Computational models of large-scale genome architecture

International Review of Cell and Molecular Biology

Volumn 307, Issue , 2014, Pages 275-349

  Rosa, Angelo ^a   Zimmer, Christophe ^b  

^a SISSA   (Italy)

^b CNRS   (France)

Author keywords

Chromosome conformation capture; Chromosomes; Computational models; Nuclear architecture; Polymer physics

Indexed keywords

MONOMER; POLYMER;

ARTICLE; BACTERIAL CHROMOSOME; BINDING AFFINITY; CHROMATIN; CHROMOSOME; CHROMOSOME SIZE; CHROMOSOME STRUCTURE; CONFORMATION; ENTROPY; GENE EXPRESSION; GENOME; GENOME ANALYSIS; HUMAN; MICELLE; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; SIMULATION;

CHROMOSOME CONFORMATION CAPTURE; CHROMOSOMES; COMPUTATIONAL MODELS; NUCLEAR ARCHITECTURE; POLYMER PHYSICS;

ANIMALS; CELL NUCLEUS; CHROMOSOMES, HUMAN; COMPUTER SIMULATION; GENOME, HUMAN; HUMANS; MODELS, BIOLOGICAL;

EID: 84891109077     PISSN: 19376448     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-800046-5.00009-6     Document Type: Chapter

References (107)

