Abstract
The hypothesis that the genome is composed of a patchwork of structural and functional domains (units) that may be either active or repressed was proposed almost 30 years ago. Here, we examine the evolution of the domain model of eukaryotic genome organization in view of the expansion of genome-scale techniques in the twenty-first century that have provided us with a wealth of information on genome organization, folding, and functioning.
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References
Adolph KW, Chang SM, Laemmli UK (1977) Role of nonhistone proteins in metaphase chromosomes structure. Cell 12:805–816. doi:10.1016/0092-8674(77)90279-3
Alipour E, Marko JF (2012) Self-organization of domain structures by DNA-loop-extruding enzymes. Nucleic Acids Res 40:11202–11212. doi:10.1093/nar/gks925
Allahverdi A, Yang R, Korolev N, Fan Y, Davey CA, Liu CF, Nordenskiold L (2011) The effects of histone H4 tail acetylations on cation-induced chromatin folding and self-association. Nucleic Acids Res 39:1680–1691. doi:10.1093/nar/gkq900
Arnold CD, Gerlach D, Stelzer C, Boryn LM, Rath M, Stark A (2013) Genome-wide quantitative enhancer activity maps identified by STARR-seq. Science 339:1074–1077. doi:10.1126/science.1232542
Arya G, Schlick T (2006) Role of histone tails in chromatin folding revealed by a mesoscopic oligonucleosome model. Proc Natl Acad Sci U S A 103:16236–16241. doi:10.1073/pnas.0604817103
Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifications. Cell Res 21:381–395. doi:10.1038/cr.2011.22
Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, Kouzarides T (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410:120–124. doi:10.1038/35065138
Bau D et al (2011) The three-dimensional folding of the alpha-globin gene domain reveals formation of chromatin globules. Nat Struct Mol Biol 18:107–114. doi:10.1038/nsmb.1936
Belton JM, McCord RP, Gibcus JH, Naumova N, Zhan Y, Dekker J (2012) Hi-C: a comprehensive technique to capture the conformation of genomes. Methods 58:268–276. doi:10.1016/j.ymeth.2012.05.001
Benyajati C, Worcel A (1976) Isolation, characterization, and structure of the folded interphase genome of Drosophila melanogaster. Cell 9:393–407. doi:10.1016/0092-8674(76)90084-2
Berlivet S, Paquette D, Dumouchel A, Langlais D, Dostie J, Kmita M (2013) Clustering of tissue-specific sub-TADs accompanies the regulation of HoxA genes in developing limbs. PLoS Genet 9:e1004018. doi:10.1371/journal.pgen.1004018
Bickmore WA (2013) The spatial organization of the human genome. Annu Rev Genomics HumGenet 14:67–84. doi:10.1146/annurev-genom-091212-153515
Bickmore WA, van Steensel B (2013) Genome architecture: domain organization of interphase chromosomes. Cell 152:1270–1284. doi:10.1016/j.cell.2013.02.001
Blacketer MJ, Feely SJ, Shogren-Knaak MA (2010) Nucleosome interactions and stability in an ordered nucleosome array model system. J Biol Chem 285:34597–34607. doi:10.1074/jbc.M110.140061
Bodnar JW (1988) A domain model for eukaryotic DNA organization: a molecular basis for cell differentiation and chromosome evolution. J Theor Biol 132:479–507
Boutanaev AM, Kalmykova AI, Shevelyov YY, Nurminsky DI (2002) Large clusters of co-expressed genes in the Drosophila genome. Nature 420:666–669. doi:10.1038/nature01216
Bulger M et al (2000) Comparative structural and functional analysis of the olfactory receptor genes flanking the human and mouse b-globin gene clusters. Proc Natl Acad Sci U S A 97:14560–14565. doi:10.1073/pnas.97.26.14560
Caron H et al (2001) The human transcriptome map: clustering of highly expressed genes in chromosomal domains. Science 291:1289–1292. doi:10.1126/science.1056794
Chen HS, Martin KA, Lu F, Lupey LN, Mueller JM, Lieberman PM, Tempera I (2014) Epigenetic deregulation of the LMP1/LMP2 locus of Epstein-Barr virus by mutation of a single CTCF-cohesin binding site. J Virol 88:1703–1713. doi:10.1128/JVI.02209-13
