Restraint-based three-dimensional modeling of genomes and genomic domains

FEBS Letters

Volumn 589, Issue 20, 2015, Pages 2987-2995

  Serra, François ^a,b   Di Stefano, Marco ^a,b   Spill, Yannick G ^a,b   Cuartero, Yasmina ^a,b   Goodstadt, Michael ^a,b   Baù, Davide ^a,b   Marti Renom, Marc A ^a,b,c  

^a Centre Nacional d'Analisi Genomica CNAG   (Spain)

^b CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

3D genome reconstruction; Chromosome Conformation Capture; Genome architecture; Restraint based modeling

Indexed keywords

ARTICLE; CONFORMATION; DATA PROCESSING; GENOME; HUMAN; MATHEMATICAL MODEL; PRIORITY JOURNAL; QUALITY CONTROL; SAMPLING; SCORING SYSTEM; THREE DIMENSIONAL IMAGING; ANIMAL; BIOLOGICAL MODEL; CHROMOSOME; COMPUTER SIMULATION; GENE EXPRESSION REGULATION; GENETICS; ULTRASTRUCTURE;

ANIMALS; CHROMOSOMES; COMPUTER SIMULATION; GENE EXPRESSION REGULATION; GENOME; HUMANS; MODELS, GENETIC; NUCLEIC ACID CONFORMATION;

EID: 84943197698     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2015.05.012     Document Type: Review

References (87)

