Nicodemi, Mario and Prisco, Antonella. (2009) Thermodynamic pathways to genome spatial organization in the cell nucleus. Biophysical Journal, Vol.96 (No.6). pp. 2168-2177. ISSN 0006-3495

Preview

PDF WRAP_Nicodemi_bj_2009_nicodemi.pdf - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader Download (346Kb)

Abstract

The architecture of the eukaryotic genome is characterized by a high degree of spatial organization. Chromosomes occupy preferred territories correlated to their state of activity and, yet, displace their genes to interact with remote sites in complex patterns requiring the orchestration of a huge number of DNA loci and molecular regulators. Far from random, this organization serves crucial functional purposes, but its governing principles remain elusive. By computer simulations of a Statistical Mechanics model, we show how architectural patterns spontaneously arise from the physical interaction between soluble binding molecules and chromosomes via collective thermodynamics mechanisms. Chromosomes colocalize, loops and territories form and find their relative positions as stable hermodynamic states. These are selected by “thermodynamic switches” which are regulated by concentrations/affinity of soluble mediators and by number/location of their attachment sites along chromosomes. Our “thermodynamic switch model” of nuclear architecture, thus, explains on quantitative grounds how well known cell strategies of upregulation of DNA binding proteins or modification of chromatin structure can dynamically shape the organization of the nucleus.

