Three-dimensional modeling of chromatin structure from interaction frequency data using Markov chain Monte Carlo sampling

BMC Bioinformatics

Volumn 12, Issue , 2011, Pages

  Rousseau, Mathieu ^a   Fraser, James ^b   Ferraiuolo, Maria A ^b   Dostie, Josée ^b   Blanchette, Mathieu ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR DIFFERENTIATION; INTERACTION FREQUENCIES; LONG RANGE INTERACTIONS; MARKOV CHAIN MONTE CARLO; MARKOV CHAIN MONTE CARLO SAMPLINGS; POSTERIOR DISTRIBUTIONS; THREE-DIMENSIONAL MODEL; TRANSCRIPTIONAL CONTROL;

CONFORMATIONS; GENES; MONTE CARLO METHODS; STRUCTURAL PROPERTIES;

THREE DIMENSIONAL;

HOMEODOMAIN PROTEIN;

ARTICLE; BIOLOGICAL MODEL; CHEMISTRY; CHROMATIN; CHROMOSOME 14; COMPUTER SIMULATION; GENETICS; HUMAN; HUMAN GENOME; METABOLISM; MONTE CARLO METHOD; PROBABILITY; REGULATORY SEQUENCE; TUMOR CELL LINE;

CELL LINE, TUMOR; CHROMATIN; CHROMOSOMES, HUMAN, PAIR 14; COMPUTER SIMULATION; GENOME, HUMAN; HOMEODOMAIN PROTEINS; HUMANS; MARKOV CHAINS; MODELS, BIOLOGICAL; MONTE CARLO METHOD; REGULATORY SEQUENCES, NUCLEIC ACID;

EID: 80054875965     PISSN: None     EISSN: 14712105     Source Type: Journal    
DOI: 10.1186/1471-2105-12-414     Document Type: Article

References (59)