1. Alber F., Dokudovskaya S., Veenhoff L.M., Zhang W., Kipper J., Devos D., Suprapto A., Karni-Schmidt O., Williams R., Chait B.T., Rout M.P., Sali A. Determining the architectures of macromolecular assemblies. Nature 2007, 450:683-694.
2. Alberts B., Johnson A., Lewis J., Raff M., Roberts K., Walter P. Molecular Biology of the Cell: Reference Edition 2008, vol. 1. Garland Publishing, New York.
3. Allen M.P., Tildesley D.J. Computer Simulation of Liquids 1987, Oxford University Press, Oxford.
4. Barbieri M., Chotalia M., Fraser J., Lavitas L.-M., Dostie J., Pombo A., Nicodemi M. Complexity of chromatin folding is captured by the strings and binders switch model. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:16173-16178.
5. Baù D., Sanyal A., Lajoie B.R., Capriotti E., Byron M., Lawrence J.B., Dekker J., Marti-Renom M.A. The three-dimensional folding of the α-globin gene domain reveals formation of chromatin globules. Nat. Struct. Mol. Biol. 2011, 18:107-114.
6. Belmont A.S. Visualizing chromosome dynamics with GFP. Trends Cell Biol. 2001, 11:250-257.
7. Benoit H., Doty P.M. Light scattering from non-Gaussian chains. J. Phys. Chem. 1953, 57:958-963.
8. Berger A.B., Cabal G.G., Fabre E., Duong T., Buc H., Nehrbass U., Olivo-Marin J.C., Gadal O., Zimmer C. High-resolution statistical mapping reveals gene territories in live yeast. Nat. Methods 2008, 5:1031-1037.
9. Bickmore W.A., van Steensel B. Genome architecture: domain organization of interphase chromosomes. Cell 2013, 152:1270-1284.
10. Bohn Manfred, Heermann D., Van Driel R. Random loop model for long polymers. Phys. Rev. E 2007, 76:051805.
11. Boyle S. The spatial organization of human chromosomes within the nuclei of normal and emerin-mutant cells. Hum. Mol. Genet. 2001, 10:211-219.
12. Bystricky K., Heun P., Gehlen L., Langowski J., Gasser S.M. Long-range compaction and flexibility of interphase chromatin in budding yeast analyzed by high-resolution imaging techniques. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:16495-16500.
13. Bystricky K., Laroche T., Van Houwe G., Blaszczyk M., Gasser S.M. Chromosome looping in yeast: telomere pairing and coordinated movement reflect anchoring efficiency and territorial organization. J. Cell Biol. 2005, 168:375-387.
14. Cates M.E., Deutsch J. Conjectures on the statistics of ring polymers. J. Phys. France 1986, 47:2121-2128.
15. Cavalli G. Chromosome kissing. Curr. Opin. Genet. Dev. 2007, 17:443-450.
16. Cavalli G., Misteli T. Functional implications of genome topology. Nat. Struct. Mol. Biol. 2013, 20:290-299.
17. Cook P.R. The organization of replication and transcription. Science 1999, 284:1790-1795.
18. Cremer T., Cremer C. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat. Rev. Genet. 2001, 2:292-301.
19. Cremer T., Cremer M. Chromosome territories. Cold Spring Harb. Perspect. Biol. 2010, 2:a003889.
20. De Gennes P.G. Scaling Concepts in Polymer Physics 1979, Cornell University Press, Ithaca.
21. De Gennes P.G. Reptation of a polymer chain in the presence of fixed obstacles. J. Chem. Phys. 1971, 55:572.
22. De Laat W., Dekker J. 3C-based technologies to study the shape of the genome. Methods 2012, 58:189-191.
23. De Wit E., De Laat W. A decade of 3C technologies: insights into nuclear organization. Genes Dev. 2012, 26:11-24.
24. Dekker Job, Marti-Renom Marc A., Mirny L.A. Exploring the three-dimensional organization of genomes: interpreting chromatin interaction data. Nat. Rev. Genet. 2013, 14:390-403.
25. Dekker J., Rippe K., Dekker M., Kleckner N. Capturing chromosome conformation. Science 2002, 295:1306-1311.
26. Di Stefano M., Rosa A., Belcastro V., Di Bernardo D., Micheletti C. Colocalization of coregulated genes: a steered molecular dynamics study of human chromosome 19. PLoS Comput. Biol. 2013, 9:e1003019.
27. Dixon J.R., Selvaraj S., Yue F., Kim A., Li Y., Shen Y., Hu M., Liu J.S., Ren B. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 2012, 485:376-380.
28. Doi M., Edwards A.M. The Theory of Polymer Dynamics 1988, Oxford University Press, Oxford.