Item Type:	Journal Article
Subjects:	Q Science > QH Natural history > QH426 Genetics
Divisions:	Faculty of Science > Physics
Library of Congress Subject Headings (LCSH):	Eukaryotic cells -- Genetics, Genomics, Binding sites (Biochemistry) -- Thermodynamics, Chromosomes -- Analysis
Journal or Publication Title:	Biophysical Journal
Publisher:	Biophysical Society
ISSN:	0006-3495
Date:	18 March 2009
Volume:	Vol.96
Number:	No.6
Page Range:	pp. 2168-2177
Identification Number:	10.1016/j.bpj.2008.12.3919
Status:	Peer Reviewed
Access rights to Published version:	Restricted or Subscription Access
Funder:	Italy. Ministero dell'istruzione, dell'università e della ricerca (MIUR), Fondo per gli Investimenti della Ricerca di Base (FIRB)
Grant number:	RBNE01S29H (MIUR-FIRB)
References:	1 T. Cremer, M. Cremer, S. Dietzel, S. Muller and I. Solovei et al., Chromosome territories—a functional nuclear landscape, Curr. Opin. Cell Biol. 18 (2006), pp. 307–316. 2 C. Lanctôt, T. Cheutin, M. Cremer, G. Cavalli and T. Cremer, Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions, Nat. Rev. Genet. 8 (2007), pp. 104–115. 3 T. Misteli, Beyond the sequence: cellular organization of genome function, Cell 128 (2007), pp. 787–800. 4 K. Meaburn and T. Misteli, Chromosome territories, Nature 445 (2007), pp. 379–381. 5 P. Fraser and W. Bickmore, Nuclear organization of the genome and the potential for gene regulation, Nature 447 (2007), pp. 413–417. 6 A. Akhtar and S. Gasser, The nuclear envelope and transcriptional control, Nat. Rev. Genet. 8 (2007), pp. 507–517. 7 W. de Laat and F. Grosvel, Spatial organization of gene expression: the active chromatin hub, Chromosome Res. 11 (2003), pp. 447–459. 8 C. Chuang, A. Carpenter, B. Fuchsova, T. Johnson and P. de Lanerolle et al., Long-range directional movement of an interphase chromosome site, Curr. Biol. 16 (2006), pp. 825–831. 9 T. Misteli, Protein dynamics: implications for nuclear architecture and gene expression, Science 291 (2001), pp. 843–847. 10 W. de Laat, Long-range DNA contacts: romance in the nucleus?, Curr. Opin. Cell Biol. 19 (2007), pp. 317–320. 11 S. Galande, P. Purbey, D. Notani and P. Kumar, The third dimension of gene regulation: organization of dynamic chromatin loopscape by SATB1, Curr. Opin. Genet. Dev. 17 (2007), pp. 408–414. 12 K. Brown, S. Guest, S. Smale, K. Hahm and M. Merkenschlager et al., Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin, Cell 91 (1997), pp. 845–854. 13 F. Bantignies, C. Grimaud, S. Lavrov, M. Gabut and G. Cavalli, Inheritance of Polycomb-dependent chromosomal interactions in Drosophila, Genes Dev. 17 (2003), pp. 2406–2420. 14 S. Kurukuti, V. Tiwari, G. Tavoosidana, E. Pugacheva and A. Murrell et al., CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2, Proc. Natl. Acad. Sci. USA 103 (2006), pp. 10684–10689. 15 J. Ling, T. Li, J. Hu, T. Vu and H. Chen et al., CTCF mediates interchromosomal colocalization between Igf2/H19 and Wsb1/Nf1, Science 312 (2006), pp. 269–272. 16 Z. Zhao, G. Tavoosidana, M. Sjlinder, A. Göndär and P. Mariano et al., Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions, Nat. Genet. 38 (2006), pp. 1341–1347. 17 N. Xu, M. Donohoe, S. Silva and J. Lee, Evidence that homologous X-chromosome pairing requires transcription of CTCF protein, Nat. Genet. 39 (2007), pp. 1390–1396. 18 R. Drissen, R. Palstra, N. Gillemans, E. Splinter and F. Grosveld et al., The active spatial organization of the beta-globin locus requires the transcription factor EKLF, Genes Dev. 18 (2004), pp. 2485–2490. 19 C. Vakoc, D. Letting, N. Gheldof, T. Sawado and M. Bender et al., Proximity among distant regulatory elements at the beta-globin locus requires GATA-1 and FOG-1, Mol. Cell. 17 (2005), pp. 453–462. 20 C. Spilianakis and R. Flavell, Long-range intrachromosomal interactions in the T helper type 2 cytokine locus, Nat. Immunol. 5 (2005), pp. 1017–1027. 21 C. Osborne, L. Chakalova, K. Brown, D. Carter and A. Horton et al., Active genes dynamically colocalize to shared sites of ongoing transcription, Nat. Genet. 36 (2004), pp. 1065–1071. 22 D. Marenduzzo, I. Faro-Trindade and P. Cook, What are the molecular ties that maintain genomic loops?, Trends Genet. 23 (2007), pp. 126–133. 23 C. Massie and I. Mills, ChIPping away at gene regulation, EMBO Rep. Rev. 9 (2008), pp. 337–343. 24 S. Maerkl and S. Guake, A system approach to measuring binding energy landscape of transcription factors, Science 315 (2007), pp. 233–237. 25 A. Morozov, J. Havranek, D. Baker and E. Siggia, Protein-DNA binding specificity predictions with structural models, Nucleic Acids Res. 33 (2005), pp. 5781–5798. 26 U. Gerland, J. Moroz and T. Hwa, Physical constraints and functional characteristics of transcription factor-DNA interaction, Proc. Natl. Acad. Sci. USA 99 (2002), pp. 12015–12020. 27 M. Lassig, From biophysics to evolutionary genetics: Statistical aspects of gene regulation, BMC Bioinform (2007) 10.1186/1471-2105-8-S6-S7 Published: 27 September 2007. 28 J. Berg, Dynamics of gene expression and the regulatory inference problem, Europhys. Lett. 82 (2008), p. 28010. 29 M. Simonis, J. Kooren and W. de Laat, An evaluation of 3C-based methods to capture DNA interactions, Nat. Methods. 4 (2007), pp. 895–901. 30 P. Purbey, S. Singh, P. Kumar, S. Mehta and K. Ganesh et al., domain-mediated dimerization and homeodomain-directed specificity are required for high-affinity DNA binding by SATB1, Nucleic Acids Res. 36 (2008), pp. 2107–2122. 