Biopolym. Cell. 2014; 30(2):83-89.
Reviews
Folded genome as a platform for the functional compartmentalization of the eukaryotic cell nucleus
- Institute of Gene Biology, Russian Academy of Sciences
34/5, Vavilova Str., Moscow, Russian Federation, 119334 - LIA 1066 French-Russian Joint Cancer Research Laboratory
Villejuif, France–Moscow, Russian Federation - Department of Molecular Biology, Faculty of Biology, M. V. Lomonosov Moscow State University
Leninskie Gory, Moscow, Russian Federation, 119991
Abstract
In a number of recent studies a tight interconnection between the spatial organization of the eukaryotic genome and its functioning has been demonstrated. Moreover, it is becoming evident that the folded DNA by itself consti- tutes an important, if not the key, factor supporting the internal nuclear organization. In this review, we will discuss the current state of chromatin research with the special attention focused on chromosome territories, chromatin folding and dynamics, chromatin domains, transcription and replication factories. Based on this analysis we will show how interphase chromosomes define the assembly of different nuclear compartments and underlie the spatial compartmentalization of the cell nucleus.
Keywords: chromosome folding, nuclear compartments, genome spatial organization
Full text: (PDF, in English)
References
[1]
Misteli T. Cell biology of transcription and pre-mRNA splicing: nuclear architecture meets nuclear function. J Cell Sci. 2000; 113(Pt 11):1841–9.
[2]
Dundr M, Misteli T. Functional architecture in the cell nucleus. Biochem J. 2001; 356(Pt 2):297–310.
[3]
Geyer PK, Vitalini MW, Wallrath LL. Nuclear organization: taking a position on gene expression. Curr Opin Cell Biol. 2011; 23(3):354–9.
[4]
Matera AG, Izaguire-Sierra M, Praveen K, Rajendra TK. Nuclear bodies: random aggregates of sticky proteins or crucibles of macromolecular assembly? Dev Cell. 2009; 17(5):639–47.
[5]
Shaper JH, Pardoll DM, Kaufmann SH, Barrack ER, Vogelstein B, Coffey DS. The relationship of the nuclear matrix to cellular structure and function. Adv Enzyme Regul. 1978; 17: 213–48.
[6]
Berezney R, Mortillaro MJ, Ma H, Wei X, Samarabandu J. The nuclear matrix: a structural milieu for genomic function. Int Rev Cytol. 1995; 162A:1–65.
[7]
Xing YG, Lawrence JB. Preservation of specific RNA distribution within the chromatin-depleted nuclear substructure demonstrated by in situ hybridization coupled with biochemical fractionation. J Cell Biol. 1991; 112(6):1055–63.
[8]
Stein GS, van Wijnen AJ, Stein JL, Lian JB, Pockwinse S, McNeil S. Interrelationships of nuclear structure and transcriptional control: functional consequences of being in the right place at the right time. J Cell Biochem. 1998; 70(2):200–12.
[9]
Hancock R. Internal organisation of the nucleus: assembly of compartments by macromolecular crowding and the nuclear matrix model. Biol Cell. 2004; 96(8):595–601.
[11]
Nickerson J. Experimental observations of a nuclear matrix. J Cell Sci. 2001; 114(Pt 3):463–74.
[12]
Simon DN, Wilson KL. The nucleoskeleton as a genome-associated dynamic «network of networks». Nat Rev Mol Cell Biol. 2011; 12(11):695–708.
[14]
Cremer T, Cremer C. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet. 2001; 2(4):292–301.
[15]
Cremer T, Cremer M. Chromosome territories. Cold Spring Harb Perspect Biol. 2010; 2(3):a003889.
[16]
Cremer T, Cremer M, Dietzel S, Muller S, Solovei I, Fakan S. Chromosome territories – a functional nuclear landscape. Curr Opin Cell Biol. 2006; 18(3):307–16.
[17]
Markaki Y, Gunkel M, Schermelleh L, Beichmanis S, Neumann J, Heidemann M, Leonhardt H, Eick D, Cremer C, Cremer T. Functional nuclear organization of transcription and DNA replication: a topographical marriage between chromatin domains and the interchromatin compartment. Cold Spring Harb Symp Quant Biol. 2010; 75:475–92.