29. Dostie J., Bickmore W.A. Chromosome organization in the nucleus-charting new territory across the Hi-Cs. Curr. Opin. Genet. Dev. 2012, 22:125-131.
30. Duan Z., Andronescu M., Schutz K., McIlwain S., Kim Y.J., Lee C., Shendure J., Fields S., Blau C.A., Noble W.S. A three-dimensional model of the yeast genome. Nature 2010, 465:363-367.
31. Edelman L.B., Fraser P. Transcription factories: genetic programming in three dimensions. Curr. Opin. Genet. Dev. 2012, 22:110-114.
32. Eltsov M., MacLellan K.M., Maeshima K., Frangakis A.S., 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. U. S. A. 2008, 105:19732.
33. Flors C. DNA and chromatin imaging with super-resolution fluorescence microscopy based on single-molecule localization. Biopolymers 2011, 95:290-297.
34. Fraser J., Rousseau M., Shenker S., Ferraiuolo M.A., Hayashizaki Y., Blanchette M., Dostie J. Chromatin conformation signatures of cellular differentiation. Genome Biol. 2009, 10:R37.
35. Gasser S.M. Visualizing chromatin dynamics in interphase nuclei. Science (New York, NY) 2002, 296:1412-1416.
36. Gehlen L.R., Gruenert G., Jones M.B., Rodley C.D., Langowski Jörg, O'Sullivan J.M. Chromosome positioning and the clustering of functionally related loci in yeast is driven by chromosomal interactions. Nucleus 2012, 3(4):370-383.
37. Grosberg A.Y., Nechaev S.K., Shakhnovich E.I. The role of topological constraints in the kinetics of collapse of macromolecules. J. Phys. France 1988, 49:2095-2100.
38. Grosberg A.Y., Rabin Y., Havlin S., Neer A. Crumpled globule model of the three-dimensional structure of DNA. Europhys. Lett. 1993, 23:373-378.
39. Hadizadeh Yazdi N., Guet C.C., Johnson R.C., Marko J.F. Variation of the folding and dynamics of the Escherichia coli chromosome with growth conditions. Mol. Microbiol. 2012, 86:1318-1333.
40. Halperin A. On the collapse of multiblock copolymers. Macromolecules 1991, 24:1418-1419.
41. Harmandaris V.A., Reith D., Van der Vegt N.F.A., Kremer Kurt Comparison between coarse-graining models for polymer systems: two mapping schemes for polystyrene. Macromol. Chem. Phys. 2007, 208:2109-2120.
42. Heun P., Laroche T., Shimada K., Furrer P., Gasser S.M. Chromosome dynamics in the yeast interphase nucleus. Science 2001, 294:2181-2186.
43. Hu M., Deng K., Qin Z., Dixon J., Selvaraj S., Fang J., Ren B., Liu J.S. Bayesian inference of spatial organizations of chromosomes. PLoS Comput. Biol. 2013, 9:e1002893.
44. Huang K. Statistical Mechanics 1987, Wiley, New York. second ed.
45. Israelachvili J.N. Intermolecular and Surface Forces (Google eBook) 2011, Academic Press, London. Revised third ed.
46. Iyer B.V.S., Arya G. Lattice animal model of chromosome organization. Phys. Rev. E 2012, 86:011911.
47. Jackson D.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, 140:1285-1295.
48. Jhunjhunwala S., Van Zelm M.C., Peak M.M., Cutchin S., Riblet R., Van Dongen J.J.M., Grosveld F.G., Knoch T.A., Murre C. The 3D structure of the immunoglobulin heavy-chain locus: implications for long-range genomic interactions. Cell 2008, 133:265-279.
49. Jun S., Mulder B. Entropy-driven spatial organization of highly confined polymers: lessons for the bacterial chromosome. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:12388-12393.
50. 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.
51. Khokhlov A., Grosberg A. Statistical Physics of Macromolecules 1994, American Institute of Physics, New York.
52. Kim J.S., Pradhan P., Backman V., Szleifer I. The influence of chromosome density variations on the increase in nuclear disorder strength in carcinogenesis. Phys. Biol. 2011, 8:015004.
53. Kornberg R.D. Chromatin structure: a repeating unit of histones and DNA. Science 1974, 184:868-871.
54. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
55. Kremer K., Grest G.S. Dynamics of entangled linear polymer melts: a molecular-dynamics simulation. J. Chem. Phys. 1990, 92:5057-5086.
56. 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.
57. Lieberman-Aiden E., Van Berkum N.L., Williams L., Imakaev M., Ragoczy T., Telling A., Amit I., Lajoie B.R., Sabo P.J., Dorschner M.O., Sandstrom R., Bernstein B., Bender M.A., Groudine M., Gnirke A., Stamatoyannopoulos J., Mirny L.A., Lander E.S., Dekker Job Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science (New York, NY) 2009, 326:289-293.
