Chromatin dynamics at DNA breaks: what, how and why?

Théo Lebeaupin; Hafida Sellou; Gyula Timinszky; Sébastien Huet; Théo Lebeaupin; Hafida Sellou; Gyula Timinszky; Sébastien Huet

doi:10.3934/biophy.2015.4.458

AIMS Biophysics

2015, Volume 2, Issue 4: 458-475. doi: 10.3934/biophy.2015.4.458

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Review Special Issues

Chromatin dynamics at DNA breaks: what, how and why?

1.
CNRS, UMR 6290, Institut Génétique et Développement de Rennes, Rennes, France
2.
Université de Rennes 1, Structure fédérative de recherche Biosit, Rennes, France
3.
Department of Physiological Chemistry, Adolf Butenandt Institute, Ludwig-Maximilians-Universität München, Munich, Germany

Received: 15 July 2015 Accepted: 06 September 2015 Published: 10 September 2015

Chromatin has a complex, dynamic architecture in the interphase nucleus, which regulates the accessibility of the underlying DNA and plays a key regulatory role in all the cellular functions using DNA as a template, such as replication, transcription or DNA damage repair. Here, we review the recent progresses in the understanding of the interplay between chromatin architecture and DNA repair mechanisms. Several reports based on live cell fluorescence imaging show that the activation of the DNA repair machinery is associated with major changes in the compaction state and the mobility of chromatin. We discuss the functional consequences of these changes in yeast and mammals in the light of the different repair pathways utilized by these organisms. In the final section of this review, we show how future developments in high-resolution light microscopy and chromatin modelling by polymer physics should contribute to a better understanding of the relationship between the structural changes in chromatin and the activity of the repair processes.
- chromatin,
- nucleus,
- DNA repair,
- double strand break,
- homologous recombination,
- non-homologous end joining,
- fluorescence microscopy,
- single particle tracking,
- anomalous diffusion,
- polymer physics
Citation: Théo Lebeaupin, Hafida Sellou, Gyula Timinszky, Sébastien Huet. Chromatin dynamics at DNA breaks: what, how and why?[J]. AIMS Biophysics, 2015, 2(4): 458-475. doi: 10.3934/biophy.2015.4.458

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Abstract

Chromatin has a complex, dynamic architecture in the interphase nucleus, which regulates the accessibility of the underlying DNA and plays a key regulatory role in all the cellular functions using DNA as a template, such as replication, transcription or DNA damage repair. Here, we review the recent progresses in the understanding of the interplay between chromatin architecture and DNA repair mechanisms. Several reports based on live cell fluorescence imaging show that the activation of the DNA repair machinery is associated with major changes in the compaction state and the mobility of chromatin. We discuss the functional consequences of these changes in yeast and mammals in the light of the different repair pathways utilized by these organisms. In the final section of this review, we show how future developments in high-resolution light microscopy and chromatin modelling by polymer physics should contribute to a better understanding of the relationship between the structural changes in chromatin and the activity of the repair processes.