[18]
Cremer T, Kupper K, Dietzel S, Fakan S. Higher order chromatin architecture in the cell nucleus: on the way from structure to function. Biol Cell. 2004; 96(8):555–67.
[19]
Habermann FA, Cremer M, Walter J, Kreth G, von Hase J, Bauer K, Wienberg J, Cremer C, Cremer T, Solovei I. Arrangements of macroand microchromosomes in chicken cells. Chromosome Res. 2001; 9(7):569–84.
[20]
Croft JA, Bridger JM, Boyle S, Perry P, Teague P, Bickmore WA. Differences in the localization and morphology of chromosomes in the human nucleus. J Cell Biol. 1999; 145(6):1119–31.
[21]
Boyle S, Gilchrist S, Bridger JM, Mahy NL, Ellis JA, Bickmore WA. The spatial organization of human chromosomes within the nuclei of normal and emerin-mutant cells. Human Mol Genet. 2001; 10(3):211–9.
[22]
Mayer R, Brero A, von Hase J, Schroeder T, Cremer T, Dietzel S. Common themes and cell type specific variations of higher order chromatin arrangements in the mouse. BMC Cell Biol. 2005; 6:44.
[23]
Lukasova E, Kozubek S, Kozubek M, Falk M, Amrichova J. The 3D structure of human chromosomes in cell nuclei. Chromosome Res. 2002; 10(7):535–48.
[24]
Taslerova R, Kozubek S, Lukasova E, Jirsova P, Bartova E, Kozubek M. Arrangement of chromosome 11 and 22 territories, EWSR1 and FLI1 genes, and other genetic elements of these chromosomes in human lymphocytes and Ewing sarcoma cells. Hum Genet. 2003; 112(2):143–55.
[25]
de Wit E, de Laat W. A decade of 3C technologies: insights into nuclear organization. Genes Dev. 2011; 26(1):11–24.
[26]
Gavrilov AA, Razin SV, Iarovaia OV. C-methods to study 3D organization of the eukaryotic genome. Biopolym Cell. 2012; 28 (4):245–51.
[27]
Belton JM, McCord RP, Gibcus JH, Naumova N, Zhan Y, Dekker J. Hi-C: a comprehensive technique to capture the conformation of genomes. Methods. 2012; 58(3):268–76.
[28]
Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO, Sandstrom R, Bernstein B, Bender MA, Groudine M, Gnirke A, Stamatoyannopoulos J, Mirny LA, Lander ES, Dekker J. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science. 2009; 326(5950):289–93.
[29]
Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, Hu M, Liu JS, Ren B. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature. 2012; 485(7398): 376–80.
[30]
Sexton T, Yaffe E, Kenigsberg E, Bantignies F, Leblanc B, Hoichman M, Parrinello H, Tanay A, Cavalli G. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell. 2012; 148(3):458–72.
[31]
Mirny LA. The fractal globule as a model of chromatin architecture in the cell. Chromosome Res. 2011; 19(1):37–51.
[32]
Bickmore WA, van Steensel B. Genome architecture: domain organization of interphase chromosomes. Cell. 2013; 152(6): 1270–84.
[33]
Olins DE, Olins AL. Chromatin history: our view from the bridge. Nat Rev Mol Cell Biol. 2003; 4(10):809–14.
[34]
Getzenberg RH, Pienta KJ, Ward WS, Coffey DS. Nuclear structure and the three-dimensional organization of DNA. J Cell Biochem. 1991; 47(4):289–99.
[35]
Gan L, Ladinsky MS, Jensen GJ. Chromatin in a marine picoeukaryote is a disordered assemblage of nucleosomes. Chromosoma. 2013; 122(5):377–86.
[36]
Fussner E, Strauss M, Djuric U, Li R, Ahmed K, Hart M, Ellis J, Bazett-Jones DP. Open and closed domains in the mouse genome are configured as 10-nm chromatin fibres. EMBO Rep. 2012; 13(11):992–6.
[37]
Eltsov M, Maclellan KM, Maeshima K, Frangakis AS, Dubochet J. Analysis of cryo-electron microscopy images does not support the existence of 30-nm chromatin fibers in mitotic chromosomes in situ. Proc Natl Acad Sci USA. 2008; 105(50):19732–7.
