|
|
Computational inference of physical spatial organization of eukaryotic genomes |
Bingxiang Xu,Zhihua Zhang( ) |
CAS Key Laboratory of Genome Sciences and Information, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing 100101, China |
|
|
Abstract Background: Chromosomes are packed in the cell’s nucleus, and chromosomal conformation is critical to nearly all intranuclear biological reactions, including gene transcription and DNA replication. Nevertheless, chromosomal conformation is largely a mystery in terms of its formation and the regulatory machinery that accesses it.
Results: Thanks to recent technological developments, we can now probe chromatin interaction in substantial detail, boosting research interest in modeling genome spatial organization. Here, we review the current computational models that simulate chromosome dynamics, and explain the physical and topological properties of chromosomal conformation, as inferred from these newly generated data.
Conclusion: Novel models shall be developed to address questions beyond averaged structure in the near further.
|
Author Summary Genome is always working in the 3D space of the nucleus, and its 3D structure is critical for gene regulation. We review the computational methods that rebuild genome 3D structures from high throughput technologies, such as Hi-C. We also discuss the pros and cons in current methods and possible further directions in the field. |
Keywords
3D genome
models
simulation
|
|
Fund: |
Corresponding Author(s):
Zhihua Zhang
|
Online First Date: 17 November 2016
Issue Date: 01 December 2016
|
|
1 |
Dillon, N. (2008) The impact of gene location in the nucleus on transcriptional regulation. Dev. Cell, 15, 182–186
https://doi.org/10.1016/j.devcel.2008.07.013
pmid: 18694558
|
2 |
Miele, A. and Dekker, J. (2008) Long-range chromosomal interactions and gene regulation. Mol. Biosyst., 4, 1046–1057
https://doi.org/10.1039/b803580f
pmid: 18931780
|
3 |
Dekker, J., Rippe, K., Dekker, M., Kleckner, N. (2002) Capturing chromosome conformation. Science, 295,1306–1311
https://doi.org/10.1126/science.1067799
|
4 |
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. (2009) Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science, 326, 289–293
https://doi.org/10.1126/science.1181369
|
5 |
Cremer, M., Grasser, F., Lanctôt, C., Müller, S., Neusser, M., Zinner, R., Solovei, I. and Cremer, T. (2008) Multicolor 3D fluorescence in situ hybridization for imaging interphase chromosomes. In The Nucleus, Hancock. R. Ed. 463, 205–239, Germany: Springer
https://doi.org/10.1007/978-1-59745-406-3_15
pmid: 18951171
|
6 |
Song, F., Chen, P., Sun, D., Wang, M., Dong, L., Liang, D., Xu, R. M., Zhu, P. and Li, G. (2014) Cryo-EM study of the chromatin fiber reveals a double helix twisted by tetranucleosomal units. Science, 344, 376–380
https://doi.org/10.1126/science.1251413
pmid: 24763583
|
7 |
Zhu, P. and Li, G. (2016) Structural insights of nucleosome and the 30-nm chromatin fiber. Curr. Opin. Struct. Biol., 36, 106–115
https://doi.org/10.1016/j.sbi.2016.01.013
pmid: 26872330
|
8 |