References

[1]	Woodcock CL, Ghosh RP (2010) Chromatin higher-order structure and dynamics. Cold Spring Harb Perspect Biol 2: a000596.
[2]	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
[3]	Miné-Hattab J, Rothstein R (2012) Increased chromosome mobility facilitates homology search during recombination. Nat Cell Biol 14: 510–517. doi: 10.1038/ncb2472
[4]	Khurana S, Kruhlak MJ, Kim J, et al. (2014) A macrohistone variant links dynamic chromatin compaction to BRCA1-dependent genome maintenance. Cell Rep 8: 1049–1062. doi: 10.1016/j.celrep.2014.07.024
[5]	Robinson PJJ, Fairall L, Huynh VAT, et al. (2006) EM measurements define the dimensions of the “30-nm” chromatin fiber: evidence for a compact, interdigitated structure. Proc Natl Acad Sci U S A 103: 6506–6511. doi: 10.1073/pnas.0601212103
[6]	Schalch T, Duda S, Sargent DF, et al. (2005) X-ray structure of a tetranucleosome and its implications for the chromatin fibre. Nature 436: 138–141. doi: 10.1038/nature03686
[7]	Joti Y, Hikima T, Nishino, et al. (2012) Chromosomes without a 30-nm chromatin fiber. Nucl Austin Tex 3: 404–410.
[8]	Fussner E, Ahmed K, Dehghani, et al. (2010) Changes in chromatin fiber density as a marker for pluripotency. Cold Spring Harb Symp Quant. Biol 75: 245–249. doi: 10.1101/sqb.2010.75.012
[9]	Yokota H, van den Engh G, Hearst JE, et al. (1995) Evidence for the organization of chromatin in megabase pair-sized loops arranged along a random walk path in the human G0/G1 interphase nucleus. J Cell Biol 130: 1239–1249. doi: 10.1083/jcb.130.6.1239
[10]	Petrascheck M, Escher D, Mahmoudi T et al. (2005) DNA looping induced by a transcriptional enhancer in vivo. Nucleic Acids Res. 33: 3743–3750. doi: 10.1093/nar/gki689
[11]	Pombo A, Dillon N (2015) Three-dimensional genome architecture: players and mechanisms. Nat Rev Mol Cell Biol 16: 245–257.
[12]	Dixon JR, Selvaraj S, Yue F, et al. (2012) Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485: 376–380. doi: 10.1038/nature11082
[13]	Nora EP, Lajoie BR, Schulz EG, et al. (2012) Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485: 381–385. doi: 10.1038/nature11049
[14]	Sexton T, Yaffe E, Kenigsberg E, 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
[15]	Lieberman-Aiden E, van Berkum NL, Williams L, 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
[16]	Bolzer A, Kreth G, Solovei I, et al. (2005) Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes. PLoS Biol 3: e157. doi: 10.1371/journal.pbio.0030157
[17]	Cremer T, Cremer M (2010) Chromosome territories. Cold Spring Harb Perspect Biol 2: a003889.
[18]	Kinney NA, Onufriev AV, Sharakhov IV (2015) Quantified effects of chromosome-nuclear envelope attachments on 3D organization of chromosomes. Nucl Austin Tex 6: 212–224.
[19]	Heun P, Laroche T, Shimada K, et al. (2001) Chromosome dynamics in the yeast interphase nucleus. Science 294: 2181–2186. doi: 10.1126/science.1065366
[20]	Levi V, Ruan Q, Plutz M, et al. (2005) Chromatin dynamics in interphase cells revealed by tracking in a two-photon excitation microscope. Biophys J 89: 4275–4285. doi: 10.1529/biophysj.105.066670
[21]	Hubner M, Spector D (2010) Chromatin Dynamics. Annu Rev Biophys 39: 471–489.
[22]	Javer A, Long Z, Nugent E, et al. (2013) Short-time movement of E. coli chromosomal loci depends on coordinate and subcellular localization. Nat Commun. 4: 3003.
[23]	Gibcus JH, Dekker J (2013) The hierarchy of the 3D genome. Mol Cell 49: 773–782. doi: 10.1016/j.molcel.2013.02.011
[24]	Weber SC, Spakowitz AJ, Theriot JA (2012) Nonthermal ATP-dependent fluctuations contribute to the in vivo motion of chromosomal loci. Proc Natl Acad Sci U S A 109: 7338–7343. doi: 10.1073/pnas.1119505109