1. B.E. Bernstein, E. Birney, I. Dunham, E.D. Green, C. Gunter, and M. Snyder An integrated encyclopedia of DNA elements in the human genome Nature 489 2012 57 74
2. S. Berlivet, D. Paquette, A. Dumouchel, D. Langlais, J. Dostie, and M. Kmita Clustering of tissue-specific sub-TADs accompanies the regulation of HoxA genes in developing limbs PLoS Genet. 9 2013 e1004018
3. J.R. Dixon, I. Jung, S. Selvaraj, Y. Shen, J.E. Antosiewicz-Bourget, A.Y. Lee, Z. Ye, A. Kim, N. Rajagopal, W. Xie, Y. Diao, J. Liang, H. Zhao, V.V. Lobanenkov, J.R. Ecker, J.A. Thomson, and B. Ren Chromatin architecture reorganization during stem cell differentiation Nature 518 2015 331 336
4. B.D. Pope, T. Ryba, V. Dileep, F. Yue, W. Wu, O. Denas, D.L. Vera, Y. Wang, R.S. Hansen, T.K. Canfield, R.E. Thurman, Y. Cheng, G. Gulsoy, J.H. Dennis, M.P. Snyder, J.A. Stamatoyannopoulos, J. Taylor, R.C. Hardison, T. Kahveci, B. Ren, and D.M. Gilbert Topologically associating domains are stable units of replication-timing regulation Nature 515 2014 402 405
5. F. Le Dily, D. Baù, A. Pohl, G.P. Vicent, F. Serra, D. Soronellas, G. Castellano, R.H. Wright, C. Ballare, G. Filion, M.A. Marti-Renom, and M. Beato Distinct structural transitions of chromatin topological domains correlate with coordinated hormone-induced gene regulation Genes Dev. 28 2014 2151 2162
6. J.R. Dixon, S. Selvaraj, F. Yue, A. Kim, Y. Li, Y. Shen, M. Hu, J.S. Liu, and B. Ren Topological domains in mammalian genomes identified by analysis of chromatin interactions Nature 485 2012 376 380
7. S.S. Rao, M.H. Huntley, N.C. Durand, E.K. Stamenova, I.D. Bochkov, J.T. Robinson, A.L. Sanborn, I. Machol, A.D. Omer, E.S. Lander, and E.L. Aiden A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping Cell 159 2014 1665 1680
8. J.G. Gall Chromosome structure and the C-value paradox J. Cell Biol. 91 1981 3s 14s
9. E.V. Chambers, W.A. Bickmore, and C.A. Semple Divergence of mammalian higher order chromatin structure is associated with developmental loci PLoS Comput. Biol. 9 2013 e1003017
10. J. Dekker, K. Rippe, M. Dekker, and N. Kleckner Capturing chromosome conformation Science 295 2002 1306 1311
11. M. Simonis, P. Klous, E. Splinter, Y. Moshkin, R. Willemsen, E. de Wit, B. van Steensel, and W. de Laat Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C) Nat. Genet. 38 2006 1348 1354
12. J. Dostie, T.A. Richmond, R.A. Arnaout, R.R. Selzer, W.L. Lee, T.A. Honan, E.D. Rubio, A. Krumm, J. Lamb, C. Nusbaum, R.D. Green, and J. Dekker Chromosome Conformation Capture Carbon Copy (5C): a massively parallel solution for mapping interactions between genomic elements Genome Res. 16 2006 1299 1309
13. E. Lieberman-Aiden, N.L. van Berkum, L. Williams, M. Imakaev, T. Ragoczy, A. Telling, I. Amit, B.R. Lajoie, P.J. Sabo, M.O. Dorschner, R. Sandstrom, B. Bernstein, M.A. Bender, M. Groudine, A. Gnirke, J. Stamatoyannopoulos, L.A. Mirny, E.S. Lander, and J. Dekker Comprehensive mapping of long-range interactions reveals folding principles of the human genome Science 326 2009 289 293
14. R. Kalhor, H. Tjong, N. Jayathilaka, F. Alber, and L. Chen Genome architectures revealed by tethered chromosome conformation capture and population-based modeling Nat. Biotechnol. 30 2011 90 98
15. P. Kolovos, H.J. van de Werken, N. Kepper, J. Zuin, R.W. Brouwer, C.E. Kockx, K.S. Wendt, I.W.F. van, F. Grosveld, and T.A. Knoch Targeted Chromatin Capture (T2C): a novel high resolution high throughput method to detect genomic interactions and regulatory elements Epigenet. Chromatin 7 2014 10
16. J.R. Hughes, N. Roberts, S. McGowan, D. Hay, E. Giannoulatou, M. Lynch, M. De Gobbi, S. Taylor, R. Gibbons, and D.R. Higgs Analysis of hundreds of cis-regulatory landscapes at high resolution in a single, high-throughput experiment Nat. Genet. 46 2014 205 212
17. S. Schoenfelder, M. Furlan-Magaril, B. Mifsud, F. Tavares-Cadete, R. Sugar, B.M. Javierre, T. Nagano, Y. Katsman, M. Sakthidevi, S.W. Wingett, E. Dimitrova, A. Dimond, L.B. Edelman, S. Elderkin, K. Tabbada, E. Darbo, S. Andrews, B. Herman, A. Higgs, E. LeProust, C.S. Osborne, J.A. Mitchell, N.M. Luscombe, and P. Fraser The pluripotent regulatory circuitry connecting promoters to their long-range interacting elements Genome Res. 25 2015 582 597
18. W.A. Bickmore The spatial organization of the human genome Annu. Rev. Genomics Hum. Genet. 2013
