impact of cohesin extrusion. Cell. 2018;175:292–294.
   PubMed Web of Science ®Google Scholar
• Rao SSP, Huang SC, Glenn St Hilaire B, et al. Cohesin loss eliminates all loop domains. Cell. 2017;171:305–20 e24.
   PubMed Web of Science ®Google Scholar
• Parker SC, Stitzel ML, Taylor DL, et al. Chromatin stretch enhancer states drive cell-specific gene regulation and harbor human disease risk variants. Proc Natl Acad Sci U S A. 2013;110:17921–17926.
   PubMed Web of Science ®Google Scholar
• Miguel-Escalada I, Bonas-Guarch S, Cebola I, et al. Human pancreatic islet three-dimensional chromatin architecture provides insights into the genetics of type 2 diabetes. Nat Genet. 2019;51:1137–1148.
   PubMed Web of Science ®Google Scholar
• Oudelaar AM, Davies JOJ, Hanssen LLP, et al. Single-allele chromatin interactions identify regulatory hubs in dynamic compartmentalized domains. Nat Genet. 2018;50:1744–1751.
   PubMed Web of Science ®Google Scholar
• Oudelaar AM, Harrold CL, Hanssen LLP, et al. A revised model for promoter competition based on multi-way chromatin interactions at the alpha-globin locus. Nat Commun. 2019;10:5412.
   PubMed Web of Science ®Google Scholar
• Allahyar A, Vermeulen C, Bouwman BAM, et al. Enhancer hubs and loop collisions identified from single-allele topologies. Nat Genet. 2018;50:1151–1160.
   PubMed Web of Science ®Google Scholar
• Jiang T, Raviram R, Snetkova V, et al. Identification of multi-loci hubs from 4C-seq demonstrates the functional importance of simultaneous interactions. Nucleic Acids Res. 2016;44:8714–8725.
   PubMed Web of Science ®Google Scholar
• Weiterer SS, Meier-Soelch J, Georgomanolis T, et al. Distinct IL-1alpha-responsive enhancers promote acute and coordinated changes in chromatin topology in a hierarchical manner. EMBO J. 2020;39:e101533.
   PubMed Web of Science ®Google Scholar
• Nagano T, Lubling Y, Yaffe E, et al. Single-cell Hi-C for genome-wide detection of chromatin interactions that occur simultaneously in a single cell. Nat Protoc. 2015;10:1986–2003.
   PubMed Web of Science ®Google Scholar
• Ramani V, Deng X, Qiu R, et al. Massively multiplex single-cell Hi-C. Nat Methods. 2017;14:263–266.
   PubMed Web of Science ®Google Scholar
• Ramani V, Deng X, Qiu R, et al. Sci-Hi-C: a single-cell Hi-C method for mapping 3D genome organization in large number of single cells. Methods. 2020;170:61–68.
   PubMed Web of Science ®Google Scholar
• Kempfer R, Pombo A. Methods for mapping 3D chromosome architecture. Nat Rev Genet. ;2020;21(4):207-226..
   PubMed Web of Science ®Google Scholar
• Beagrie RA, Scialdone A, Schueler M, et al. Complex multi-enhancer contacts captured by genome architecture mapping. Nature. 2017;543:519–524.
   PubMed Web of Science ®Google Scholar
• Quinodoz SA, Ollikainen N, Tabak B, et al. Higher-order inter-chromosomal hubs shape 3D genome organization in the nucleus. Cell. 2018;174:744–57 e24.
   PubMed Web of Science ®Google Scholar
• Lai B, Tang Q, Jin W, et al. Trac-looping measures genome structure and chromatin accessibility. Nat Methods. 2018;15:741–747.
   PubMed Web of Science ®Google Scholar
• Mateo LJ, Murphy SE, Hafner A, et al. Visualizing DNA folding and RNA in embryos at single-cell resolution. Nature. 2019;568:49–54.
   PubMed Web of Science ®Google Scholar
• Zheng M, Tian SZ, Capurso D, et al. Multiplex chromatin interactions with single-molecule precision. Nature. 2019;566:558–562.
   PubMed Web of Science ®Google Scholar
• Finn EH, Pegoraro G, Brandao HB, et al. Extensive heterogeneity and intrinsic variation in spatial genome organization. Cell. 2019;176:1502–15 e10.