Chen RA et al (2013) The landscape of RNA polymerase II transcription initiation in C. elegans reveals promoter and enhancer architectures. Genome Res 23:1339–1347. doi:10.1101/gr.153668.112
Chong S, Riggs AD, Bonifer C (2002) The chicken lysozyme chromatin domain contains a second, widely expressed gene. Nucl Acids Res 30:463–467. doi:10.1093/nar/30.2.463
Ciejek EM, Tsai M-J, O'Malley BW (1983) Actively transcribed genes are associated with the nuclear matrix. Nature 306:607–609
Cockerill PN (2011) Structure and function of active chromatin and DNase I hypersensitive sites. FEBS J 278:2182–2210. doi:10.1111/j.1742-4658.2011.08128.x
Cockerill PN, Garrard WT (1986) Chromosomal loop anchorage of the kappa immunoglobulin gene occurs next to the enhancer in a region containing topoisomerase II sites. Cell 44:273–282. doi:10.1016/0092-8674(86)90761-0
Consortium EP, Bernstein BE, Birney E, Dunham I, Green ED, Gunter C, Snyder M (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489:57–74. doi:10.1038/nature11247
Cook PR, Brazell IA, Jost E (1976) Characterization of nuclear structures containing superhelical DNA. J Cell Sci 22:303–324
Cook PR, Lang J, Hayday A, L. L, Fried M, Chiswell DJ, Wyke A (1982) Active viral genes in transformed cells lie close to the nuclear cage. EMBO J 1:447–452
Craddock CF, Vyas P, Sharpe JA, Ayyub H, Wood WG, Higgs DR (1995) Contrasting effects of alpha and beta globin regulatory elements on chromatin structure may be related to their different chromosomal environments. EMBO J 14:1718–1726
Cremer T, Cremer C (2001) Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet 2:292–301. doi:10.1038/35066075
de Laat W, Grosveld F (2003) Spatial organization of gene expression: the active chromatin hub. Chromosome Res 11:447–459
de Wit E, de Laat W (2012) A decade of 3C technologies: insights into nuclear organization. Genes Dev 26:11–24. doi:10.1101/gad.179804.111
Dekker J, Mirny L (2016) The 3D genome as moderator of chromosomal communication. Cell 164:1110–1121. doi:10.1016/j.cell.2016.02.007
Dekker J, Rippe K, Dekker M, Kleckner N (2002) Capturing chromosome conformation. Science 295:1306–1311. doi:10.1126/science.1067799
Dileep V, Ay F, Sima J, Vera DL, Noble WS, Gilbert DM (2015a) Topologically associating domains and their long-range contacts are established during early G1 coincident with the establishment of the replication-timing program. Genome Res 25:1104–1113. doi:10.1101/gr.183699.114
Dileep V, Rivera-Mulia JC, Sima J, Gilbert DM (2015b) Large-scale chromatin structure-function relationships during the cell cycle and development: insights from replication timing. Cold Spring Harb Symp Quant Biol. doi:10.1101/sqb.2015.80.027284
Dillon N, Sabbatini P (2000) Functional gene expression domains: defining the functional units of eukaryotic gene regulation. BioEssays 22:657–665. doi:10.1002/1521-1878(200007)22:7<657::AID-BIES8>3.0.CO;2-2
Dixon JR et al (2015) Chromatin architecture reorganization during stem cell differentiation. Nature 518:331–336. doi:10.1038/nature14222
Dixon JR et al (2012) Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485:376–380. doi:10.1038/nature11082
Eberharter A, Becker PB (2002) Histone acetylation: a switch between repressive and permissive chromatin. Second in review series on chromatin dynamics. EMBO Rep 3:224–229. doi:10.1093/embo-reports/kvf053
Fabre PJ, Benke A, Joye E, Nguyen Huynh TH, Manley S, Duboule D (2015) Nanoscale spatial organization of the HoxD gene cluster in distinct transcriptional states. Proc Natl Acad Sci U S A 112:13964–13969. doi:10.1073/pnas.1517972112
Fanucchi S, Shibayama Y, Burd S, Weinberg MS, Mhlanga MM (2013) Chromosomal contact permits transcription between coregulated genes. Cell 155:606–620. doi:10.1016/j.cell.2013.09.051
Farkash-Amar S, Simon I (2010) Genome-wide analysis of the replication program in mammals. Chromosome Res 18:115–125. doi:10.1007/s10577-009-9091-5