Naumova, N., Imakaev, M., Fudenberg, G., Zhan, Y., Lajoie, B. R., Mirny, L. A. and Dekker, J. (2013) Organization of the mitotic chromosome. Science, 342, 948–953
https://doi.org/10.1126/science.1236083
pmid: 24200812
|
9 |
Tang, Z., Luo, O. J., Li, X., Zheng, M., Zhu, J. J., Szalaj, P., Trzaskoma, P., Magalska, A., Wlodarczyk, J., Ruszczycki, B., (2015) CTCF-mediated human 3D genome architecture reveals chromatin topology for transcription. Cell, 163, 1611–1627
https://doi.org/10.1016/j.cell.2015.11.024
pmid: 26686651
|
10 |
Bickmore, W. A. (2013) The spatial organization of the human genome. Annu. Rev. Genomics Hum. Genet., 14, 67–84
https://doi.org/10.1146/annurev-genom-091212-153515
pmid: 23875797
|
11 |
Selvaraj, S., R Dixon, J., Bansal, V. and Ren, B. (2013) Whole-genome haplotype reconstruction using proximity-ligation and shotgun sequencing. Nat. Biotechnol., 31, 1111–1118
https://doi.org/10.1038/nbt.2728
pmid: 24185094
|
12 |
Klenin, K., Merlitz, H. and Langowski, J. (1998) A Brownian dynamics program for the simulation of linear and circular DNA and other wormlike chain polyelectrolytes. Biophys. J., 74, 780–788
https://doi.org/10.1016/S0006-3495(98)74003-2
pmid: 9533691
|
13 |
Bednar, J., Furrer, P., Stasiak, A., Dubochet, J., Egelman, E. H. and Bates, A. D. (1994) The twist, writhe and overall shape of supercoiled DNA change during counterion-induced transition from a loosely to a tightly interwound superhelix: possible implications for DNA structure in vivo. J. Mol. Biol., 235, 825–847
https://doi.org/10.1006/jmbi.1994.1042
pmid: 8289322
|
14 |
Gr�nbech-Jensen, N., Mashl, R. J., Bruinsma, R. F. and Gelbart, W. M. (1997) Counterion-induced attraction between rigid polyelectrolytes. Phys. Rev. Lett., 78, 2477–2480
https://doi.org/10.1103/PhysRevLett.78.2477
|
15 |
Langowski, J. and Heermann, D. W. (2007) Computational modeling of the chromatin fiber. Semin. Cell. Dev. Biol., 235, 659–667
|
16 |
Meluzzi, D. and Arya, G. (2013) Recovering ensembles of chromatin conformations from contact probabilities. Nucleic Acids Res., 41, 63–75
https://doi.org/10.1093/nar/gks1029
pmid: 23143266
|
17 |
Tolhuis, B., Palstra, R. J., Splinter, E., Grosveld, F. and de Laat, W. (2002) Looping and interaction between hypersensitive sites in the active β-globin locus. Mol. Cell, 10, 1453–1465
https://doi.org/10.1016/S1097-2765(02)00781-5
pmid: 12504019
|
18 |
Brackley, C. A., Brown, J. M., Waithe, D., Babbs, C., Davies, J., Hughes, J. R., Buckle, V. J. and Marenduzzo, D. (2016) Predicting the three-dimensional folding of cis-regulatory regions in mammalian genomes using bioinformatic data and polymer models. Genome Biol., 17, 59
https://doi.org/10.1186/s13059-016-0909-0
pmid: 27036497
|
19 |
Rosa, A. and Everaers, R. (2008) Structure and dynamics of interphase chromosomes. PLoS Comput. Biol., 4, e1000153
https://doi.org/10.1371/journal.pcbi.1000153
pmid: 18725929
|
20 |
Tokuda, N., Terada, T. P. and Sasai, M. (2012) Dynamical modeling of three-dimensional genome organization in interphase budding yeast. Biophys. J., 102, 296–304
https://doi.org/10.1016/j.bpj.2011.12.005
pmid: 22339866
|
21 |
Fudenberg, G. and Mirny, L. A. (2012) Higher-order chromatin structure: bridging physics and biology. Curr. Opin. Genet. Dev., 22, 115–124