19. M.A. Marti-Renom, and L.A. Mirny Bridging the resolution gap in structural modeling of 3D genome organization PLoS Comput. Biol. 7 2011 e1002125
20. T. Cremer, G. Kreth, H. Koester, R.H. Fink, R. Heintzmann, M. Cremer, I. Solovei, D. Zink, and C. Cremer Chromosome territories, interchromatin domain compartment, and nuclear matrix: an integrated view of the functional nuclear architecture Crit. Rev. Eukaryot. Gene Expr. 10 2000 179 212
21. E.P. Nora, J. Dekker, and E. Heard Segmental folding of chromosomes: a basis for structural and regulatory chromosomal neighborhoods? BioEssays 35 2013 818 828
22. E.P. Nora, B.R. Lajoie, E.G. Schulz, L. Giorgetti, I. Okamoto, N. Servant, T. Piolot, N.L. van Berkum, J. Meisig, J. Sedat, J. Gribnau, E. Barillot, N. Bluthgen, J. Dekker, and E. Heard Spatial partitioning of the regulatory landscape of the X-inactivation centre Nature 485 2012 381 385
23. Z. Duan, and C.A. Blau The genome in space and time: does form always follow function? How does the spatial and temporal organization of a eukaryotic genome reflect and influence its functions? BioEssays 34 2012 800 810
24. E. Yaffe, and A. Tanay Probabilistic modeling of Hi-C contact maps eliminates systematic biases to characterize global chromosomal architecture Nat. Genet. 43 2011 1059 1065
25. M. Imakaev, G. Fudenberg, R.P. McCord, N. Naumova, A. Goloborodko, B.R. Lajoie, J. Dekker, and L.A. Mirny Iterative correction of Hi-C data reveals hallmarks of chromosome organization Nat. Methods 9 2012 999 1003
26. M. Hu, K. Deng, Z. Qin, and J.S. Liu Understanding spatial organizations of chromosomes via statistical analysis of Hi-C data Quant. Biol. 1 2013 156 174
27. D.M. Witten, and W.S. Noble On the assessment of statistical significance of three-dimensional colocalization of sets of genomic elements Nucleic Acids Res. 40 2012 3849 3855
28. J. Dekker, M.A. Marti-Renom, and L.A. Mirny Exploring the three-dimensional organization of genomes: interpreting chromatin interaction data Nat. Rev. Genet. 14 2013 390 403
29. A. Rosa, and C. Zimmer Computational models of large-scale genome architecture Int. Rev. Cell Mol. Biol. 307 2014 275 349
30. L.A. Mirny The fractal globule as a model of chromatin architecture in the cell Chromosome Res. 19 2011 37 51
31. M. Barbieri, M. Chotalia, J. Fraser, L.M. Lavitas, J. Dostie, A. Pombo, and M. Nicodemi A model of the large-scale organization of chromatin Biochem. Soc. Trans. 41 2013 508 512
32. D. Jost, P. Carrivain, G. Cavalli, and C. Vaillant Modeling epigenome folding: formation and dynamics of topologically associated chromatin domains Nucleic Acids Res. 42 2014 9553 9561
33. M. Emanuel, N.H. Radja, A. Henriksson, and H. Schiessel The physics behind the larger scale organization of DNA in eukaryotes Phys. Biol. 6 2009 025008
34. P. Hahnfeldt, J.E. Hearst, D.J. Brenner, R.K. Sachs, and L.R. Hlatky Polymer models for interphase chromosomes Proc. Natl. Acad. Sci. USA 90 1993 7854 7858
35. C. Münkel, and J. Langowski Chromosome structure predicted by a polymer model Phys. Rev. E 57 1998 5888
36. M. Di Stefano, A. Rosa, V. Belcastro, D. di Bernardo, and C. Micheletti Colocalization of coregulated genes: a steered molecular dynamics study of human chromosome 19 PLoS Comput. Biol. 9 2013 e1003019
37. Z. Zhang, G. Li, K.C. Toh, and W.K. Sung 3D chromosome modeling with semi-definite programming and Hi-C data J. Comput. Biol. 20 2013 831 846
38. A. Lesne, J. Riposo, P. Roger, A. Cournac, and J. Mozziconacci 3D genome reconstruction from chromosomal contacts Nat. Methods 11 2014 1141 1143
39. T. Nagano, Y. Lubling, T.J. Stevens, S. Schoenfelder, E. Yaffe, W. Dean, E.D. Laue, A. Tanay, and P. Fraser Single-cell Hi-C reveals cell-to-cell variability in chromosome structure Nature 502 2013 59 64
40. L. Giorgetti, R. Galupa, E.P. Nora, T. Piolot, F. Lam, J. Dekker, G. Tiana, and E. Heard Predictive polymer modeling reveals coupled fluctuations in chromosome conformation and transcription Cell 157 2014 950 963
41. Z. Duan, M. Andronescu, K. Schutz, S. McIlwain, Y.J. Kim, C. Lee, J. Shendure, S. Fields, C.A. Blau, and W.S. Noble A three-dimensional model of the yeast genome Nature 465 2010 363
42. F. Ay, E.M. Bunnik, N. Varoquaux, J.P. Vert, W.S. Noble, and K.G. Le Roch Multiple dimensions of epigenetic gene regulation in the malaria parasite Plasmodium falciparum: gene regulation via histone modifications, nucleosome positioning and nuclear architecture in P. falciparum BioEssays 2014