Filion GJ et al (2010) Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143:212–224. doi:10.1016/j.cell.2010.09.009
Filippova D, Patro R, Duggal G, Kingsford C (2014) Identification of alternative topological domains in chromatin. Algorithms Mol Biol AMB 9:14. doi:10.1186/1748-7188-9-14
Forrester WC, Epner E, Driscoll MC, Enver T, Brice M, Papayannopoulou T, Groudine M (1990) A deletion of the human b-globin locus activation region causes a major alteration in chromatin structure and replication across the entire b-globin locus. Gene Dev 4:1637–1649. doi:10.1101/gad.4.10.1637
Forrester WC, Takegawa S, Papayannopoulou T, Stamatoyannopoulos G, Groudine M (1987) Evidence for a locus activating region: the formation of developmentally stable hypersensitive sites in globin expressing hybrids. Nucleic Acids Res 15:10159–10175. doi:10.1093/nar/15.24.10159
Forsberg EC, Bresnick EH (2001) Histone acetylation beyond promoters: long-range acetylation patterns in the chromatin world. BioEssays 23:820–830. doi:10.1002/bies.1117
Forsberg EC, Downs KM, Christensen HM, Im H, Nuzzi PA, Bresnick EH (2000) Developmentally dynamic histone acetylation pattern of a tissue-specific chromatin domain. Proc Natl Acad Sci U S A 97:14494–14499. doi:10.1073/pnas.97.26.14494
Fraser J et al. (2015) Hierarchical folding and reorganization of chromosomes are linked to transcriptional changes in cellular differentiation. Mol Syst Biol 11:852. doi:10.15252/msb.20156492
Fudenberg G, Imakaev M, Lu C, Goloborodko A, Abdennur N, Mirny LA (2015) Formation of chromosomal domains by loop extrusion BioRxiv doi:10.1101/024620
Garel A, Axel R (1976) Selective digestion of transcriptionally active ovalbumin genes from oviduct nuclei. Proc Natl Acad Sci U S A 73:3966–3970
Gavrilov AA, Razin SV (2008) Spatial configuration of the chicken {alpha}-globin gene domain: immature and active chromatin hubs. Nucleic Acids Res 36:4629–4640. doi:10.1093/nar/gkp838
Gibcus JH, Dekker J (2013) The hierarchy of the 3D genome. Mol Cell 49:773–782. doi:10.1016/j.molcel.2013.02.011
Gilbert DM (2002) Replication timing and transcriptional control: beyond cause and effect. Curr Opin Cell Biol 14:377–383. doi:10.1016/S0955-0674(02)00326-5
Goldman MA (1988) The chromatin domain as a unit of gene regulation. BioEssays 9:50–55. doi:10.1002/bies.950090204
Grosveld F, van Assandelt GB, Greaves DR, Kollias B (1987) Position-independent, high-level expression of the human b-globin gene in transgenic mice. Cell 51:975–985. doi:10.1016/0092-8674(87)90584-8
Guelen L et al (2008) Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 453:948–951. doi:10.1038/nature06947
Hansen JC (2002) Conformational dynamics of the chromatin fiber in solution: determinants, mechanisms, and functions. Annu Rev Biophys Biomol Struct 31:361–392. doi:10.1146/annurev.biophys.31.101101.140858
Hebbes TR, Clayton AL, Thorne AW, Crane-Robinson C (1994) Core histone hyperacetylation co-maps with generalized DNase I sensitivity in the chicken beta-globin chromosomal domain. EMBO J 13:1823–1830
Hebbes TR, Thorne AW, Crane-Robinson C (1988) A direct link between core histone acetylation and transcriptionally active chromatin. EMBO J 7:1395–1402
Heintzman ND et al (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459:108–112. doi:10.1038/nature07829
Hou C, Li L, Qin ZS, Corces VG (2012) Gene density, transcription, and insulators contribute to the partition of the Drosophila genome into physical domains. Mol Cell 48:471–484. doi:10.1016/j.molcel.2012.08.031
Hsieh TH, Weiner A, Lajoie B, Dekker J, Friedman N, Rando OJ (2015) Mapping nucleosome resolution chromosome folding in yeast by micro-C. Cell 162:108–119. doi:10.1016/j.cell.2015.05.048
Ibn-Salem J et al (2014) Deletions of chromosomal regulatory boundaries are associated with congenital disease. Genome Biol 15:423. doi:10.1186/s13059-014-0423-1
