A polymer model explains the complexity of large-scale chromatin folding

Nucleus (United States)

Volumn 4, Issue 4, 2013, Pages

  Barbieri, Mariano ^a   Fraser, James ^b   Lavitas, Liron Mark ^c   Chotalia, Mita ^d   Dostie, Josée ^b   Pombo, Ana ^c,d   Nicodemi, Mario ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b MCGILL UNIVERSITY   (Canada)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^d HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

Chromatin organization; FISH; Hi C; Polymer physics; Statistical mechanics

Indexed keywords

POLYMER;

ARTICLE; BASE PAIRING; BINDING AFFINITY; BINDING SITE; CELL NUCLEUS; CHEMICAL STRUCTURE; CHEMISTRY; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN ORGANIZATION; CHROMOSOMAL INSTABILITY; CHROMOSOME STRUCTURE; CONFORMATIONAL TRANSITION; DNA BINDING; EPIGENETICS; FEEDBACK SYSTEM; FISH; HI-C; HUMAN; METABOLISM; MODEL; POLYMER PHYSICS; PROBABILITY; STATISTICAL MECHANICS; STRINGS AND BINDERS SWITCH MODEL; THERMODYNAMICS; UPREGULATION; CHEMICAL BINDING; CHROMATIN FOLDING; FLUORESCENCE IN SITU HYBRIDIZATION; GENOME-WIDE ASSOCIATION STUDY; MOLECULAR INTERACTION; MOLECULAR PHYSICS; NONHUMAN;

CHROMATIN ORGANIZATION; FISH; HI-C; POLYMER PHYSICS; STATISTICAL MECHANICS;

CELL NUCLEUS; CHEMISTRY; CHROMATIN; HUMANS; METABOLISM; MODELS, MOLECULAR; POLYMERS;

EID: 84981488759     PISSN: 19491034     EISSN: 19491042     Source Type: Journal    
DOI: 10.4161/nucl.25432     Document Type: Article

References (39)

1. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 2009; 326:289-293. PMID:19815776. http://dx.doi.org/10.1126/science.1181369
2. Cook PR. The organization of replication and transcription. Science 1999; 284:1790-1795. PMID:10364545. http://dx.doi.org/10.1126/science.284.5421.1790
3. Cremer T, Cremer C. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet 2001; 2:292-301. PMID:11283701. http://dx.doi.org/10.1038/35066075
4. Kreth G, Finsterle J, von Hase J, Cremer M, Cremer C. 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 2004; 86:2803-2812. PMID:15111398. http://dx.doi.org/10.1016/S0006-3495(04)74333-7
5. Pombo A, Branco MR. Functional organisation of the genome during interphase. Curr Opin Genet Dev 2007; 17:451-455. PMID:17920259. http://dx.doi. org/10.1016/j.gde.2007.08.008
6. Lanctôt C, Cheutin T, Cremer M, Cavalli G, Cremer T. Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions. Nat Rev Genet 2007; 8:104-115. PMID:17230197. http://dx.doi.org/10.1038/nrg2041
7. Misteli T. Beyond the sequence: cellular organization of genome function. Cell 2007; 128:787-800. PMID:17320514. http://dx.doi.org/10.1016/j. cell.2007.01.028
8. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 2012; 485:376-380. PMID:22495300. http://dx.doi.org/10.1038/nature11082
9. Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I, Servant N, et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 2012; 485:381-385. PMID:22495304. http://dx.doi.org/10.1038/nature11049
10. Shopland LS, Lynch CR, Peterson KA, Thornton K, Kepper N, Hase Jv, et al. Folding and organization of a contiguous chromosome region according to the gene distribution pattern in primary genomic sequence. J Cell Biol 2006; 174:27-38. PMID:16818717. http://dx.doi.org/10.1083/jcb.200603083
11. Kalhor R, Tjong H, Jayathilaka N, Alber F, Chen L. Genome architectures revealed by tethered chromosome conformation capture and population-based modeling. Nat Biotechnol 2012; 30:90-98. PMID:22198700. http://dx.doi.org/10.1038/nbt.2057
12. Sexton T, Yaffe E, Kenigsberg E, Bantignies F, Leblanc B, Hoichman M, et al. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 2012; 148:458-472. PMID:22265598. http://dx.doi.org/10.1016/j. cell.2012.01.010
13. Branco MR, Pombo A. Intermingling of chromosome territories in interphase suggests role in translocations and transcription-dependent associations. PLoS Biol 2006; 4:e138. PMID:16623600. http://dx.doi. org/10.1371/journal.pbio.0040138
14. Yokota H, van den Engh G, Hearst JE, Sachs RK, Trask BJ. 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 1995; 130:1239-1249. PMID:7559748. http://dx.doi.org/10.1083/jcb.130.6.1239
15. Bohn M, Heermann DW. Diffusion-driven looping provides a consistent framework for chromatin organization. PLoS One 2010; 5:e12218. PMID:20811620. http://dx.doi.org/10.1371/journal. pone.0012218
16. Sachs RK, van den Engh G, Trask B, Yokota H, Hearst JE. A random-walk/giant-loop model for interphase chromosomes. Proc Natl Acad Sci U S A 1995; 92:2710-2714. PMID:7708711. http://dx.doi. org/10.1073/pnas.92.7.2710
17. Bohn M, Heermann DW, van Driel R. Random loop model for long polymers. Phys Rev E Stat Nonlin Soft Matter Phys 2007; 76:051805. PMID:18233679. http://dx.doi.org/10.1103/PhysRevE.76.051805
18. Barbieri M, Chotalia M, Fraser J, Lavitas LM, Dostie J, Pombo A, et al. Complexity of chromatin folding is captured by the strings and binders switch model. Proc Natl Acad Sci U S A 2012; 109:16173-16178. PMID:22988072. http://dx.doi.org/10.1073/pnas.1204799109
19. Nicodemi M, Panning B, Prisco A. A thermodynamic switch for chromosome colocalization. Genetics 2008; 179:717-721. PMID:18493085. http://dx.doi. org/10.1534/genetics.107.083154
20. Nicodemi M, Prisco A. Thermodynamic pathways to genome spatial organization in the cell nucleus. Biophys J 2009; 96:2168-2177. PMID:19289043. http://dx.doi.org/10.1016/j.bpj.2008.12.3919
21. Binder K. Applications of Monte Carlo methods to statistical physics. Rep Prog Phys 1997; 60:487. http://dx.doi.org/10.1088/0034-4885/60/5/001
22. Doi M, Edwards SF. The Theory of Polymer Dynamics. Oxford: Clarendon Press; 1984.
23. Stanley HE. Introduction to Phase Transitions and Critical Phenomena. Oxford: Clarendon Press; 1971.
24. Mateos-Langerak J, Bohn M, de Leeuw W, Giromus O, Manders EMM, Verschure PJ, et al. Spatially confined folding of chromatin in the interphase nucleus. Proc Natl Acad Sci U S A 2009; 106:3812-3817. PMID:19234129. http://dx.doi.org/10.1073/pnas.0809501106
25. de Gennes PG. Scaling concepts in polymer physics. Ithaca (NY): Cornell University Press; 1979.
26. Cataudella V, Franzese G, Nicodemi M, Scala A, Coniglio A. Critical clusters and efficient dynamics for frustrated spin models. Phys Rev Lett 1994; 72:1541-1544. PMID:10055635. http://dx.doi. org/10.1103/PhysRevLett.72.1541
27. Tarzia M, et al. Glass transition in granular media. Europhys Lett 2004; 66:531-537; http://dx.doi.org/10.1209/epl/i2004-10015-y
28. Coniglio A, Nicodemi M. The jamming transition of Granular Media. J Phys Condens Matter 2000; 12:6601-6610. http://dx.doi.org/10.1088/0953-8984/12/29/331
29. Coniglio A, et al. Segregation of granular mixtures in presence of compaction. Europhys Lett 1998; 43:591-7. http://dx.doi.org/10.1209/epl/i1998-00402-x
30. Nicodemi M, Jeldtoft Jensen H. Creep of super-conducting vortices in the limit of vanishing temperature: a fingerprint of off-equilibrium dynamics. Phys Rev Lett 2001; 86:4378-4381. PMID:11328179. http://dx.doi.org/10.1103/PhysRevLett.86.4378
31. Scialdone A, Cataudella I, Barbieri M, Prisco A, Nicodemi M. Conformation regulation of the X chromosome inactivation center: a model. PLoS Comput Biol 2011; 7:e1002229. PMID:22046112. http://dx.doi.org/10.1371/journal.pcbi.1002229
32. Nicodemi M, Prisco A. Symmetry-breaking model for X-chromosome inactivation. Phys Rev Lett 2007; 98:108104. PMID:17358571. http://dx.doi. org/10.1103/PhysRevLett.98.108104
33. Scialdone A, Barbieri M, Pallotti D, Nicodemi M. Mean-Field Theory of the Symmetry Breaking Model for X Chromosome Inactivation. Prog Theor Phys Sup 2011; 191:40. http://dx.doi.org/10.1143/PTPS.191.40
34. Zickler D, Kleckner N. The leptotene-zygotene transition of meiosis. Annu Rev Genet 1998; 32:619-697. PMID:9928494. http://dx.doi.org/10.1146/annurev. genet.32.1.619
35. Gerton JL, Hawley RS. Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat Rev Genet 2005; 6:477-487. PMID:15931171. http://dx.doi.org/10.1038/nrg1614
36. Scialdone A, Nicodemi M. Diffusion-based DNA target colocalization by thermodynamic mechanisms. Development 2010; 137:3877-3885. PMID:20978079. http://dx.doi.org/10.1242/dev.053322
37. Volpi EV, Chevret E, Jones T, Vatcheva R, Williamson J, Beck S, et al. Large-scale chromatin organization of the major histocompatibility complex and other regions of human chromosome 6 and its response to interferon in interphase nuclei. J Cell Sci 2000; 113:1565-1576. PMID:10751148
38. Chambeyron S, Bickmore WA. Does looping and clustering in the nucleus regulate gene expression? Curr Opin Cell Biol 2004; 16:256-262. PMID:15145349. http://dx.doi.org/10.1016/j.ceb.2004.03.004
39. Ferrai C, Xie SQ, Luraghi P, Munari D, Ramirez F, Branco MR, et al. Poised transcription factories prime silent uPA gene prior to activation. PLoS Biol 2010; 8:e1000270. PMID:20052287. http://dx.doi. org/10.1371/journal.pbio.1000270