https://doi.org/10.1016/j.gde.2012.01.006
pmid: 22360992
|
22 |
Tark-Dame, M., van Driel, R. and Heermann, D. W. (2011) Chromatin folding—from biology to polymer models and back. J. Cell Sci., 124, 839–845
https://doi.org/10.1242/jcs.077628
pmid: 21378305
|
23 |
Mateos-Langerak, J., Bohn, M., de Leeuw, W., Giromus, O., Manders, E. M., Verschure, P. J., Indemans, M. H., Gierman, H. J., Heermann, D. W., van Driel, R., (2009) Spatially confined folding of chromatin in the interphase nucleus. Proc. Natl. Acad. Sci. USA, 106, 3812–3817
https://doi.org/10.1073/pnas.0809501106
pmid: 19234129
|
24 |
Marko, J. F. and Siggia, E. D. (1997) Polymer models of meiotic and mitotic chromosomes. Mol. Biol. Cell, 8, 2217–2231
https://doi.org/10.1091/mbc.8.11.2217
pmid: 9362064
|
25 |
Göndör, A. and Ohlsson, R. (2009) Chromosome crosstalk in three dimensions. Nature, 461, 212–217
https://doi.org/10.1038/nature08453
pmid: 19741702
|
26 |
Kadauke, S. and Blobel, G. A. (2009) Chromatin loops in gene regulation. Biochim. Biophys. Acta, 1789, 17–25
https://doi.org/10.1016/j.bbagrm.2008.07.002
pmid: 18675948
|
27 |
Bohn, M. and Heermann, D. W. (2010) Diffusion-driven looping provides a consistent framework for chromatin organization. PLoS One, 5, e12218
https://doi.org/10.1371/journal.pone.0012218
pmid: 20811620
|
28 |
Nicodemi, M., Panning, B. and Prisco, A. (2008) A thermodynamic switch for chromosome colocalization. Genetics, 179, 717–721
https://doi.org/10.1534/genetics.107.083154
pmid: 18493085
|
29 |
Alipour, E. and Marko, J. F. (2012) Self-organization of domain structures by DNA-loop-extruding enzymes. Nucleic Acids Res., 40, 11202–11212
https://doi.org/10.1093/nar/gks925
pmid: 23074191
|
30 |
Grosberg, A. Iu., Nechaev, S. K. and Shakhnovich, E. I. (1988) The role of topological limitations in the kinetics of homopolymer collapse and self-assembly of biopolymers. Biofizika, 33, 247–253
pmid: 3390477
|
31 |
Nicodemi, M., Panning, B. and Prisco, A. (2008) A thermodynamic switch for chromosome colocalization. Genetics, 179, 717–721
https://doi.org/10.1534/genetics.107.083154
pmid: 18493085
|
32 |
Barbieri, M., Chotalia, M., Fraser, J., Lavitas, L. M., Dostie, J., Pombo, A. and Nicodemi, M. (2012) Complexity of chromatin folding is captured by the strings and binders switch model. Proc. Natl. Acad. Sci. USA, 109, 16173–16178
https://doi.org/10.1073/pnas.1204799109
pmid: 22988072
|
33 |
Goloborodko, A., Marko, J. F. and Mirny, L. A. (2016) Chromosome compaction by active loop extrusion. Biophys. J., 110, 2162–2168
https://doi.org/10.1016/j.bpj.2016.02.041
pmid: 27224481
|
34 |
Rao, S. S., Huntley, M. H., Durand, N. C., Stamenova, E. K., Bochkov, I. D., Robinson, J. T., Sanborn, A. L., Machol, I., Omer, A. D., Lander, E. S., (2014) A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell, 159, 1665–1680
https://doi.org/10.1016/j.cell.2014.11.021
pmid: 25497547
|
35 |
Fudenberg, G., Imakaev, M., Lu, C., Goloborodko, A., Abdennur, N., Mimy, L.A. (2015) Formation of chromosomal domains by loop extrusion. Cell Rep., 15, 2038–2049
|
36 |