31 M. Donohoe, L. Zhang, N. Xu, Y. Shi and J. Lee, Identification of a CTCF cofactor, Yy1, for the X chromosome binary Switch, Mol. Cell. 25 (2007), pp. 43–56. 32 A. Scialdone and M. Nicodemi, Mechanics and dynamics of X-chromosome pairing at X inactivation, PLoS Comp. Biol. 5 (2008), p. e10002444. 33 H. Jing, C. Vakoc, L. Ying, S. Mandat and H. Wang et al., Exchange of GATA factors mediates transitions in looped chromatin organization at a developmentally regulated gene locus, Mol. Cell. 29 (2008), pp. 232–242. 34 R. Hancock, A role for macromolecular crowding effects in the assembly and function of compartments in the nucleus, J. Struct. Biol. 146 (2004), pp. 281–290. 35 F. Hediger and S. Gasser, Heterochromatin protein 1: don't judge the book by its cover!, Curr. Opin. Genet. Dev. 16 (2006), pp. 143–150. 36 S. Kwon and J. Workman, The heterochromatin protein 1 (HP1) family: put away a bias toward HP1, Mol. Cells. 26 (2008), pp. 217–227. 37 J. Locke, M. Kotarski and K. Tartof, Dosage-dependent modifiers of position effect variegation in Drosophila and a mass action model that explains their effect, Genetics 120 (1988), pp. 181–198. 38 P. Hahnfeldt, J. Hearst, D. Brenner, R. Sachs and L. Hlatky, Polymer models for interphase chromosomes, Proc. Natl. Acad. Sci. USA 90 (1993), pp. 7854–7858. 39 H. Yokota, G. van den Engh, J. Hearst, R. Sachs and B. Trask, 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 (1995), pp. 1239–1249. 40 R. Sachs, G. Engh, B. Trask, H. Yokota and J. Hearst, A random-walk/giant-loop model for interphase chromosomes, Proc. Natl. Acad. Sci. USA 92 (1995), pp. 2710–2714. 41 C. Munkel and J. Langowski, Chromosome structure predicted by a polymer model, Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscip. Topics 57 (1998), pp. 5888–5896. 42 C. Munkel, R. Eils, S. Dietzel, D. Zink and C. Mehring et al., Compartmentalization of interphase chromosomes observed in simulation and experiment, J. Mol. Biol. 285 (1999), pp. 1053–1065. 43 G. Kreth, J. Finsterle, J. von Hase, M. Cremer and C. Cremer, Radial arrangement of chromosome territories in human cell nuclei: a computer model approach based on gene density indicates a probabilistic global positioning code, Biophys. J. 86 (2004), pp. 2803–2812. 44 B. Mergell, R. Everaers and H. Schiessel, Nucleosome interactions in chromatin: fiber stiffening and hairpin formation, Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 70 (2004), p. 011915. 45 D. Marenduzzo, C. Micheletti and P. Cook, Entropy-driven genome organization, Biophys. J. 90 (2006), pp. 3712–3721. 46 M. Bon, D. Marenduzzo and P. Cook, Modeling a self-avoiding chromatin loop: relation to the packing problem, action-at-a-distance, and nuclear context, Structure 14 (2006), pp. 197–204. 47 M. Bohn, D. Heermann and R. van Driel, Random loop model for long polymers, Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 76 (2007), p. 051805. 48 M. Nicodemi and A. Prisco, A symmetry breaking model for X chromosome inactivation, Phys. Rev. Lett. 98 (2007), p. 108104. 49 M. Nicodemi and A. Prisco, Self-assembly and DNA binding of the blocking factor in X chromosome inactivation, PLoS Comp. Biol. 3 (2007), pp. 2135–2142. 50 M. Nicodemi, B. Panning and A. Prisco, A thermodynamic switch for chromosome colocalization, Genetics 179 (2008), pp. 717–721. 51 M. Nicodemi, B. Panning and A. Prisco, Colocalization transition of homologous chromosomes at meiosis, Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 77 (2008), p. 061913. 52 M. Doi and S. Edwards, The Theory of Polymer Dynamics, Clarendon Press, Oxford, UK (1984). 53 K. Binder and D. Heermann, Monte Carlo Simulation in Statistical Physics, Springer-Verlag, Berlin, Heidelberg, and New York (2002). 54 K. Binder, Applications of Monte Carlo methods to statistical physics, Rep. Prog. Phys. 60 (1997), p. 487. 55 H. Stanley, Introduction to Phase Transitions and Critical Phenomena, Clarendon Press, Oxford, UK (1971). 56 M. Branco and A. Pombo, Intermingling of chromosome territories in interphase suggests role in translocations and transcription-dependent associations, PLoS Biol. 4 (2006), p. e138. 57 N. Maynard, J. Chen, R. Stuart, J. Fan and B. Ren, Genome-wide mapping of allele-specific protein-DNA interactions in human cells, Nat. Methods 5 (2008), pp. 307–309. 58 S. Lomvardas, G. Barnea, D. Pisapia, M. Mendelsohn and J. Kirkland et al., Interchromosomal interactions and olfactory receptor choice, Cell 126 (2006), pp. 403–413. 59 T. Takizawa, P. Gudla, L. Guo, S. Lockett and T. Misteli, Allele-specific nuclear positioning of the monoallelically expressed astrocyte marker GFAP, Genes Dev. 22 (2008), pp. 489–498. 60 K. Handwerger, J. Cordero and J. Gall, Cajal bodies, nucleoli, and speckles in the Xenopus oocyte nucleus have a low-density, sponge-like structure, MBC 16 (2005), pp. 202–211. 61 R. Hancock, Packing of the polynucleosome chain in interphase chromosomes: evidence for a contribution of crowding and entropic forces, SCDB 18 (2007), pp. 668–675. 62 P. Cook, Predicting three-dimensional genome structure from transcriptional activity, Nat. Genet. 32 (2002), pp. 347–352. 63 C. Osborne, L. Chakalova, K. Brown, D. Carter and A. Horton et al., Replication and transcription: shaping the landscape of the genome, Nat. Rev. Genet. 6 (2005), pp. 669–677.
URI:	http://wrap.warwick.ac.uk/id/eprint/2190

Request changes to a record

Actions (login required)

View Item