[38]
Hihara S, Pack CG, Kaizu K, Tani T, Hanafusa T, Nozaki T, Takemoto S, Yoshimi T, Yokota H, Imamoto N, Sako Y, Kinjo M, Takahashi K, Nagai T, Maeshima K. Local nucleosome dynamics facilitate chromatin accessibility in living mammalian cells. Cell Rep. 2012; 2(6):1645–56.
[39]
Schoenfelder S, Sexton T, Chakalova L, Cope NF, Horton A, Andrews S, Kurukuti S, Mitchell JA, Umlauf D, Dimitrova DS, Eskiw CH, Luo Y, Wei CL, Ruan Y, Bieker JJ, Fraser P. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat Genet. 2010; 42(1):53–61.
[40]
Osborne CS, Chakalova L, Brown KE, Carter D, Horton A, Debrand E, Goyenechea B, Mitchell JA, Lopes S, Reik W, Fraser P. Active genes dynamically colocalize to shared sites of ongoing transcription. Nat Genet. 2004; 36(10):1065–71.
[41]
Rapkin LM, Anchel DR, Li R, Bazett-Jones DP. A view of the chromatin landscape. Micron. 2012; 43(2–3):150–8.
[42]
Gilbert N, Gilchrist S, Bickmore WA. Chromatin organization in the mammalian nucleus. Int Rev Cytol. 2005; 242:283–336.
[44]
Marshall WF, Straight A, Marko JF, Swedlow J, Dernburg A, Belmont A, Murray AW, Agard DA, Sedat JW. Interphase chromosomes undergo constrained diffusional motion in living cells. Curr Biol. 1997; 7(12):930–9.
[45]
Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, Eussen BH, de Klein A, Wessels L, de Laat W, van Steensel B. Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature. 2008; 453(7197):948–51.
[46]
van Bemmel JG, Pagie L, Braunschweig U, Brugman W, Meuleman W, Kerkhoven RM, van Steensel B. The insulator protein SU(HW) fine-tunes nuclear lamina interactions of the Drosophila genome. PLoS One. 2010; 5(11):e15013.
[47]
van Koningsbruggen S, Gierlinski M, Schofield P, Martin D, Barton GJ, Ariyurek Y, den Dunnen JT, Lamond AI. High-resolution whole-genome sequencing reveals that specific chromatin domains from most human chromosomes associate with nucleoli. Mol Biol Cell. 2010; 21(21):3735–48.
[48]
Kumaran RI, Spector DL. A genetic locus targeted to the nuclear periphery in living cells maintains its transcriptional competence. J Cell Biol. 2008; 180(1):51–65.
[49]
Reddy KL, Zullo JM, Bertolino E, Singh H. Transcriptional repression mediated by repositioning of genes to the nuclear lamina. Nature. 2008; 452(7184):243–7.
[50]
Kind J, Pagie L, Ortabozkoyun H, Boyle S, de Vries SS, Janssen H, Amendola M, Nolen LD, Bickmore WA, van Steensel B. Single-cell dynamics of genome-nuclear lamina interactions. Cell. 2013; 153(1):178–92.
[51]
Kind J, van Steensel B. Genome-nuclear lamina interactions and gene regulation. Curr Opin Cell Biol. 2010; 22(3):320–5.
[52]
Festenstein R, Pagakis SN, Hiragami K, Lyon D, Verreault A, Sekkali B, Kioussis D. Modulation of heterochromatin protein 1 dynamics in primary Mammalian cells. Science. 2003; 299(5607): 719–71.
[53]
Ficz G, Heintzmann R, Arndt-Jovin DJ. Polycomb group protein complexes exchange rapidly in living Drosophila. Development. 2005; 132(17):3963–76.
[54]
Carter DR, Eskiw C, Cook PR. Transcription factories. Biochem Soc Trans. 2008; 36(Pt 4):585–9.
[55]
Sutherland H, Bickmore WA. Transcription factories: gene expression in unions? Nat Rev Genet. 2009; 10(7):457–66.