Gruber, S. (2014) Multilayer chromosome organization through DNA bending, bridging and extrusion. Curr. Opin. Microbiol., 22, 102–110
https://doi.org/10.1016/j.mib.2014.09.018
pmid: 25460803
|
37 |
Simonis, M., Klous, P., Splinter, E., Moshkin, Y., Willemsen, R., de Wit, E., van Steensel, B. and de Laat, W. (2006) Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat. Genet., 38, 1348–1354
https://doi.org/10.1038/ng1896
pmid: 17033623
|
38 |
Dostie, J., Richmond, T. A., Arnaout, R. A., Selzer, R. R., Lee, W. L., Honan, T. A., Rubio, E. D., Krumm, A., Lamb, J., Nusbaum, C., (2006) Chromosome Conformation Capture Carbon Copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res., 16, 1299–1309
https://doi.org/10.1101/gr.5571506
pmid: 16954542
|
39 |
Zhang, J., Poh, H. M., Peh, S. Q., Sia, Y. Y., Li, G., Mulawadi, F. H., Goh, Y., Fullwood, M. J., Sung, W. K., Ruan, X., (2012) ChIA-PET analysis of transcriptional chromatin interactions. Methods, 58, 289–299
https://doi.org/10.1016/j.ymeth.2012.08.009
pmid: 22926262
|
40 |
Denker, A. and de Laat, W. (2016) The second decade of 3C technologies: detailed insights into nuclear organization. Genes Dev., 30, 1357–1382
https://doi.org/10.1101/gad.281964.116
pmid: 27340173
|
41 |
Duan, Z., Andronescu, M., Schutz, K., McIlwain, S., Kim, Y. J., Lee, C., Shendure, J., Fields, S., Blau, C. A. and Noble, W. S. (2010) A three-dimensional model of the yeast genome. Nature, 465, 363–367
https://doi.org/10.1038/nature08973
pmid: 20436457
|
42 |
Sexton, T., Yaffe, E., Kenigsberg, E., Bantignies, F., Leblanc, B., Hoichman, M., Parrinello, H., Tanay, A. and Cavalli, G. (2012) Three-dimensional folding and functional organization principles of the Drosophila genome. Cell, 148, 458–472
https://doi.org/10.1016/j.cell.2012.01.010
pmid: 22265598
|
43 |
Zhang, Y., McCord, R. P., Ho, Y. J., Lajoie, B. R., Hildebrand, D. G., Simon, A. C., Becker, M. S., Alt, F. W. and Dekker, J. (2012) Spatial organization of the mouse genome and its role in recurrent chromosomal translocations. Cell, 148, 908–921
https://doi.org/10.1016/j.cell.2012.02.002
pmid: 22341456
|
44 |
Hübner, M. R. and Spector, D. L. (2010) Chromatin dynamics. Annu. Rev. Biophys., 39, 471–489
https://doi.org/10.1146/annurev.biophys.093008.131348
pmid: 20462379
|
45 |
Lesne, A., Riposo, J., Roger, P., Cournac, A. and Mozziconacci, J. (2014) 3D genome reconstruction from chromosomal contacts. Nat. Methods, 11, 1141–1143
https://doi.org/10.1038/nmeth.3104
pmid: 25240436
|
46 |
Zhang, Z., Li, G., Toh, K. C. and Sung, W. K. (2013) 3D chromosome modeling with semi-definite programming and Hi-C data. J. Comput. Biol., 20, 831–846
https://doi.org/10.1089/cmb.2013.0076
pmid: 24195706
|
47 |
Varoquaux, N., Ay, F., Noble, W. S. and Vert, J. P. (2014) A statistical approach for inferring the 3D structure of the genome. Bioinformatics, 30, i26–i33
https://doi.org/10.1093/bioinformatics/btu268
pmid: 24931992
|
48 |
Peng, C., Fu, L. Y., Dong, P. F., Deng, Z. L., Li, J. X., Wang, X. T. and Zhang, H. Y. (2013) The sequencing bias relaxed characteristics of Hi-C derived data and implications for chromatin 3D modeling. Nucleic Acids Res., 41, e183
https://doi.org/10.1093/nar/gkt745
pmid: 23965308
|
49 |