Jantzen K, Friton HP, Igo-Kimenes T (1986) The DNase I sensitive domain of the chicken lyzozyme gene spans 24 kb. Nucleic Acids Res 14:6085–6099. doi:10.1093/nar/14.15.6085
Jarman AP, Wood WG, Sharpe JA, Gourdon G, Ayyub H, Higgs DR (1991) Characterization of the major regulatory element upstream of the human a-globin gene cluster. Mol Cell Biol 11:4679–4689. doi:10.1128/MCB.11.9.4679
Ji X et al (2016) 3D chromosome regulatory landscape of human pluripotent cells. Cell Stem Cell 18:262–275. doi:10.1016/j.stem.2015.11.007
Julienne H, Zoufir A, Audit B, Arneodo A (2013) Human genome replication proceeds through four chromatin states. PLoS Comput Biol 9, e1003233. doi:10.1371/journal.pcbi.1003233
Kalashnikova AA, Porter-Goff ME, Muthurajan UM, Luger K, Hansen JC (2013) The role of the nucleosome acidic patch in modulating higher order chromatin structure. J R Soc Interface R Soc 10:20121022. doi:10.1098/rsif.2012.1022
Kang J, Xu B, Yao Y, Lin W, Hennessy C, Fraser P, Feng J (2011) A dynamical model reveals gene co-localizations in nucleus. PLoS Comput Biol 7:e1002094. doi:10.1371/journal.pcbi.1002094
Kawamura R, Tanabe H, Wada T, Saitoh S, Fukushima Y, Wakui K (2012) Visualization of the spatial positioning of the SNRPN, UBE3A, and GABRB3 genes in the normal human nucleus by three-color 3D fluorescence in situ hybridization. Chromosome Res 20:659–672. doi:10.1007/s10577-012-9300-5
Kellum R, Schedl P (1991) A position-effect assay for boundaries of higher-order chromosomal domains. Cell 64:941–950. doi:10.1016/0092-8674(91)90318-S
Kellum R, Schedl P (1992) A group of scs elements function as boundaries in enhancer-blocking assay. Mol Cell Biol 12:2424–2431. doi:10.1128/MCB.12.5.2424
Kharchenko PV et al (2011) Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471:480–485. doi:10.1038/nature09725
Kind J et al (2013) Single-cell dynamics of genome-nuclear lamina interactions. Cell 153:178–192. doi:10.1016/j.cell.2013.02.028
Kind J, van Steensel B (2010) Genome-nuclear lamina interactions and gene regulation. Curr Opin Cell Biol 22:320–325. doi:10.1016/j.ceb.2010.04.002
Kozubek S et al (2002) 3D Structure of the human genome: order in randomness. Chromosoma 111:321–331. doi:10.1007/s00412-002-0210-8
Krajewski WA, Becker PB (1998) Reconstitution of hyperacetylated, DNase I-sensitive chromatin characterized by high conformational flexibility of nucleosomal DNA. Proc Natl Acad Sci U S A 95:1540–1545
Lawson GM, Knoll BJ, March CJ, Woo SLC, Tsai M-J, O'Malley BW (1982) Definition of 5' and 3' structural boundaries of the chromatin domain containing the ovalbumin multigene family. J Biol Chem 257:1501–1507
Le Dily F et al (2014) Distinct structural transitions of chromatin topological domains correlate with coordinated hormone-induced gene regulation. Genes Dev 28:2151–2162. doi:10.1101/gad.241422.114
Le Dily F, Beato M (2015) TADs as modular and dynamic units for gene regulation by hormones. FEBS Lett 589:2885–2892. doi:10.1016/j.febslet.2015.05.026
Letourneau A et al (2014) Domains of genome-wide gene expression dysregulation in Down's syndrome. Nature 508:345–350. doi:10.1038/nature13200
Li L et al (2015) Widespread rearrangement of 3D chromatin organization underlies polycomb-mediated stress-induced silencing. Mol Cell 58:216–231. doi:10.1016/j.molcel.2015.02.023
Li Q, Zhou B, Powers P, Enver T, Stamatoyannopoulos G (1990) Beta-globin locus activations regions: conservation of organization, structure and function. Proc Natl Acad Sci U S A 87:8207–8211
Lieberman-Aiden E et al (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289–293. doi:10.1126/science.1181369
Lonfat N, Duboule D (2015) Structure, function and evolution of topologically associating domains (TADs) at HOX loci. FEBS Lett 589:2869–2876. doi:10.1016/j.febslet.2015.04.024
Lonfat N, Montavon T, Darbellay F, Gitto S, Duboule D (2014) Convergent evolution of complex regulatory landscapes and pleiotropy at Hox loci. Science 346:1004–1006. doi:10.1126/science.1257493