[25]	Pliss A, Malyavantham KS, Bhattacharya S, et al. (2013) Chromatin dynamics in living cells: identification of oscillatory motion. J Cell Physiol 228, 609–616.
[26]	Gerlich D, Beaudouin J, Kalbfuss B, et al. (2003) Global chromosome positions are transmitted through mitosis in mammalian cells. Cell 112: 751–764. doi: 10.1016/S0092-8674(03)00189-2
[27]	Walter J, Schermelleh L, Cremer M, et al. (2003) Chromosome order in HeLa cells changes during mitosis and early G1, but is stably maintained during subsequent interphase stages. J Cell Biol 160: 685–697. doi: 10.1083/jcb.200211103
[28]	Müller I, Boyle S, Singer RH, et al. (2010) Stable morphology, but dynamic internal reorganisation, of interphase human chromosomes in living cells. PloS One 5: e11560. doi: 10.1371/journal.pone.0011560
[29]	Kruhlak MJ, Celeste A, Dellaire G, et al. (2006) Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J Cell Biol 172: 823–834. doi: 10.1083/jcb.200510015
[30]	Zink D, Cremer T, Saffrich R, et al. (1998) Structure and dynamics of human interphase chromosome territories in vivo. Hum Genet 102: 241–251. doi: 10.1007/s004390050686
[31]	Jackson DA, Pombo A (1998) Replicon clusters are stable units of chromosome structure: evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J Cell Biol 140: 1285–1295. doi: 10.1083/jcb.140.6.1285
[32]	Robinett CC, Straight A, Li G, et al. (1996) In vivo localization of DNA sequences and visualization of large-scale chromatin organization using lac operator/repressor recognition. J Cell Biol 135: 1685–1700. doi: 10.1083/jcb.135.6.1685
[33]	Jacome A, Fernandez-Capetillo O (2011) Lac operator repeats generate a traceable fragile site in mammalian cells. EMBO Rep 12: 1032–1038. doi: 10.1038/embor.2011.158
[34]	Dubarry M, Loïodice I, Chen CL, et al. (2011) Tight protein-DNA interactions favor gene silencing. Genes Dev 25: 1365–1370. doi: 10.1101/gad.611011
[35]	Saad H, Gallardo F, Dalvai M, et al. (2014) DNA dynamics during early double-strand break processing revealed by non-intrusive imaging of living cells. PLoS Genet 10: e1004187. doi: 10.1371/journal.pgen.1004187
[36]	Chen B, Gilbert LA, Cimini BA, et al. (2013) Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155: 1479–1491. doi: 10.1016/j.cell.2013.12.001
[37]	Miyanari Y, Ziegler-Birling C, Torres-Padilla M-E (2013) Live visualization of chromatin dynamics with fluorescent TALEs. Nat Struct Mol Biol 20: 1321–1324. doi: 10.1038/nsmb.2680
[38]	Zidovska A, Weitz DA, Mitchison TJ (2013) Micron-scale coherence in interphase chromatin dynamics. Proc Natl Acad Sci U S A 110: 15555–15560. doi: 10.1073/pnas.1220313110
[39]	Hinde E, Kong X, Yokomori K, et al. (2014) Chromatin dynamics during DNA repair revealed by pair correlation analysis of molecular flow in the nucleus. Biophys J 107: 55–65. doi: 10.1016/j.bpj.2014.05.027
[40]	Marshall WF, Straight A, Marko JF, et al. (1997) Interphase chromosomes undergo constrained diffusional motion in living cells. Curr Biol CB 7: 930–939. doi: 10.1016/S0960-9822(06)00412-X
[41]	Bornfleth H, Edelmann P, Zink D, et al. (1999) Quantitative motion analysis of subchromosomal foci in living cells using four-dimensional microscopy. Biophys J 77: 2871–2886. doi: 10.1016/S0006-3495(99)77119-5
[42]	Qian H, Sheetz MP, Elson EL (1991) Single particle tracking. Analysis of diffusion and flow in two-dimensional systems. Biophys J 60: 910–921.
[43]	Rosa A, Everaers R (2008) Structure and dynamics of interphase chromosomes. PLoS Comput Biol 4: e1000153. doi: 10.1371/journal.pcbi.1000153