1. Fraser P, Bickmore W. Nuclear organization of the genome and the potential for gene regulation. Nature 2007, 447(7143):413-7. 10.1038/nature05916, 17522674.
2. Babu MM, Janga SC, de Santiago I, Pombo A. Eukaryotic gene regulation in three dimensions and its impact on genome evolution. Curr Opin Genet Dev 2008, 18(6):571-82. 10.1016/j.gde.2008.10.002, 19007886.
3. Berger SL. The complex language of chromatin regulation during transcription. Nature 2007, 447(7143):407-12. 10.1038/nature05915, 17522673.
4. Kharchenko PV, Woo CJ, Tolstorukov MY, Kingston RE, Park PJ. Nucleosome positioning in human HOX gene clusters. Genome Res 2008, 18(10):1554-61. 10.1101/gr.075952.107, 2556261, 18723689.
5. Cook PR. A model for all genomes: the role of transcription factories. J Mol Biol 2010, 395:1-10. 10.1016/j.jmb.2009.10.031, 19852969.
6. Ferraiuolo MA, Rousseau M, Miyamoto C, Shenker S, Wang XQD, Nadler M, Blanchette M, Dostie J. The three-dimensional architecture of Hox cluster silencing. Nucleic Acids Res 2010,
7. Hon G, Wang W, Ren B. Discovery and annotation of functional chromatin signatures in the human genome. PLoS Comput Biol 2009, 5(11):e1000566. 10.1371/journal.pcbi.1000566, 2775352, 19918365.
8. Hon G, Ren B, Wang W. ChromaSig: a probabilistic approach to finding common chromatin signatures in the human genome. PLoS Comput Biol 2008, 4(10):e1000201. 10.1371/journal.pcbi.1000201, 2556089, 18927605.
9. Won KJ, Chepelev I, Ren B, Wang W. Prediction of regulatory elements in mammalian genomes using chromatin signatures. BMC Bioinformatics 2008, 9:547. 10.1186/1471-2105-9-547, 2657164, 19094206.
10. Woodcock CL. Chromatin architecture. Curr Opin Struct Biol 2006, 16(2):213-20. 10.1016/j.sbi.2006.02.005, 16540311.
11. West AG, Fraser P. Remote control of gene transcription. Hum Mol Genet 2005, 14 Spec No 1:R101-11.
12. Göndör A, Ohlsson R. Chromosome crosstalk in three dimensions. Nature 2009, 461(7261):212-7. 10.1038/nature08453, 19741702.
13. Kanduri C, Pant V, Loukinov D, Pugacheva E, Qi CF, Wolffe A, Ohlsson R, Lobanenkov VV. Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive. Curr Biol 2000, 10(14):853-6. 10.1016/S0960-9822(00)00597-2, 10899010.
14. Hark AT, Schoenherr CJ, Katz DJ, Ingram RS, Levorse JM, Tilghman SM. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 2000, 405(6785):486-9. 10.1038/35013106, 10839547.
15. Bell AC, Felsenfeld G. Methylation of a CTCF- dependent boundary controls imprinted expression of the Igf2 gene. Nature 2000, 405(6785):482-5. 10.1038/35013100, 10839546.
16. Court F, Baniol M, Hagege H, Petit JS, Lelay-Taha MN, Carbonell F, Weber M, Cathala G, Forne T. Long-range chromatin interactions at the mouse Igf2/H19 locus reveal a novel paternally expressed long non-coding RNA. Nucleic Acids Res 2011,
17. Baù D, Sanyal A, Lajoie BR, Capriotti E, Byron M, Lawrence JB, Dekker J, Marti-Renom MA. The three-dimensional folding of the alpha-globin gene do- main reveals formation of chromatin globules. Nat Struct Mol Biol 2011, 18:107-14. 10.1038/nsmb.1936, 3056208, 21131981.
18. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO, Sandstrom R, Bernstein B, Bender MA, Groudine M, Gnirke A, Stamatoyannopoulos J, Mirny LA, Lander ES, Dekker J. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 2009, 326(5950):289-293. 10.1126/science.1181369, 2858594, 19815776.
19. Fraser J, Rousseau M, Shenker S, Ferraiuolo M, Hayashizaki Y, Blanchette M, Dostie J. Chromatin conformation signatures of cellular differentiation. Genome Biology 2009, 10(4):R37. 10.1186/gb-2009-10-4-r37, 2688928, 19374771., http://genomebiology.com/2009/10/4/R37
20. Tolhuis B, Palstra RJ, Splinter E, Grosveld F, de Laat W. Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol Cell 2002, 10(6):1453-65. 10.1016/S1097-2765(02)00781-5, 12504019.