Lupianez DG et al (2015) Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161:1012–1025. doi:10.1016/j.cell.2015.04.004
Lupianez DG, Spielmann M, Mundlos S (2016) Breaking TADs: how alterations of chromatin domains result in disease. Trends Genet 32:225–237. doi:10.1016/j.tig.2016.01.003
Maeshima K et al. (2016) Nucleosomal arrays self-assemble into supramolecular globular structures lacking 30-nm fibers. EMBO J doi:10.15252/embj.201592660
Marinic M, Aktas T, Ruf S, Spitz F (2013) An integrated holo-enhancer unit defines tissue and gene specificity of the Fgf8 regulatory landscape. Dev Cell 24:530–542. doi:10.1016/j.devcel.2013.01.025
Markaki Y et al (2010) Functional nuclear organization of transcription and DNA replication: a topographical marriage between chromatin domains and the interchromatin compartment. Cold Spring Harb Symp Quant Biol 75:475–492. doi:10.1101/sqb.2010.75.042
Matharu N, Ahituv N (2015) Minor loops in major folds: enhancer-promoter looping, chromatin restructuring, and their association with transcriptional regulation and disease. PLoS Genet 11:e1005640. doi:10.1371/journal.pgen.1005640
Meuleman W et al (2013) Constitutive nuclear lamina-genome interactions are highly conserved and associated with A/T-rich sequence. Genome Res 23:270–280. doi:10.1101/gr.141028.112
Mifsud B et al (2015) Mapping long-range promoter contacts in human cells with high-resolution capture Hi-C. Nat Genet 47:598–606. doi:10.1038/ng.3286
Mijalski T et al (2005) Identification of coexpressed gene clusters in a comparative analysis of transcriptome and proteome in mouse tissues. Proc Natl Acad Sci U S A 102:8621–8626. doi:10.1073/pnas.0407672102
Milon B et al (2014) Map of open and closed chromatin domains in Drosophila genome. BMC Genomics 15:988. doi:10.1186/1471-2164-15-988
Mirkovitch J, Mirault M-E, Laemmli UK (1984) Organization of the higher-order chromatin loop: specific DNA attachment sites on nuclear scaffold. Cell 39:223–232. doi:10.1016/0092-8674(84)90208-3
Montavon T et al (2011) A regulatory archipelago controls Hox genes transcription in digits. Cell 147:1132–1145. doi:10.1016/j.cell.2011.10.023
Nagano T et al (2013) Single-cell Hi-C reveals cell-to-cell variability in chromosome structure. Nature 502:59–64. doi:10.1038/nature12593
Nora EP et al (2012) Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485:381–385. doi:10.1038/nature11049
Papantonis A, Larkin JD, Wada Y, Ohta Y, Ihara S, Kodama T, Cook PR (2010) Active RNA polymerases: mobile or immobile molecular machines? PLoS Biol 8, e1000419. doi:10.1371/journal.pbio.1000419
Pepenella S, Murphy KJ, Hayes JJ (2014) Intra- and inter-nucleosome interactions of the core histone tail domains in higher-order chromatin structure. Chromosoma 123:3–13. doi:10.1007/s00412-013-0435-8
Petrov A, Allinne J, Pirozhkova I, Laoudj D, Lipinski M, Vassetzky YS (2008) A nuclear matrix attachment site in the 4q35 locus has an enhancer-blocking activity in vivo: implications for the facio-scapulo-humeral dystrophy. Genome Res 18:39–45. doi:10.1101/gr.6620908
Petrov A, Pirozhkova I, Carnac G, Laoudj D, Lipinski M, Vassetzky YS (2006) Chromatin loop domain organization within the 4q35 locus in facioscapulohumeral dystrophy patients versus normal human myoblasts. Proc Natl Acad Sci U S A 103:6982–6987. doi:10.1073/pnas.0511235103
Philonenko ES, Klochkov DB, Borunova VV, Gavrilov AA, Razin SV, Iarovaia OV (2009) TMEM8—a non-globin gene entrapped in the globin web. Nucleic Acids Res 37:7394–7406. doi:10.1093/nar/gkp838
Pombo A, Dillon N (2015) Three-dimensional genome architecture: players and mechanisms. Nat Rev Mol Cell Biol 16:245–257. doi:10.1038/nrm3965
Pope BD et al (2014) Topologically associating domains are stable units of replication-timing regulation. Nature 515:402–405. doi:10.1038/nature13986