[44]	Hajjoul H, Mathon J, Ranchon H, et al. (2013) High-throughput chromatin motion tracking in living yeast reveals the flexibility of the fiber throughout the genome. Genome Res 23: 1829–1838.
[45]	Havlin S, Ben-Avraham D (2002) Diffusion in disordered media. Adv Phys 51: 187–292. doi: 10.1080/00018730110116353
[46]	Doi M (1996) Introduction to polymer physics Oxford University Press.
[47]	Bronstein I, Israel Y, Kepten E, et al. (2009) Transient anomalous diffusion of telomeres in the nucleus of mammalian cells. Phys Rev Lett 103: 018102. doi: 10.1103/PhysRevLett.103.018102
[48]	Dion V, Kalck V, Seeber A, et al. (2013) Cohesin and the nucleolus constrain the mobility of spontaneous repair foci. EMBO Rep 14: 984–991. doi: 10.1038/embor.2013.142
[49]	Gartenberg MR, Neumann FR, Laroche T, et al. (2004) Sir-mediated repression can occur independently of chromosomal and subnuclear contexts. Cell 119: 955–967. doi: 10.1016/j.cell.2004.11.008
[50]	Hu Y, Kireev I, Plutz M, et al. (2009) Large-scale chromatin structure of inducible genes: transcription on a condensed, linear template. J Cell Biol 185: 87–100. doi: 10.1083/jcb.200809196
[51]	Neumann FR, Dion V, Gehlen LR, et al. (2012) Targeted INO80 enhances subnuclear chromatin movement and ectopic homologous recombination. Genes Dev 26: 369–383. doi: 10.1101/gad.176156.111
[52]	Chuang C-H, Carpenter AE, Fuchsova B, et al. (2006) Long-range directional movement of an interphase chromosome site. Curr Biol 16: 825–831.
[53]	Khanna N, Hu Y, Belmont AS (2014) HSP70 transgene directed motion to nuclear speckles facilitates heat shock activation. Curr Biol 24: 1138–1144.
[54]	Chubb JR, Boyle S, Perry P, et al. (2002) Chromatin motion is constrained by association with nuclear compartments in human cells. Curr Biol 12: 439–445.
[55]	Lucas JS, Zhang Y, Dudko OK, et al. (2014) 3D trajectories adopted by coding and regulatory DNA elements: first-passage times for genomic interactions. Cell 158: 339–352. doi: 10.1016/j.cell.2014.05.036
[56]	Daley JM, Gaines WA, Kwon Y, et al. (2014) Regulation of DNA pairing in homologous recombination. Cold Spring Harb Perspect Biol 6: a017954. doi: 10.1101/cshperspect.a017954
[57]	Lieber MR (2010) The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem 79: 181–211. doi: 10.1146/annurev.biochem.052308.093131
[58]	Sonoda E, Hochegger H, Saberi A, et al. (2006) Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Repair 5: 1021–1029. doi: 10.1016/j.dnarep.2006.05.022
[59]	Dion V, Kalck V, Horigome C, et al. (2012) Increased mobility of double-strand breaks requires Mec1, Rad9 and the homologous recombination machinery. Nat Cell Biol 14: 502–509. doi: 10.1038/ncb2465
[60]	Seeber A, Dion V, Gasser SM (2013) Checkpoint kinases and the INO80 nucleosome remodeling complex enhance global chromatin mobility in response to DNA damage. Genes Dev 27: 1999–2008. doi: 10.1101/gad.222992.113
[61]	Lisby M, Mortensen UH, Rothstein R (2003) Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat Cell Biol 5: 572–577. doi: 10.1038/ncb997
[62]	Nagai S, Dubrana K, Tsai-Pflugfelder M, et al. (2008) Functional targeting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase. Science 322: 597–602. doi: 10.1126/science.1162790
[63]	Kalocsay M, Hiller NJ, Jentsch S (2009) Chromosome-wide Rad51 spreading and SUMO-H2A.Z-dependent chromosome fixation in response to a persistent DNA double-strand break. Mol Cell 33: 335–343.
[64]	Krawczyk PM, Borovski T, Stap J, et al. (2012) Chromatin mobility is increased at sites of DNA double-strand breaks. J Cell Sci 125: 2127–2133. doi: 10.1242/jcs.089847