   PubMed Web of Science ®Google Scholar
• Osterwalder M, Barozzi I, Tissieres V, et al. Enhancer redundancy provides phenotypic robustness in mammalian development. Nature. 2018;554:239–243.
   PubMed Web of Science ®Google Scholar
• Hay D, Hughes JR, Babbs C, et al. Genetic dissection of the alpha-globin super-enhancer in vivo. Nat Genet. 2016;48:895–903.
   PubMed Web of Science ®Google Scholar
• Whalen S, Truty RM, Pollard KS. Enhancer-promoter interactions are encoded by complex genomic signatures on looping chromatin. Nat Genet. 2016;48:488–496.
   PubMed Web of Science ®Google Scholar
• Cao Q, Anyansi C, Hu X, et al. Reconstruction of enhancer-target networks in 935 samples of human primary cells, tissues and cell lines. Nat Genet. 2017;49:1428–1436.
   PubMed Web of Science ®Google Scholar
• Fulco CP, Munschauer M, Anyoha R, et al. Systematic mapping of functional enhancer-promoter connections with CRISPR interference. Science. 2016;354:769–773.
   PubMed Web of Science ®Google Scholar
• Sanjana NE, Wright J, Zheng K, et al. High-resolution interrogation of functional elements in the noncoding genome. Science. 2016;353:1545–1549.
   PubMed Web of Science ®Google Scholar
• Schmidt F, Kern F, Schulz MH. Integrative prediction of gene expression with chromatin accessibility and conformation data. Epigenetics Chromatin. 2020;13:4.
   PubMed Web of Science ®Google Scholar
• Fulco CP, Nasser J, Jones TR, et al. Activity-by-contact model of enhancer-promoter regulation from thousands of CRISPR perturbations. Nat Genet. 2019;51:1664–1669.
   PubMed Web of Science ®Google Scholar
• Fudenberg G, Abdennur N, Imakaev M, et al. Emerging evidence of chromosome folding by loop extrusion. Cold Spring Harb Symp Quant Biol. 2017;82:45–55.
   PubMedGoogle Scholar
• Sanborn AL, Rao SS, Huang SC, et al. Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. Proc Natl Acad Sci U S A. 2015;112:E6456–65.
   PubMed Web of Science ®Google Scholar
• Fudenberg G, Imakaev M, Lu C, et al. Formation of chromosomal domains by loop extrusion. Cell Rep. 2016;15:2038–2049.
   PubMed Web of Science ®Google Scholar
• Barrington C, Georgopoulou D, Pezic D, et al. Enhancer accessibility and CTCF occupancy underlie asymmetric TAD architecture and cell type specific genome topology. Nat Commun. 2019;10:2908.
   PubMed Web of Science ®Google Scholar
• Nora EP, Goloborodko A, Valton AL, et al. Targeted degradation of CTCF decouples local insulation of chromosome domains from genomic compartmentalization. Cell. 2017;169:930–44 e22.
   PubMed Web of Science ®Google Scholar
• Wutz G, Varnai C, Nagasaka K, et al. Topologically associating domains and chromatin loops depend on cohesin and are regulated by CTCF, WAPL, and PDS5 proteins. Embo J. 2017;36:3573–3599.
   PubMed Web of Science ®Google Scholar
• Busslinger GA, Stocsits RR, van der Lelij P, et al. Cohesin is positioned in mammalian genomes by transcription, CTCF and Wapl. Nature. 2017;544:503–507.
   PubMed Web of Science ®Google Scholar
• Haarhuis JHI, van der Weide RH, Blomen VA, et al. The cohesin release factor WAPL restricts chromatin loop extension. Cell. 2017;169:693–707 e14.
   PubMed Web of Science ®Google Scholar
• Sima J, Chakraborty A, Dileep V, et al. Identifying cis elements for spatiotemporal control of mammalian DNA replication. Cell. 2019;176:816–30 e18.
   PubMed Web of Science ®Google Scholar
• Thiecke MJ, Wutz G, Muhar M, et al. Cohesin-dependent and independent mechanisms support chromosomal contacts between promoters and enhancers. Cell Rep. 2020;21;32(3):107929.