43. D. Baù, and M.A. Marti-Renom Genome structure determination via 3C-based data integration by the integrative modeling platform Methods 58 2012 300 306
44. C. Peng, L.Y. Fu, P.F. Dong, Z.L. Deng, J.X. Li, X.T. Wang, and H.Y. Zhang The sequencing bias relaxed characteristics of Hi-C derived data and implications for chromatin 3D modeling Nucleic Acids Res. 41 2013 e183
45. M. Hu, K. Deng, Z. Qin, J. Dixon, S. Selvaraj, J. Fang, B. Ren, and J.S. Liu Bayesian inference of spatial organizations of chromosomes PLoS Comput. Biol. 9 2013 e1002893
46. J. Fraser, M. Rousseau, S. Shenker, M.A. Ferraiuolo, Y. Hayashizaki, M. Blanchette, and J. Dostie Chromatin conformation signatures of cellular differentiation Genome Biol. 10 2009 R37
47. N. Varoquaux, F. Ay, W.S. Noble, and J.P. Vert A statistical approach for inferring the 3D structure of the genome Bioinformatics 30 2014 i26 i33
48. D. Meluzzi, and G. Arya Recovering ensembles of chromatin conformations from contact probabilities Nucleic Acids Res. 41 2013 63 75
49. M. Rousseau, J. Fraser, M.A. Ferraiuolo, J. Dostie, and M. Blanchette Three-dimensional modeling of chromatin structure from interaction frequency data using Markov chain Monte Carlo sampling BMC Bioinformatics 12 2011 414
50. D. Baù, A. Sanyal, B.R. Lajoie, E. Capriotti, M. Byron, J.B. Lawrence, J. Dekker, and M.A. Marti-Renom The three-dimensional folding of the alpha-globin gene domain reveals formation of chromatin globules Nat. Struct. Mol. Biol. 18 2011 107 114
51. A. Sanyal, D. Baù, M.A. Marti-Renom, and J. Dekker Chromatin globules: a common motif of higher order chromosome structure? Curr. Opin. Cell Biol. 23 2011 325 331
52. M.A. Umbarger, E. Toro, M.A. Wright, G.J. Porreca, D. Baù, S.H. Hong, M.J. Fero, L.J. Zhu, M.A. Marti-Renom, H.H. McAdams, L. Shapiro, J. Dekker, and G.M. Church The three-dimensional architecture of a bacterial genome and its alteration by genetic perturbation Mol. Cell 44 2011 252 264
53. H. Tjong, K. Gong, L. Chen, and F. Alber Physical tethering and volume exclusion determine higher-order genome organization in budding yeast Genome Res. 22 2012 1295 1305
54. F. Ay, E.M. Bunnik, N. Varoquaux, S.M. Bol, J. Prudhomme, J.P. Vert, W.S. Noble, and K.G. Le Roch Three-dimensional modeling of the P. falciparum genome during the erythrocytic cycle reveals a strong connection between genome architecture and gene expression Genome Res. 24 2014 974 988
55. J.M. Belton, R.P. McCord, J.H. Gibcus, N. Naumova, Y. Zhan, and J. Dekker Hi-C: a comprehensive technique to capture the conformation of genomes Methods 58 2012 268 276
56. J. Dekker, and L. Mirny Biological techniques: chromosomes captured one by one Nature 502 2013 45 46
57. L.M. Rapkin, D.R. Anchel, R. Li, and D.P. Bazett-Jones A view of the chromatin landscape Micron 43 2012 150 158
58. C. Flors, and W.C. Earnshaw Super-resolution fluorescence microscopy as a tool to study the nanoscale organization of chromosomes Curr. Opin. Chem. Biol. 15 2011 838 844
59. B. Huang, H. Babcock, and X. Zhuang Breaking the diffraction barrier: super-resolution imaging of cells Cell 143 2010 1047 1058
60. M.P. Scheffer, M. Eltsov, and A.S. Frangakis Evidence for short-range helical order in the 30-nm chromatin fibers of erythrocyte nuclei Proc. Natl. Acad. Sci. USA 108 2011 16992 16997
61. F. Song, P. Chen, D. Sun, M. Wang, L. Dong, D. Liang, R.M. Xu, P. Zhu, and G. Li Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units Science 344 2014 376 380
62. A.A. Gavrilov, E.S. Gushchanskaya, O. Strelkova, O. Zhironkina, I.I. Kireev, O.V. Iarovaia, and S.V. Razin Disclosure of a structural milieu for the proximity ligation reveals the elusive nature of an active chromatin hub Nucleic Acids Res. 41 2013 3563 3575
63. D. Russel, K. Lasker, B. Webb, J. Velazquez-Muriel, E. Tjioe, D. Schneidman-Duhovny, B. Peterson, and A. Sali Putting the pieces together: integrative modeling platform software for structure determination of macromolecular assemblies PLoS Biol. 10 2012 e1001244
64. F. Greil, C. Moorman, and B. van Steensel DamID: mapping of in vivo protein-genome interactions using tethered DNA adenine methyltransferase Methods Enzymol. 410 2006 342 359