[65]	Aten JA, Stap J, Krawczyk PM, et al. (2004) Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 303: 92–95. doi: 10.1126/science.1088845
[66]	Dimitrova N, Chen Y-CM, Spector DL, et al. (2008) 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature 456: 524–528. doi: 10.1038/nature07433
[67]	Jakob B, Splinter J, Conrad S, et al. (2011) DNA double-strand breaks in heterochromatin elicit fast repair protein recruitment, histone H2AX phosphorylation and relocation to euchromatin. Nucleic Acids Res 39: 6489–6499. doi: 10.1093/nar/gkr230
[68]	Ježková L, Falk M, Falková I, et al. (2014) Function of chromatin structure and dynamics in DNA damage, repair and misrepair: γ-rays and protons in action. Appl Radiat Isot Data Instrum Methods Use Agric Ind Med 83: 128–136.
[69]	Chiolo I, Minoda A, Colmenares SU, et al. (2011) Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 144: 732–744. doi: 10.1016/j.cell.2011.02.012
[70]	Nelms BE, Maser RS, MacKay JF, et al. (1998) In situ visualization of DNA double-strand break repair in human fibroblasts. Science 280: 590–592. doi: 10.1126/science.280.5363.590
[71]	Jakob B, Splinter J, Durante M, et al. (2009) Live cell microscopy analysis of radiation-induced DNA double-strand break motion. Proc Natl Acad Sci U S A 106: 3172–3177. doi: 10.1073/pnas.0810987106
[72]	Soutoglou E, Dorn JF, Sengupta K, et al. (2007) Positional stability of single double-strand breaks in mammalian cells. Nat Cell Biol 9: 675–682. doi: 10.1038/ncb1591
[73]	Roukos V, Voss TC, Schmidt CK, et al. (2013) Spatial dynamics of chromosome translocations in living cells. Science 341: 660–664. doi: 10.1126/science.1237150
[74]	Smerdon MJ, Lieberman MW (1978) Nucleosome rearrangement in human chromatin during UV-induced DNA- reapir synthesis. Proc Natl Acad Sci U S A 75: 4238–4241. doi: 10.1073/pnas.75.9.4238
[75]	Ziv Y, Bielopolski D, Galanty Y, et al. (2006) Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM- and KAP-1 dependent pathway. Nat Cell Biol 8: 870–876. doi: 10.1038/ncb1446
[76]	Burgess RC, Burman B, Kruhlak MJ, et al. (2014) Activation of DNA damage response signaling by condensed chromatin. Cell Rep 9: 1703–1717. doi: 10.1016/j.celrep.2014.10.060
[77]	Smeenk G, Wiegant WW, Marteijn JA, et al. (2013) Poly(ADP-ribosyl)ation links the chromatin remodeler SMARCA5/SNF2H to RNF168-dependent DNA damage signaling. J Cell Sci 126: 889–903. doi: 10.1242/jcs.109413
[78]	Baldeyron C, Soria G, Roche D, et al. (2011) HP1alpha recruitment to DNA damage by p150CAF-1 promotes homologous recombination repair. J Cell Biol 193: 81–95. doi: 10.1083/jcb.201101030
[79]	Ayrapetov MK, Gursoy-Yuzugullu O, Xu C, et al. (2014) DNA double-strand breaks promote methylation of histone H3 on lysine 9 and transient formation of repressive chromatin. Proc Natl Acad Sci U S A 111: 9169–9174. doi: 10.1073/pnas.1403565111
[80]	Zhu L, Brangwynne CP (2015) Nuclear bodies: the emerging biophysics of nucleoplasmic phases. Curr Opin Cell Biol 34: 23–30. doi: 10.1016/j.ceb.2015.04.003
[81]	Chubb JR, Bickmore WA (2003) Considering nuclear compartmentalization in the light of nuclear dynamics. Cell 112: 403–406. doi: 10.1016/S0092-8674(03)00078-3
[82]	Lemaître C, Soutoglou E (2015) DSB (Im)mobility and DNA repair compartmentalization in mammalian cells. J Mol Biol 427: 652–658. doi: 10.1016/j.jmb.2014.11.014
[83]	Klein IA, Resch W, Jankovic M, et al. (2011) Translocation-capture sequencing reveals the extent and nature of chromosomal rearrangements in B lymphocytes. Cell 147: 95–106. doi: 10.1016/j.cell.2011.07.048