21. van Steensel B, Henikoff S. Identification of in vivo DNA targets of chromatin proteins using tethered dam methyltransferase. Nat Biotechnol 2000, 18(4):424-8. 10.1038/74487, 10748524.
22. Dekker J, Rippe K, Dekker M, Kleckner N. Capturing chromosome conformation. Science 2002, 295(5558):1306-11. 10.1126/science.1067799, 11847345.
23. Simonis M, Klous P, Splinter E, Moshkin Y, Willemsen R, de Wit E, van Steensel B, de Laat W. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nat Genet 2006, 38(11):1348-54. 10.1038/ng1896, 17033623.
24. Zhao Z, Tavoosidana G, Sjölinder M, Göndör A, Mariano P, Wang S, Kanduri C, Lezcano M, Sandhu KS, Singh U, Pant V, Tiwari V, Kurukuti S, Ohlsson R. Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra-and interchromosomal interactions. Nat Genet 2006, 38(11):1341-7. 10.1038/ng1891, 17033624.
25. Dostie J, Richmond TA, Arnaout RA, Selzer RR, Lee WL, Honan TA, Rubio ED, Krumm A, Lamb J, Nusbaum C, Green RD, Dekker J. Chromosome Conformation Capture Carbon Copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res 2006, 16(10):1299-309. 10.1101/gr.5571506, 1581439, 16954542.
26. Li G, Fullwood MJ, Xu H, Mulawadi FH, Velkov S, Vega V, Ariyaratne PN, Mohamed YB, Ooi HS, Tennakoon C, Wei CL, Ruan Y, Sung WK. ChIA-PET tool for comprehensive chromatin interaction analysis with paired-end tag sequencing. Genome Biol 2010, 11(2):R22. 10.1186/gb-2010-11-2-r22, 2872882, 20181287.
27. Duan Z, Andronescu M, Schutz K, McIlwain S, Kim YJ, Lee C, Shendure J, Fields S, Blau CA, Noble WS. A three-dimensional model of the yeast genome. Nature 2010,
28. Baù D, Marti-Renom MA. Structure determination of genomic domains by satisfaction of spatial restraints. Chromosome Res 2010,
29. Tanizawa H, Iwasaki O, Tanaka A, Capizzi J, 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(22):8164-77. 10.1093/nar/gkq955, 3001101, 21030438.
30. Metzler D, Nebel ME. Predicting RNA secondary structures with pseudoknots by MCMC sampling. J Math Biol 2008, 56(1-2):161-81.
31. Meyer IM, Miklós I. SimulFold: simultaneously inferring RNA structures including pseudoknots, alignments, and trees using a Bayesian MCMC framework. PLoS Comput Biol 2007, 3(8):e149. 10.1371/journal.pcbi.0030149, 1941756, 17696604.
32. Boomsma W, Mardia KV, Taylor CC, Ferkinghoff-Borg J, Krogh A, Hamelryck T. A generative, probabilistic model of local protein structure. Proc Natl Acad Sci USA 2008, 105(26):8932-7. 10.1073/pnas.0801715105, 2440424, 18579771.
33. Robinson DM, Jones DT, Kishino H, Goldman N, Thorne JL. Protein evolution with dependence among codons due to tertiary structure. Mol Biol Evol 2003, 20(10):1692-704. 10.1093/molbev/msg184, 12885968.
34. Rodrigue N, Kleinman CL, Philippe H, Lartillot N. Computational methods for evaluating phylogenetic models of coding sequence evolution with dependence between codons. Mol Biol Evol 2009, 26(7):1663-76. 10.1093/molbev/msp078, 19383983.
35. Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP. Bayesian inference of phylogeny and its impact on evolutionary biology. Science 2001, 294(5550):2310-4. 10.1126/science.1065889, 11743192.
36. Lunter G, Miklós I, Drummond A, Jensen JL, Hein J. Bayesian coestimation of phylogeny and sequence alignment. BMC Bioinformatics 2005, 6:83. 10.1186/1471-2105-6-83, 1087833, 15804354.
37. Zhu J, Liu JS, Lawrence CE. Bayesian adaptive sequence alignment algorithms. Bioinformatics 1998, 14:25-39. 10.1093/bioinformatics/14.1.25, 9520499.
38. Wüthrich K. The way to NMR structures of proteins. Nat Struct Biol 2001, 8(11):923-5. 10.1038/nsb1101-923, 11685234.
39. Rieping W, Habeck M, Nilges M. Inferential structure determination. Science 2005, 309(5732):303-6. 10.1126/science.1110428, 16002620.
40. Fraser J, Rousseau M, Blanchette M, Dostie J. Computing chromosome conformation. Methods Mol Biol 2010, 674:251-68. 10.1007/978-1-60761-854-6_16, 20827597.