65. J.F. Marko Micromechanical studies of mitotic chromosomes Chromosome Res. 16 2008 469 497
66. B.R. Lajoie, J. Dekker, and N. Kaplan The Hitchhiker's guide to Hi-C analysis: practical guidelines Methods 72 2015 65 75
67. N. Naumova, M. Imakaev, G. Fudenberg, Y. Zhan, B.R. Lajoie, L.A. Mirny, and J. Dekker Organization of the mitotic chromosome Science 342 2013 948 953
68. M. Trussart, F. Serra, D. Baù, I. Junier, L. Serrano, and M.A. Marti-Renom Assessing the limits of restraint-based 3D modeling of genomes and genomic domains Nucleic Acids Res. 2015
69. T.F. Havel, and M.E. Snow A new method for building protein conformations from sequence alignments with homologues of known structure J. Mol. Biol. 217 1991 1 7
70. T.F. Havel, and K. Wuthrich An evaluation of the combined use of nuclear magnetic resonance and distance geometry for the determination of protein conformations in solution J. Mol. Biol. 182 1985 281 294
71. J. Langowski, and D.W. Heermann Computational modeling of the chromatin fiber Semin. Cell Dev. Biol. 18 2007 659 667
72. D. Baù, and M.A. Marti-Renom Structure determination of genomic domains by satisfaction of spatial restraints Chromosome Res. 19 2011 25 35
73. A. Grosberg, S.K. Nechaev, and E.I. Shakhnovich The role of topological limitations in the kinetics of homopolymer collapse and self-assembly of biopolymers Biofizika 33 1988 247 253
74. P. Chen, P. Zhu, and G. Li New insights into the helical structure of 30-nm chromatin fibers Protein Cell 5 2014 489 491
75. A. Bassett, S. Cooper, C. Wu, and A. Travers The folding and unfolding of eukaryotic chromatin Curr. Opin. Genet. Dev. 19 2009 159 165
76. S.E. Gerchman, and V. Ramakrishnan Chromatin higher-order structure studied by neutron scattering and scanning transmission electron microscopy Proc. Natl. Acad. Sci. USA 84 1987 7802 7806
77. R. Ghirlando, and G. Felsenfeld Hydrodynamic studies on defined heterochromatin fragments support a 30-nm fiber having six nucleosomes per turn J. Mol. Biol. 376 2008 1417 1425
78. P.J. Robinson, L. Fairall, V.A. Huynh, and D. Rhodes EM measurements define the dimensions of the "30-nm" chromatin fiber: evidence for a compact, interdigitated structure Proc. Natl. Acad. Sci. USA 103 2006 6506 6511
79. K. Bystricky, P. Heun, L. Gehlen, J. Langowski, and S.M. Gasser Long-range compaction and flexibility of interphase chromatin in budding yeast analyzed by high-resolution imaging techniques Proc. Natl. Acad. Sci. USA 101 2004 16495 16500
80. G. Felsenfeld, and M. Groudine Controlling the double helix Nature 421 2003 448 453
81. F. Alber, M.F. Kim, and A. Sali Structural characterization of assemblies from overall shape and subcomplex compositions Structure 13 2005 435 445
82. X. Zhou, R.F. Lowdon, D. Li, H.A. Lawson, P.A. Madden, J.F. Costello, and T. Wang Exploring long-range genome interactions using the WashU Epigenome Browser Nat. Methods 10 2013 375 376
83. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
84. T.M. Asbury, M. Mitman, J. Tang, and W.J. Zheng Genome3D: a viewer-model framework for integrating and visualizing multi-scale epigenomic information within a three-dimensional genome BMC Bioinformatics 11 2010 444
85. M. Meyer, T. Munzner, A. DePace, and H. Pfister MulteeSum: a tool for comparative spatial and temporal gene expression data IEEE Trans. Visual Comput. Graphics 16 2010 908 917
86. S.I. O'Donoghue, K.S. Sabir, M. Kalemanov, C. Stolte, B. Wellmann, V. Ho, M. Roos, N. Perdigao, F.A. Buske, J. Heinrich, B. Rost, and A. Schafferhans Aquaria: simplifying discovery and insight from protein structures Nat. Methods 12 2015 98 99
87. Andrej Sali, Helen M. Berman, Torsten Schwede, Jill Trewhella, Gerard Kleywegt, Stephen K. Burley, John Markley, Haruki Nakamura, Paul Adams, Alexandre M.J.J. Bonvin, Wah Chiu, Matteo Dal Peraro, Frank Di Maio, Thomas E. Ferrin, Kay Grünewald, Aleksandras Gutmanas, Richard Henderson, Gerhard Hummer, Kenji Iwasaki, Graham Johnson, Catherine L. Lawson, Jens Meiler, Marc A. Marti-Renom, G.T. Montelione, Michael Nilges, Ruth Nussinov, Ardan Patwardhan, Juri Rappsilber, Randy J. Read, Helen Saibil, Gunnar F. Schröder, Charles Schwieters, Claus A.M. Seidel, Dmitri Svergun, Maya Topf, Eldon L. Ulrich, S. Velankar, J.D. Westbrook, Outcome of the first wwPDB hybrid/integrative methods task force workshop, Structure (2015) (accepted for publication).