58. Luger K., Dechassa M.L., Tremethick D.J. New insights into nucleosome and chromatin structure: an ordered state or a disordered affairα. Nat. Rev. Mol. Cell Biol. 2012, 13:436-447.
59. Maeshima K., Hihara S., Eltsov M. Chromatin structure: does the 30-nm fibre exist in vivoα. Curr. Opin. Cell Biol. 2010, 22:291-297.
60. Marenduzzo D., Micheletti C., Cook P.R. Entropy-driven genome organization. Biophys. J. 2006, 90:3712-3721.
61. Markaki Y., Smeets D., Fiedler S., Schmid V.J., Schermelleh L., Cremer T., Cremer M. The potential of 3D-FISH and super-resolution structured illumination microscopy for studies of 3D nuclear architecture: 3D structured illumination microscopy of defined chromosomal structures visualized by 3D (immuno)-FISH opens new perspectives for stud. BioEssays 2012, 34:412-426.
62. Marko J.F., Siggia E.D. Stretching DNA. Macromolecules 1995, 28:8759-8770.
63. Marti-Renom M.A., Mirny L.A. Bridging the resolution gap in structural modeling of 3D genome organization. PLoS Comput. Biol. 2011, 7:e1002125.
64. Mateos-Langerak J., Bohn M., De Leeuw W., Giromus O., Manders E.M.M., Verschure P.J., Indemans M.H.G., Gierman H.J., Heermann D.W., Van Driel R. Spatially confined folding of chromatin in the interphase nucleus. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:3812.
65. Mekhail K., Seebacher J., Gygi S.P., Moazed D. Role for perinuclear chromosome tethering in maintenance of genome stability. Nature 2008, 456:667-670.
66. Meluzzi D., Arya G. Recovering ensembles of chromatin conformations from contact probabilities. Nucleic Acids Res. 2013, 41:63-75.
67. Micheletti C. Comparing proteins by their internal dynamics: exploring structure-function relationships beyond static structural alignments. Phys. Life Rev. 2012, 10:1-26.
68. Misteli T. Higher-order genome organization in human disease. Cold Spring Harb. Perspect. Biol. 2010, 2:a000794.
69. Müller M., Wittmer J., Cates M. Topological effects in ring polymers: a computer simulation study. Phys. Rev. E 1996, 53:5063-5074.
70. Münkel C., Eils R., Dietzel S., Zink D., Mehring C., Wedemann G., Cremer T., Munkel C., Langowski J. Compartmentalization of interphase chromosomes observed in simulation and experiment. J. Mol. Biol. 1999, 285:1053-1065.
71. Münkel C., Langowski J. Chromosome structure predicted by a polymer model. Phys. Rev. E 1998, 57:5888-5896.
72. Ostashevsky J. A polymer model for the structural organization of chromatin loops and minibands in interphase. Mol. Biol. Cell 1998, 9:3031-3040.
73. Pelletier J., Halvorsen K., Ha B.-Y., Paparcone R., Sandler S.J., Woldringh C.L., Wong W.P., Jun S. Physical manipulation of the Escherichia coli chromosome reveals its soft nature. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E2649-E2656.
74. Possoz C., Junier I., Espeli O. Bacterial chromosome segregation. Front. Biosci. 2012, 17:1020-1034.
75. Rieping W., Habeck M., Nilges M. Inferential structure determination. Science 2005, 309:303.
76. Rippe K. Making contacts on a nucleic acid polymer. Trends Biochem. Sci. 2001, 26:733-740.
77. Rodley C.D.M., Bertels F., Jones B., O'Sullivan J.M. Global identification of yeast chromosome interactions using Genome conformation capture. Fungal Genet. Biol. 2009, 46:879-886.
78. Rosa A., Becker N.B., Everaers R. Looping probabilities in model interphase chromosomes. Biophys. J. 2010, 98:2410-2419.
79. Rosa A., Everaers R. Structure and dynamics of interphase chromosomes. PLoS Comput. Biol. 2008, 4.
80. Rouquette J., Cremer C., Cremer T., Fakan S. Functional nuclear architecture studied by microscopy: present and future. Int. Rev. Cell Mol. Biol. 2010, 282:1-90.
81. Rousseau M., Fraser J., Ferraiuolo M.A., Dostie J., Blanchette M. Three-dimensional modeling of chromatin structure from interaction frequency data using Markov chain Monte Carlo sampling. BMC Bioinformat. 2011, 12:414.
82. Rubinstein M., Colby R. Polymer Physics 2003, Oxford University Press, New York.