   Google Scholar
• Bintu B, Mateo LJ, Su JH, et al. Super-resolution chromatin tracing reveals domains and cooperative interactions in single cells. Science. 2018:362(6413):eaau1783
   PubMed Web of Science ®Google Scholar
• Hsieh TS, Cattoglio C, Slobodyanyuk E, et al. Resolving the 3D landscape of transcription-linked mammalian chromatin folding. Mol Cell. 2020;78(3):539–553.e8.
   Web of Science ®Google Scholar
• Brackley CA, Johnson J, Michieletto D, et al. Extrusion without a motor: a new take on the loop extrusion model of genome organization. Nucleus. 2018;9:95–103.
   PubMed Web of Science ®Google Scholar
• Marenduzzo D, Finan K, Cook PR. The depletion attraction: an underappreciated force driving cellular organization. J Cell Biol. 2006;175:681–686.
   PubMed Web of Science ®Google Scholar
• Boija A, Klein IA, Sabari BR, et al. Transcription factors activate genes through the phase-separation capacity of their activation domains. Cell. 2018;175:1842–55 e16.
   PubMed Web of Science ®Google Scholar
• Hnisz D, Shrinivas K, Young RA, et al. A phase separation model for transcriptional control. Cell. 2017;169:13–23.
   PubMed Web of Science ®Google Scholar
• Sabari BR, Dall’Agnese A, Boija A, et al. Coactivator condensation at super-enhancers links phase separation and gene control. Science. 2018:361(6400):eaar3958
   PubMed Web of Science ®Google Scholar
• Chong S, Dugast-Darzacq C, Liu Z, et al. Imaging dynamic and selective low-complexity domain interactions that control gene transcription. Science. 2018:361(6400):eaar2555
   Web of Science ®Google Scholar
• Hnisz D, Abraham BJ, Lee TI, et al. Super-enhancers in the control of cell identity and disease. Cell. 2013;155:934–947.
   PubMed Web of Science ®Google Scholar
• Tatavosian R, Kent S, Brown K, et al. Nuclear condensates of the polycomb protein chromobox 2 (CBX2) assemble through phase separation. J Biol Chem. 2019;294:1451–1463.
   PubMed Web of Science ®Google Scholar
• Cho WK, Spille JH, Hecht M, et al. Mediator and RNA polymerase II clusters associate in transcription-dependent condensates. Science. 2018;361:412–415.
   PubMed Web of Science ®Google Scholar
• Zamudio AV, Dall’Agnese A, Henninger JE, et al. Mediator condensates localize signaling factors to key cell identity genes. Mol Cell. 2019;76:753–66 e6.
   PubMed Web of Science ®Google Scholar
• Fox AH, Nakagawa S, Hirose T, et al. Paraspeckles: where long noncoding RNA meets phase separation. Trends Biochem Sci. 2018;43:124–135.
   PubMed Web of Science ®Google Scholar
• Wang L, Gao Y, Zheng X, et al. Histone Modifications regulate chromatin compartmentalization by contributing to a phase separation mechanism. Mol Cell. 2019;76:646–59 e6.
   PubMed Web of Science ®Google Scholar
• Crump NT, Ballabio E, Godfrey L, et al. BET inhibition disrupts transcription but retains enhancer-promoter contact. bioRxiv. 2019;848325.
   Google Scholar
• Dall’Agnese A, Caputo L, Nicoletti C, et al. Transcription factor-directed re-wiring of chromatin architecture for somatic cell nuclear reprogramming toward trans-differentiation. Mol Cell. 2019;76:453–72 e8.
   PubMed Web of Science ®Google Scholar
• Stadhouders R, Filion GJ, Graf T. Transcription factors and 3D genome conformation in cell-fate decisions. Nature. 2019;569:345–354.
   PubMed Web of Science ®Google Scholar
• Kim S, Shendure J. Mechanisms of interplay between transcription factors and the 3D genome. Mol Cell. 2019;76:306–319.
   PubMed Web of Science ®Google Scholar
• Elemento O, Rubin MA, Rickman DS. Oncogenic transcription factors as master regulators of chromatin topology: a new role for ERG in prostate cancer. Cell Cycle. 2012;11:3380–3383.