[84]	Murr R, Loizou JI, Yang Y-G, et al. (2006) Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat Cell Biol 8: 91–99. doi: 10.1038/ncb1343
[85]	Verschure PJ, van der Kraan I, Manders EMM, et al. (2003) Condensed chromatin domains in the mammalian nucleus are accessible to large macromolecules. EMBO Rep 4: 861–866. doi: 10.1038/sj.embor.embor922
[86]	Bancaud A, Huet S, Daigle N, et al. (2009) Molecular crowding affects diffusion and binding of nuclear proteins in heterochromatin and reveals the fractal organization of chromatin. EMBO J 28: 3785–3798. doi: 10.1038/emboj.2009.340
[87]	Dinant C, de Jager M, Essers J, et al. (2007) Activation of multiple DNA repair pathways by sub-nuclear damage induction methods. J Cell Sci 120: 2731–2740. doi: 10.1242/jcs.004523
[88]	Kong X, Mohanty SK, Stephens J, et al. (2009) Comparative analysis of different laser systems to study cellular responses to DNA damage in mammalian cells. Nucleic Acids Res 37: e68. doi: 10.1093/nar/gkp221
[89]	Gilbert N, Allan J (2014) Supercoiling in DNA and chromatin. Curr Opin Genet Dev 25: 15–21. doi: 10.1016/j.gde.2013.10.013
[90]	Elbel T, Langowski J (2015) The effect of DNA supercoiling on nucleosome structure and stability. J Phys Condens Matter Inst Phys J 27: 064105. doi: 10.1088/0953-8984/27/6/064105
[91]	Polo SE (2015) Reshaping chromatin after DNA damage: the choreography of histone proteins. J Mol Biol 427: 626–636. doi: 10.1016/j.jmb.2014.05.025
[92]	Downs JA, Lowndes NF, Jackson SP (2000) A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 408: 1001–1004. doi: 10.1038/35050000
[93]	Heo K, Kim H, Choi SH, et al. (2008) FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16. Mol Cell 30: 86–97. doi: 10.1016/j.molcel.2008.02.029
[94]	Li A, Yu Y, Lee S-C, et al. (2010) Phosphorylation of histone H2A.X by DNA-dependent protein kinase is not affected by core histone acetylation, but it alters nucleosome stability and histone H1 binding. J Biol Chem 285: 17778–17788.
[95]	Golia B, Singh HR, Timinszky G (2015) Poly-ADP-ribosylation signaling during DNA damage repair. Front Biosci Landmark Ed 20: 440–457. doi: 10.2741/4318
[96]	Poirier GG, de Murcia G, Jongstra-Bilen J, et al. (1982) Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure. Proc Natl Acad Sci U S A 79: 3423–3427. doi: 10.1073/pnas.79.11.3423
[97]	de Murcia G, Huletsky A, Lamarre D, et al. (1986) Modulation of chromatin superstructure induced by poly(ADP-ribose) synthesis and degradation. J Biol Chem 261: 7011–7017.
[98]	Xu Y, Ayrapetov MK, Xu C, et al. (2012) Histone H2A.Z controls a critical chromatin remodeling step required for DNA double-strand break repair. Mol Cell 48: 723–733.
[99]	Clapier CR, Cairns BR (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78: 273–304. doi: 10.1146/annurev.biochem.77.062706.153223
[100]	Cheezum MK, Walker WF, Guilford WH (2001) Quantitative comparison of algorithms for tracking single fluorescent particles. Biophys J 81: 2378–2388. doi: 10.1016/S0006-3495(01)75884-5
[101]	Wombacher R, Heidbreder M, van de Linde S, et al. (2010) Live-cell super-resolution imaging with trimethoprim conjugates. Nat Methods 7: 717–719. doi: 10.1038/nmeth.1489
[102]	Benke A, Manley S (2012) Live-cell dSTORM of cellular DNA based on direct DNA labeling. Chembiochem Eur J Chem Biol 13: 298–301. doi: 10.1002/cbic.201100679
[103]	Hihara S, Pack C-G, Kaizu K, et al. (2012) Local nucleosome dynamics facilitate chromatin accessibility in living mammalian cells. Cell Rep 2: 1645–1656. doi: 10.1016/j.celrep.2012.11.008
[104]	Récamier V, Izeddin I, Bosanac L, et al. (2014) Single cell correlation fractal dimension of chromatin: a framework to interpret 3D single molecule super-resolution. Nucl Austin Tex 5: 75–84.