41. Lanctôt C, Kaspar C, Cremer T. Positioning of the mouse Hox gene clusters in the nuclei of developing embryos and differentiating embryoid bodies. Exp Cell Res 2007, 313(7):1449-59. 10.1016/j.yexcr.2007.01.027, 17346703.
42. Cremer M, Grasser F, Lanctôt C, Müller S, Neusser M, Zinner R, Solovei I, Cremer T. Multicolor 3D fluorescence in situ hybridization for imaging interphase chromosomes. Methods Mol Biol 2008, 463:205-39. 10.1007/978-1-59745-406-3_15, 18951171.
43. Torrie GM, Valleau JP. Monte-Carlo free energy estimates using non-Boltzmann sampling. Chemical Physics Letters 1974, 28:578-581.
44. Metropolis, T HA, Rosenbluth AW, Teller E. Equation of state calculation by fast computing machines. Journal of Chemical Physics 1953, 21:1087-1092.
45. Ward J. Hierarchical grouping to optimize an objective function. Journal of the American Statistical Association 1963, 58(301):236.
46. Cohen FE, Sternberg MJ. On the prediction of protein structure: The significance of the root-mean-square deviation. J Mol Biol 1980, 138(2):321-33. 10.1016/0022-2836(80)90289-2, 7411610.
47. Maiorov VN, Crippen GM. Significance of root-mean-square deviation in comparing three-dimensional structures of globular proteins. J Mol Biol 1994, 235(2):625-34. 10.1006/jmbi.1994.1017, 8289285.
48. Tkachuk DC, Kohler S, Cleary ML. Involvement of a homolog of Drosophila trithorax by 11q23 chromosomal translocations in acute leukemias. Cell 1992, 71(4):691-700. 10.1016/0092-8674(92)90602-9, 1423624.
49. Ayton PM, Cleary ML. Transformation of myeloid progenitors by MLL oncoproteins is dependent on Hoxa7 and Hoxa9. Genes Dev 2003, 17(18):2298-307. 10.1101/gad.1111603, 196466, 12952893.
50. Mateos-Langerak J, Bohn M, de Leeuw W, Giromus O, Manders E, Verschure P, Indemans M, Gierman H, Heermann D, van Driel R, Goetze S. Spatially confined folding of chromatin in the interphase nucleus. Proc Natl Acad Sci USA 2009, 106(10):3812-7. 10.1073/pnas.0809501106, 2656162, 19234129.
51. Bystricky K, Heun P, Gehlen L, Langowski J, Gasser SM. Long-range compaction and exibility of interphase chromatin in budding yeast analyzed by high-resolution imaging techniques. Proc Natl Acad Sci USA 2004, 101(47):16495-500. 10.1073/pnas.0402766101, 534505, 15545610.
52. et al. FANTOM Consortium The transcriptional network that controls growth arrest and differentiation in a human myeloid leukemia cell line. Nat Genet 2009, 41(5):553-62. 10.1038/ng.375, 19377474, FANTOM Consortium.
53. Spilianakis CG, Flavell RA. Long-range intrachromosomal interactions in the T helper type 2 cytokine locus. Nat Immunol 2004, 5(10):1017-27. 10.1038/ni1115, 15378057.
54. Liu Z, Garrard WT. Long-range interactions between three transcriptional enhancers, active Vkappa gene promoters, and a 3' boundary sequence spanning 46 kilobases. Mol Cell Biol 2005, 25(8):3220-31. 10.1128/MCB.25.8.3220-3231.2005, 1069589, 15798207.
55. Crutchley JL, Wang XQD, Ferraiuolo MA, Dostie J. Chromatin conformation signatures: ideal human disease biomarkers?. Biomark Med 2010, 4(4):611-29. 10.2217/bmm.10.68, 20701449.
56. Dostie J, Dekker J. Mapping networks of physical interactions between genomic elements using 5C technology. Nat Protoc 2007, 2(4):988-1002. 10.1038/nprot.2007.116, 17446898.
57. Rodley CDM, Bertels F, Jones B, O'Sullivan JM. Global identification of yeast chromosome interactions using Genome conformation capture. Fungal Genet Biol 2009, 46(11):879-86. 10.1016/j.fgb.2009.07.006, 19628047.
58. Schrödinger, LLC The PyMOL Molecular Graphics System, Version 1.3r1. 2010, Schrödinger, LLC.
59. Langowski J, Heermann DW. Computational modeling of the chromatin fiber. Semin Cell Dev Biol 2007, 18(5):659-67. 10.1016/j.semcdb.2007.08.011, 17936653.