Ba�, D. and Marti-Renom, M. A. (2012) Genome structure determination via 3C-based data integration by the Integrative Modeling Platform. Methods, 58, 300–306
https://doi.org/10.1016/j.ymeth.2012.04.004
pmid: 22522224
|
50 |
Zou, C., Zhang, Y. and Ouyang, Z. (2016) HSA: integrating multi-track Hi-C data for genome-scale reconstruction of 3D chromatin structure. Genome Biol., 17, 40
https://doi.org/10.1186/s13059-016-0896-1
pmid: 26936376
|
51 |
Nowotny, J., Ahmed, S., Xu, L., Oluwadare, O., Chen, H., Hensley, N., Trieu, T., Cao, R. and Cheng, J. (2015) Iterative reconstruction of three-dimensional models of human chromosomes from chromosomal contact data. BMC Bioinformatics, 16, 338
https://doi.org/10.1186/s12859-015-0772-0
pmid: 26493399
|
52 |
Trieu, T. and Cheng, J. (2014) Large-scale reconstruction of 3D structures of human chromosomes from chromosomal contact data. Nucleic Acids Res., 42, e52
https://doi.org/10.1093/nar/gkt1411
pmid: 24465004
|
53 |
Serra, F., Di Stefano, M., Spill, Y. G., Cuartero, Y., Goodstadt, M., Ba�, D. and Marti-Renom, M. A. (2015) Restraint-based three-dimensional modeling of genomes and genomic domains. FEBS Lett., 589, 2987–2995
https://doi.org/10.1016/j.febslet.2015.05.012
pmid: 25980604
|
54 |
Yaffe, E. and Tanay, A. (2011) Probabilistic modeling of Hi-C contact maps eliminates systematic biases to characterize global chromosomal architecture. Nat. Genet., 43, 1059–1065
https://doi.org/10.1038/ng.947
pmid: 22001755
|
55 |
Wang, S., Xu, J. and Zeng, J. (2015) Inferential modeling of 3D chromatin structure. Nucleic Acids Res., 43, e54.
https://doi.org/10.1093/nar/gkv100
pmid: 25690896
|
56 |
Tjong, H., Li, W., Kalhor, R., Dai, C., Hao, S., Gong, K., Zhou, Y., Li, H., Zhou, X. J., Le Gros, M. A., (2016) Population-based 3D genome structure analysis reveals driving forces in spatial genome organization. Proc. Natl. Acad. Sci. USA, 113, E1663–E1672
https://doi.org/10.1073/pnas.1512577113
pmid: 26951677
|
57 |
Rousseau, M., Fraser, J., Ferraiuolo, M. A., Dostie, J. and Blanchette, M. (2011) Three-dimensional modeling of chromatin structure from interaction frequency data using Markov chain Monte Carlo sampling. BMC Bioinformatics, 12, 414
https://doi.org/10.1186/1471-2105-12-414
pmid: 22026390
|
58 |
Hu, M., Deng, K., Qin, Z., Dixon, J., Selvaraj, S., Fang, J., Ren, B. and Liu, J. S. (2013) Bayesian inference of spatial organizations of chromosomes. PLoS Comput. Biol., 9, e1002893
https://doi.org/10.1371/journal.pcbi.1002893
pmid: 23382666
|
59 |
He, C., Wang, X. and Zhang, M. Q. (2014) Nucleosome eviction and multiple co-factor binding predict estrogen-receptor-alpha-associated long-range interactions. Nucleic Acids Res., 42, 6935–6944
https://doi.org/10.1093/nar/gku327
pmid: 24782518
|
60 |
Dixon, J. R., Selvaraj, S., Yue, F., Kim, A., Li, Y., Shen, Y., Hu, M., Liu, J. S. and Ren, B. (2012) Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature, 485, 376– 380
https://doi.org/10.1038/nature11082
pmid: 22495300
|
61 |
Ho, J. W., Jung, Y. L., Liu, T., Alver, B. H., Lee, S., Ikegami, K., Sohn, K. A., Minoda, A., Tolstorukov, M. Y., Appert, A., (2014) Comparative analysis of metazoan chromatin organization. Nature, 512, 449–452