[57]
Ma H, Samarabandu J, Devdhar RS, Acharya R, Cheng PC, Meng C, Berezney R. Spatial and temporal dynamics of DNA replication sites in mammalian cells. J Cell Biol. 1998; 143(6): 1415–25.
[58]
Adachi Y, Laemmli UK. Identification of nuclear pre-replication centers poised for DNA synthesis in Xenopus egg extracts: immunolocalization study of replication protein A. J Cell Biol. 1992; 119(1):1–15.
[59]
Berezney R. Visualizing DNA replication sites in the cell nucleus. Semin Cell Biol. 1991; 2(2):103–15.
[60]
Han J, Herzfeld J. Macromolecular diffusion in crowded solutions. Biophys J. 1993; 65(3):1155–61.
[61]
Ellis RJ. Macromolecular crowding: obvious but underappreciated. Trends Biochem Sci. 2001; 26(10):597–604.
[62]
Hancock R. A role for macromolecular crowding effects in the assembly and function of compartments in the nucleus. J Struct Biol. 2004; 146(3):281–90.
[63]
Razin SV, Gromova II. The channels model of the nuclear matrix structure. Bioessays. 1995; 17(5):443–50.
[64]
Lebofsky R, Heilig R, Sonnleitner M, Weissenbach J, Bensimon A. DNA replication origin interference increases the spacing between initiation events in human cells. Mol Biol Cell. 2006; 17 (12):5337–45.
[65]
Mechali M, Yoshida K, Coulombe P, Pasero P. Genetic and epigenetic determinants of DNA replication origins, position and activation. Curr Opin Genet Dev. 2013; 23(2):124–31.
[66]
Jackson DA, Pombo A. 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. 1998; 140(6):1285–95.
[67]
Razin SV, Gavrilov AA, Pichugin A, Lipinski M, Iarovaia OV, Vassetzky YS. Transcription factories in the context of the nuclear and genome organization. Nucleic Acids Res. 2011; 39(21):9085–92.
[68]
Mitchell JA, Fraser P. Transcription factories are nuclear subcompartments that remain in the absence of transcription. Genes Dev. 2008; 22(1):20–5.
[69]
Marenduzzo D, Finan K, Cook PR. The depletion attraction: an underappreciated force driving cellular organization. J Cell Biol. 2006; 175(5):681–6.
[70]
Marenduzzo D, Micheletti C, Cook PR. Entropy-driven genome organization. Biophys J. 2006; 90(10):3712–21.
[71]
Razin SV, Gavrilov AA, Ioudinkova ES, Iarovaia OV. Communication of genome regulatory elements in a folded chromosome. FEBS Lett. 2013; 587(13):1840–7.
[72]
Cisse II, Izeddin I, Causse SZ, Boudarene L, Senecal A, Muresan L, Dugast-Darzacq C, Hajj B, Dahan M, Darzacq X. Real-time dynamics of RNA polymerase II clustering in live human cells. Science. 2013; 341(6146):664–7.
[73]
Sims RJ 3rd, Nishioka K, Reinberg D. Histone lysine methylation: a signature for chromatin function. Trends Genet. 2003; 19 (11):629–39.
[75]
Simon JA, Kingston RE. Occupying chromatin: polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put. Mol Cell. 2013; 49(5):808–24.
[76]
Tiwari VK, McGarvey KM, Licchesi JD, Ohm JE, Herman JG, Schubeler D, Baylin SB. PcG proteins, DNA methylation, and gene repression by chromatin looping. PLoS Biol. 2008; 6(12): 2911–27.
[77]
Hu Y, Plutz M, Belmont AS. Hsp70 gene association with nuclear speckles is Hsp70 promoter specific. J Cell Biol. 2010; 191 (4):711–9.
[78]
Huang S, Spector DL. Nascent pre-mRNA transcripts are associated with nuclear regions enriched in splicing factors. Genes Dev. 1991; 5(12A):2288–302.
[79]
Melcak I, Cermanova S, Jirsova K, Koberna K, Malinsky J, Raska I. Nuclear pre-mRNA compartmentalization: trafficking of released transcripts to splicing factor reservoirs. Mol Biol Cell. 2000; 11(2):497–510.
[80]
Misteli T. Protein dynamics: implications for nuclear architecture and gene expression. Science. 2001; 291(5505):843–7.