Rao SS et al (2014) A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159:1665–1680. doi:10.1016/j.cell.2014.11.021
Razin SV, Farrell CM, Recillas-Targa F (2003) Genomic domains and regulatory elements operating at the domain level. Int Rev Cytol 226:63–125
Razin SV, Gavrilov AA (2014) Chromatin without the 30-nm fiber: constrained disorder instead of hierarchical folding. Epigenetics 9:653–657. doi:10.4161/epi.28297
Razin SV, Gavrilov AA, Ioudinkova ES, Iarovaia OV (2013) Communication of genome regulatory elements in a folded chromosome. FEBS Lett 587:1840–1847. doi:10.1016/j.febslet.2013.04.027
Razin SV, Gromova II, Iarovaia OV (1995) Specificity and functional significance of DNA interaction with the nuclear matrix: New approaches to clarify the old questions. Int Rev Cytol 162B:405–448
Razin SV et al (2007) Chromatin domains and regulation of transcription. J Mol Biol 369:597–607. doi:10.1016/j.jmb.2007.04.003
Remeseiro S, Hornblad A, Spitz F (2015) Gene regulation during development in the light of topologically associating domains. Wiley Interdiscip Rev Dev Biol. doi:10.1002/wdev.218
Rowley MJ, Corces VG (2016) The three-dimensional genome: principles and roles of long-distance interactions. Curr Opin Cell Biol 40:8–14. doi:10.1016/j.ceb.2016.01.009
Sanborn AL et al (2015) Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. Proc Natl Acad Sci U S A 112:E6456–6465. doi:10.1073/pnas.1518552112
Schalch T, Duda S, Sargent DF, Richmond TJ (2005) X-ray structure of a tetranucleosome and its implications for the chromatin fibre. Nature 436:138–141. doi:10.1038/nature03686
Schoenfelder S et al (2010) Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat Genet 42:53–61. doi:10.1038/ng.496
Schubeler D, Francastel C, Cimbora DM, Reik A, Martin DI, Groudine M (2000) Nuclear localization and histone acetilation: a pathway for chromatin opening and transcription activation of the human b-globin locus. Gen Dev 14:940–950. doi:10.1101/gad.14.8.940
Sexton T, Cavalli G (2015) The role of chromosome domains in shaping the functional genome. Cell 160:1049–1059. doi:10.1016/j.cell.2015.02.040
Sexton T et al (2012) Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148:458–472. doi:10.1016/j.cell.2012.01.010
Shogren-Knaak M, Ishii H, Sun JM, Pazin MJ, Davie JR, Peterson CL (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311:844–847. doi:10.1126/science.1124000
Sinha D, Shogren-Knaak MA (2010) Role of direct interactions between the histone H4 Tail and the H2A core in long range nucleosome contacts. J Biol Chem 285:16572–16581. doi:10.1074/jbc.M109.091298
Small D, Vogelstein B (1985) The anatomy of supercoiled loops in the Drosophila 7F locus. Nucl Acids Res 13
Smeets D et al (2014) Three-dimensional super-resolution microscopy of the inactive X chromosome territory reveals a collapse of its active nuclear compartment harboring distinct Xist RNA foci. Epigenetics Chromatin 7:8. doi:10.1186/1756-8935-7-8
Spellman PT, Rubin GM (2002) Evidence for large domains of similarly expressed genes in the Drosophila genome. J Biol 1:5. doi:10.1186/1475-4924-1-5
Spitz F, Gonzalez F, Duboule D (2003) A global control region defines a chromosomal regulatory landscape containing the HoxD cluster. Cell 113:405–417. doi:10.1016/S0092-8674(03)00310-6
Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41–45. doi:10.1038/47412
Symmons O, Spitz F (2013) From remote enhancers to gene regulation: charting the genome's regulatory landscapes. Philos Trans R Soc Lond B Biol Sci 368:20120358. doi:10.1098/rstb.2012.0358
Symmons O et al (2014) Functional and topological characteristics of mammalian regulatory domains. Genome Res 24:390–400. doi:10.1101/gr.163519.113
Tang Z et al (2015) CTCF-mediated human 3D genome architecture reveals chromatin topology for transcription. Cell 163:1611–1627. doi:10.1016/j.cell.2015.11.024