https://doi.org/10.1038/nature13415
pmid: 25164756
|
62 |
Fortin, J. P. and Hansen, K. D. (2015) Reconstructing A/B compartments as revealed by Hi-C using long-range correlations in epigenetic data. Genome Biol., 16, 180
https://doi.org/10.1186/s13059-015-0741-y
pmid: 26316348
|
63 |
Huang, J., Marco, E., Pinello, L. and Yuan, G. C. (2015) Predicting chromatin organization using histone marks. Genome Biol., 16, 162
https://doi.org/10.1186/s13059-015-0740-z
pmid: 26272203
|
64 |
Zhang, Z. and Zhang, M. Q. (2011) Histone modification profiles are predictive for tissue/cell-type specific expression of both protein-coding and microRNA genes. BMC Bioinformatics, 12, 155
https://doi.org/10.1186/1471-2105-12-155
pmid: 21569556
|
65 |
Wang, Z., Zang, C., Rosenfeld, J. A., Schones, D. E., Barski, A., Cuddapah, S., Cui, K., Roh, T. Y., Peng, W., Zhang, M. Q., (2008) Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet., 40, 897–903
https://doi.org/10.1038/ng.154
pmid: 18552846
|
66 |
Karlić, R., Chung, H. R., Lasserre, J., Vlahovicek, K. and Vingron, M. (2010) Histone modification levels are predictive for gene expression. Proc. Natl. Acad. Sci. USA, 107, 2926–2931
https://doi.org/10.1073/pnas.0909344107
pmid: 20133639
|
67 |
Allis, C. D., Jenuwein, T., Reinberg, D., Caparros, M. (2015) Epigenetics. New York: Cold Spring Harbor Laboratory Press
|
68 |
Zhu, Y., Chen, Z., Zhang, K., Wang, M., Medovoy, D., Whitaker, J. W., Ding, B., Li, N., Zheng, L. and Wang, W. (2016) Constructing 3D interaction maps from 1D epigenomes. Nat. Commun., 7, 10812
https://doi.org/10.1038/ncomms10812
pmid: 26960733
|
69 |
Chen, Y., Wang, Y., Xuan, Z., Chen, M. and Zhang, M. Q. (2016) De novo deciphering three-dimensional chromatin interaction and topological domains by wavelet transformation of epigenetic profiles. Nucleic Acids Res., 44, e106
https://doi.org/10.1093/nar/gkw225
pmid: 27060148
|
70 |
Whalen, S., Truty, R. M. and Pollard, K. S. (2016) Enhancer-promoter interactions are encoded by complex genomic signatures on looping chromatin. Nat. Genet., 48, 488–496
https://doi.org/10.1038/ng.3539
pmid: 27064255
|
71 |
The ENCODE Project Consortium. (2012) An integrated encyclopedia of DNA elements in the human genome. Nature, 489, 57–74
https://doi.org/10.1038/nature11247
pmid: 22955616
|
72 |
Kornberg, R. D. and Stryer, L. (1988) Statistical distributions of nucleosomes: nonrandom locations by a stochastic mechanism. Nucleic Acids Res., 16, 6677–6690
https://doi.org/10.1093/nar/16.14.6677
pmid: 3399412
|
73 |
Kalhor, R., Tjong, H., Jayathilaka, N., Alber, F. and Chen, L. (2011) Genome architectures revealed by tethered chromosome conformation capture and population-based modeling. Nat. Biotechnol., 30, 90–98
https://doi.org/10.1038/nbt.2057
pmid: 22198700
|
74 |
Giorgetti, L., Galupa, R., Nora, E. P., Piolot, T., Lam, F., Dekker, J., Tiana, G. and Heard, E. (2014) Predictive polymer modeling reveals coupled fluctuations in chromosome conformation and transcription. Cell, 157, 950–963
https://doi.org/10.1016/j.cell.2014.03.025
pmid: 24813616
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|