83. Sachs R.K., Van den Engh G., Trask B., Yokota H., Hearst J.E. A random-walk/giant-loop model for interphase chromosomes. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:2710-2714.
84. Schram R.D., Barkema G.T., Schiessel H. On the stability of fractal globules. J. Chem. Phys. 2013, 138:224901.
85. Shimada J., Yamakawa H. Ring-closure probabilities for twisted wormlike chains. Application to DNA. Macromolecules 1984, 17:689-698.
86. Sikorav J.L., Jannink G. Kinetics of chromosome condensation in the presence of topoisomerases: a phantom chain model. Biophys. J. 1994, 66:827-837.
87. Sumners D.W., Whittington S.G. Knots in self-avoiding walks. J. Phys. A Math. Genet. 1988, 21:1689-1694.
88. Taddei A., Schober H., Gasser S.M. The budding yeast nucleus. Cold Spring Harb. Perspect. Biol. 2010, 2:a000612.
89. Tanizawa H., Iwasaki O., Tanaka A., Capizzi J.R., Wickramasinghe P., Lee M., Fu Z., Noma K. Mapping of long-range associations throughout the fission yeast genome reveals global genome organization linked to transcriptional regulation. Nucleic Acids Res. 2010, 38:8164-8177.
90. Thérizols P., Duong T., Dujon B., Zimmer C., Fabre E. Chromosome arm length and nuclear constraints determine the dynamic relationship of yeast subtelomeres. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:2025.
91. Tjong H., Gong K., Chen L., Alber F. Physical tethering and volume exclusion determine higher-order genome organization in budding yeast. Genome Res. 2012, 22:1295-1305.
92. Toan N., Marenduzzo D., Cook P., Micheletti C. Depletion effects and loop formation in self-avoiding polymers. Phys. Rev. Lett. 2006, 97:178302.
93. Tokuda N., Terada T.P., Sasai M. Dynamical modeling of three-dimensional genome organization in interphase budding yeast. Biophys. J. 2012, 102:296-304.
94. Uchida N., Grest G.S., Everaers R. Viscoelasticity and primitive path analysis of entangled polymer liquids: from F-actin to polyethylene. J. Chem. Phys. 2008, 128:044902.
95. Umbarger M.A., Toro E., Wright M.A., Porreca G.J., Bau D., Hong S.H., Fero M.J., Zhu L.J., Marti-Renom M.A., McAdams H.H., Shapiro L., Dekker J., Church G.M. The three-dimensional architecture of a bacterial genome and its alteration by genetic perturbation. Mol. Cell 2011, 44:252-264.
96. Van Rensburg E.J.J., Madras N. A nonlocal Monte Carlo algorithm for lattice trees. J. Phys. A Math. Genet. 1992, 25:303-333.
97. Vanderzande C. Lattice Models of Polymers 1998, Cambridge University Press, Cambridge.
98. Vettorel T., Grosberg A.Y., Kremer K. Statistics of polymer rings in the melt: a numerical simulation study. Phys. Biol. 2009, 6:025013.
99. Viollier P.H., Thanbichler M., McGrath P.T., West L., Meewan M., McAdams H.H., Shapiro L. Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:9257-9262.
100. Wang X., Montero Llopis P., Rudner D.Z. Organization and segregation of bacterial chromosomes. Nat. Rev. Genet. 2013, 14:191-203.
101. Wiggins P.A., Cheveralls K.C., Martin J.S., Lintner R., Kondev J. Strong intranucleoid interactions organize the Escherichia coli chromosome into a nucleoid filament. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:4991-4995.
102. Wong H., Marie-Nelly H., Herbert S., Carrivain P., Blanc H., Koszul R., Fabre E., Zimmer C. A predictive computational model of the dynamic 3D interphase yeast nucleus. Curr. Biol. 2012, 22:1881-1890.
103. Yaffe E., Tanay A. Probabilistic modeling of Hi-C contact maps eliminates systematic biases to characterize global chromosomal architecture. Nat. Genet. 2011, 43:1059-1065.
104. Yoffe A.M., Prinsen P., Gopal A., Knobler C.M., Gelbart W.M., Ben-Shaul A. Predicting the sizes of large RNA molecules. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:16153-16158.
105. Yokota H., Van den Engh G., Hearst J.E., Sachs R.K., Trask B.J. 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.
106. Zhang Y., Heermann D.W. Loops determine the mechanical properties of mitotic chromosomes. PLoS One 2011, 6:e29225.
107. Zimmer C., Fabre E. Principles of chromosomal organization: lessons from yeast. J. Cell Biol. 2011, 192:723-733.