Tempera I, Klichinsky M, Lieberman PM (2011) EBV latency types adopt alternative chromatin conformations. PLoS Pathog 7:e1002180. doi:10.1371/journal.ppat.1002180
Tolhuis B, de Wit E, Muijrers I, Teunissen H, Talhout W, van Steensel B, van Lohuizen M (2006) Genome-wide profiling of PRC1 and PRC2 polycomb chromatin binding in Drosophila melanogaster. Nat Genet 38:694–699. doi:10.1038/ng1792
Tolhuis B, Palstra RJ, Splinter E, Grosveld F, de Laat W (2002) Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol Cell 10:1453–1465. doi:10.1016/S1097-2765(02)00781-5
Udvardy A, Schedl P, Sander M, Hsieh T-S (1986) Topoisomerase II cleavage in chromatin. J Mol Biol 191:231–246. doi:10.1016/0022-2836(86)90260-3
Ulianov SV, Gavrilov AA, Razin SV (2012) Spatial organization of the chicken beta-globin gene domain in erythroid cells of embryonic and adult lineages. Epigenetics Chromatin 5:16. doi:10.1186/1756-8935-5-16
Ulianov SV, Gavrilov AA, Razin SV (2015a) Nuclear compartments, genome folding, and enhancer-promoter communication. Int Rev Cell Mol Biol 315:183–244. doi:10.1016/bs.ircmb.2014.11.004
Ulianov SV et al (2015b) Active chromatin and transcription play a key role in chromosome partitioning into topologically associating domains. Genome Res 26:70–84. doi:10.1101/gr.196006.115
Vietri Rudan M, Barrington C, Henderson S, Ernst C, Odom DT, Tanay A, Hadjur S (2015) Comparative Hi-C reveals that CTCF underlies evolution of chromosomal domain architecture. Cell Rep 10:1297–1309. doi:10.1016/j.celrep.2015.02.004
Vyas P, Vickers MA, Simmons DL, Ayyub H, Craddock CF, Higgs DR (1992) cis-acting sequences regulating expression of the human a-globin cluster lie within constitutively open chromatin. Cell 69:781–793. doi:10.1016/0092-8674(92)90290-S
Vyas P, Vickers MA, Picketts DJ, Higgs DR (1995) Conservation of position and sequence of a novel, widely expressed gene containing the major human alpha-globin regulatory element. Genomics 29:679–689. doi:10.1006/geno.1995.9951
Weinreb C, Raphael BJ (2015) Identification of hierarchical chromatin domains. Bioinformatics. doi:10.1093/bioinformatics/btv485
Weintraub H, Groudine M (1976) Chromosomal subunits in active genes have an altered conformation. Science 73:848–856. doi:10.1126/science.948749
Weintraub H, Larsen A, Groudine M (1981) Alpha-Globin-gene switching during the development of chicken embryos: expression and chromosome structure. Cell 24:333–344. doi:10.1016/0092-8674(81)90323-8
Wen B, Wu H, Shinkai Y, Irizarry RA, Feinberg AP (2009) Large histone H3 lysine 9 dimethylated chromatin blocks distinguish differentiated from embryonic stem cells. Nat Genet 41:246–250. doi:10.1038/ng.297
Zhang Y et al (2012) Spatial organization of the mouse genome and its role in recurrent chromosomal translocations. Cell 148:908–21. doi:10.1016/j.cell.2012.02.002
Zhu Y et al (2016) Constructing 3D interaction maps from 1D epigenomes. Nat Commun 7:10812. doi:10.1038/ncomms10812
Zuniga A et al (2004) Mouse limb deformity mutations disrupt a global control region within the large regulatory landscape required for Gremlin expression. Genes Dev 18:1553–1564. doi:10.1101/gad.299904
Acknowledgments
We thank Ms. Shirmoné Botha for critical reading of the manuscript. This work was supported by the Russian Science Foundation (grant no. 14-24-00022).
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The study was approved by the ethics committee of the Institute of Gene Biology, Moscow, Russia.
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An erratum to this article is available at http://dx.doi.org/10.1007/s00412-016-0623-4.
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Razin, S.V., Vassetzky, Y.S. 3D genomics imposes evolution of the domain model of eukaryotic genome organization. Chromosoma 126, 59–69 (2017). https://doi.org/10.1007/s00412-016-0604-7
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DOI: https://doi.org/10.1007/s00412-016-0604-7