   PubMed Web of Science ®Google Scholar
• Iborra FJ, Pombo A, Jackson DA, et al. Active RNA polymerases are localized within discrete transcription “factories’ in human nuclei. J Cell Sci. 1996;109(Pt 6):1427–1436.
   PubMedGoogle Scholar
• de Wit E, Bouwman BA, Zhu Y, et al. The pluripotent genome in three dimensions is shaped around pluripotency factors. Nature. 2013;501:227–231.
   PubMed Web of Science ®Google Scholar
• Johanson TM, Lun ATL, Coughlan HD, et al. Transcription-factor-mediated supervision of global genome architecture maintains B cell identity. Nat Immunol. 2018;19:1257–1264.
   PubMed Web of Science ®Google Scholar
• Bertolini JA, Favaro R, Zhu Y, et al. Mapping the global chromatin connectivity network for Sox2 function in neural stem cell maintenance. Cell Stem Cell. 2019;24:462–76 e6.
   PubMed Web of Science ®Google Scholar
• Magli A, Baik J, Pota P, et al. Pax3 cooperates with Ldb1 to direct local chromosome architecture during myogenic lineage specification. Nat Commun. 2019;10:2316.
   PubMed Web of Science ®Google Scholar
• Nitzsche A, Paszkowski-Rogacz M, Matarese F, et al. RAD21 cooperates with pluripotency transcription factors in the maintenance of embryonic stem cell identity. PLoS One. 2011;6:e19470.
   PubMed Web of Science ®Google Scholar
• Vakoc CR, Letting DL, Gheldof N, et al. Proximity among distant regulatory elements at the beta-globin locus requires GATA-1 and FOG-1. Mol Cell. 2005;17:453–462.
   PubMed Web of Science ®Google Scholar
• Beagan JA, Duong MT, Titus KR, et al. YY1 and CTCF orchestrate a 3D chromatin looping switch during early neural lineage commitment. Genome Res. 2017;27:1139–1152.
   PubMed Web of Science ®Google Scholar
• Deng W, Lee J, Wang H, et al. Controlling long-range genomic interactions at a native locus by targeted tethering of a looping factor. Cell. 2012;149:1233–1244.
   PubMed Web of Science ®Google Scholar
• Monahan K, Horta A, Lomvardas S. LHX2- and LDB1-mediated trans interactions regulate olfactory receptor choice. Nature. 2019;565:448–453.
   PubMed Web of Science ®Google Scholar
• Kagey MH, Newman JJ, Bilodeau S, et al. Mediator and cohesin connect gene expression and chromatin architecture. Nature. 2010;467:430–435.
   PubMed Web of Science ®Google Scholar
• Huang D, Wei Z, Lu W. Genome organization by Klf4 regulates transcription in pluripotent stem cells. Cell Cycle. 2013;12:3351–3352.
   PubMed Web of Science ®Google Scholar
• Hansen AS, Hsieh TS, Cattoglio C, et al. Distinct classes of chromatin loops revealed by deletion of an RNA-binding region in CTCF. Mol Cell. 2019;76:395–411 e13.
   PubMed Web of Science ®Google Scholar
• Yin Y, Morgunova E, Jolma A, et al. Impact of cytosine methylation on DNA binding specificities of human transcription factors. Science. 2017;356(6337):eaaj2239.
   Web of Science ®Google Scholar
• Zhu F, Farnung L, Kaasinen E, et al. The interaction landscape between transcription factors and the nucleosome. Nature. 2018;562:76–81.
   PubMed Web of Science ®Google Scholar
• Schoenfelder S, Sugar R, Dimond A, et al. Polycomb repressive complex PRC1 spatially constrains the mouse embryonic stem cell genome. Nat Genet. 2015;47:1179–1186.
   PubMed Web of Science ®Google Scholar
• Cuartero S, Weiss FD, Dharmalingam G, et al. Control of inducible gene expression links cohesin to hematopoietic progenitor self-renewal and differentiation. Nat Immunol. 2018;19:932–941.
   PubMed Web of Science ®Google Scholar
• Ferrari F, Apostolou E, Park PJ, et al. Rearranging the chromatin for pluripotency. Cell Cycle. 2014;13:167–168.