[105]	Ricci MA, Manzo C, García-Parajo MF, et al. (2015) Chromatin fibers are formed by heterogeneous groups of nucleosomes in vivo. Cell 160: 1145–1158. doi: 10.1016/j.cell.2015.01.054
[106]	Zhang Y, Máté G, Müller P, et al. (2015) Radiation induced chromatin conformation changes analysed by fluorescent localization microscopy, statistical physics, and graph theory. PloS One 10: e0128555. doi: 10.1371/journal.pone.0128555
[107]	Llères D, James J, Swift S, et al. (2009) Quantitative analysis of chromatin compaction in living cells using FLIM-FRET. J Cell Biol 187: 481–496. doi: 10.1083/jcb.200907029
[108]	Emanuel M, Radja NH, Henriksson A, et al. (2009) The physics behind the larger scale organization of DNA in eukaryotes. Phys Biol 6: 025008. doi: 10.1088/1478-3975/6/2/025008
[109]	Rouse P (1953) A Theory of the Linear Viscoelastic Properties of Dilute Solutions of Coiling Polymers. J Chem Phys 21: 1272–1280. doi: 10.1063/1.1699180
[110]	Weber SC, Spakowitz AJ, Theriot JA (2010) Bacterial chromosomal loci move subdiffusively through a viscoelastic cytoplasm. Phys Rev Lett 104: 238102. doi: 10.1103/PhysRevLett.104.238102
[111]	Metzler R, Jeon J-H, Cherstvy AG, et al. (2014) Anomalous diffusion models and their properties: non-stationarity, non-ergodicity, and ageing at the centenary of single particle tracking. Phys Chem Chem Phys 16: 24128–24164.
[112]	Mirny LA (2011) The fractal globule as a model of chromatin architecture in the cell. Chromosome Res Int J Mol Supramol Evol Asp Chromosome Biol 19: 37–51.
[113]	Huet S, Lavelle C, Ranchon H, et al. (2014) Relevance and limitations of crowding, fractal, and polymer models to describe nuclear architecture. Int Rev Cell Mol Biol 307: 443–479. doi: 10.1016/B978-0-12-800046-5.00013-8
[114]	Barbieri M, Chotalia M, Fraser J, et al. (2012) Complexity of chromatin folding is captured by the strings and binders switch model. Proc Natl Acad Sci U S A 109: 16173–16178. doi: 10.1073/pnas.1204799109
[115]	Mateos-Langerak J, Bohn M, de Leeuw W, et al. (2009) Spatially confined folding of chromatin in the interphase nucleus. Proc Natl Acad Sci U S A 106: 3812–3817. doi: 10.1073/pnas.0809501106
[116]	Bohn M, Heermann DW (2010) Diffusion-driven looping provides a consistent framework for chromatin organization. PloS One 5: e12218. doi: 10.1371/journal.pone.0012218
[117]	Jerabek H, Heermann DW (2014) How chromatin looping and nuclear envelope attachment affect genome organization in eukaryotic cell nuclei. Int Rev Cell Mol Biol 307: 351–381. doi: 10.1016/B978-0-12-800046-5.00010-2
[118]	Cook PR, Marenduzzo D (2009) Entropic organization of interphase chromosomes. J Cell Biol 186: 825–834.
[119]	Bohn M, Heermann DW (2011) Repulsive forces between looping chromosomes induce entropy-driven segregation. PloS One 6: e14428. doi: 10.1371/journal.pone.0014428
[120]	Jost D, Carrivain P, Cavalli G, et al. (2014) Modeling epigenome folding: formation and dynamics of topologically associated chromatin domains. Nucleic Acids Res 42: 9553–9561. doi: 10.1093/nar/gku698
[121]	Finan K, Cook PR, Marenduzzo D (2011) Non-specific (entropic) forces as major determinants of the structure of mammalian chromosomes. Chromosome Res Int J Mol Supramol Evol Asp Chromosome Biol 19: 53–61. doi: 10.1007/s10577-010-9150-y
[122]	Zhang B, Wolynes PG (2015) Topology, structures, and energy landscapes of human chromosomes. Proc Natl. Acad Sci U S A 112: 6062–6067. doi: 10.1073/pnas.1506257112

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