   PubMed Web of Science ®Google Scholar
• Hu JF, Hoffman AR. Chromatin looping is needed for iPSC induction. Cell Cycle. 2014;13:1–2.
   PubMed Web of Science ®Google Scholar
• Teves SS, An L, Hansen AS, et al. A dynamic mode of mitotic bookmarking by transcription factors. Elife. 2016:5:e22280.
   PubMed Web of Science ®Google Scholar
• Festuccia N, Gonzalez I, Owens N, et al. Mitotic bookmarking in development and stem cells. Development. 2017;144:3633–3645.
   PubMed Web of Science ®Google Scholar
• Zhang H, Emerson DJ, Gilgenast TG, et al. Chromatin structure dynamics during the mitosis-to-G1 phase transition. Nature. 2019;576:158–162.
   PubMed Web of Science ®Google Scholar
• Abramo K, Valton AL, Venev SV, et al. A chromosome folding intermediate at the condensin-to-cohesin transition during telophase. Nat Cell Biol. 2019;21:1393–1402.
   PubMed Web of Science ®Google Scholar
• Hsiung CC, Bartman CR, Huang P, et al. A hyperactive transcriptional state marks genome reactivation at the mitosis-G1 transition. Genes Dev. 2016;30:1423–1439.
   PubMed Web of Science ®Google Scholar
• Viny AD, Bowman RL, Liu Y, et al. Cohesin members stag1 and stag2 display distinct roles in chromatin accessibility and topological control of hsc self-renewal and differentiation. Cell Stem Cell. 2019;25:682–96 e8.
   PubMed Web of Science ®Google Scholar
• Flavahan WA, Drier Y, Liau BB, et al. Insulator dysfunction and oncogene activation in IDH mutant gliomas. Nature. 2016;529:110–114.
   PubMed Web of Science ®Google Scholar
• Chen X, Zhang M, Gan H, et al. A novel enhancer regulates MGMT expression and promotes temozolomide resistance in glioblastoma. Nat Commun. 2018;9:2949.
   PubMed Web of Science ®Google Scholar
• Sur I, Taipale J. The role of enhancers in cancer. Nat Rev Cancer. 2016;16:483–493.
   PubMed Web of Science ®Google Scholar
• Morton AR, Dogan-Artun N, Faber ZJ, et al. Functional enhancers shape extrachromosomal oncogene amplifications. Cell. 2019;179:1330–41 e13.
   PubMed Web of Science ®Google Scholar
• He Y, Long W, Liu Q. Targeting super-enhancers as a therapeutic strategy for cancer treatment. Front Pharmacol. 2019;10:361.
   PubMed Web of Science ®Google Scholar
• Sengupta S, George RE. Super-enhancer-driven transcriptional dependencies in cancer. Trends Cancer. 2017;3:269–281.
   PubMed Web of Science ®Google Scholar
• Lupianez DG, Kraft K, Heinrich V, et al. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell. 2015;161:1012–1025.
   PubMed Web of Science ®Google Scholar
• Li X, Shi L, Wang Y, et al. OncoBase: a platform for decoding regulatory somatic mutations in human cancers. Nucleic Acids Res. 2019;47:D1044–D55.
   PubMed Web of Science ®Google Scholar
• Song M, Yang X, Ren X, et al. Mapping cis-regulatory chromatin contacts in neural cells links neuropsychiatric disorder risk variants to target genes. Nat Genet. 2019;51:1252–1262.
   PubMed Web of Science ®Google Scholar
• Kikuchi M, Hara N, Hasegawa M, et al. Enhancer variants associated with Alzheimer’s disease affect gene expression via chromatin looping. BMC Med Genomics. 2019;12:128.
   PubMed Web of Science ®Google Scholar
• Hung V, Udeshi ND, Lam SS, et al. Spatially resolved proteomic mapping in living cells with the engineered peroxidase APEX2. Nat Protoc. 2016;11:456–475.
   PubMed Web of Science ®Google Scholar
• Dekker J, Rippe K, Dekker M, et al. Capturing chromosome conformation. Science. 2002;295:1306–1311.
   PubMed Web of Science ®Google Scholar