Analysis methods for studying the 3D architecture of the genome

Genome Biology

Volumn 16, Issue 1, 2015, Pages

  Ay, Ferhat ^a,b   Noble, William S ^a,c  

^a UNIVERSITY OF WASHINGTON   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c University of Washington   (United States)

Author keywords

Chromatin conformation capture; Genome architecture; Three dimensional genome; Three dimensional modeling

Indexed keywords

ANALYTIC METHOD; CHROMATIN STRUCTURE; CHROMOSOME PAIRING; COMPUTER PROGRAM; DATA PROCESSING; GENE MAPPING; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC DISTANCE; GENETIC PROCEDURES; GENOME; HIDDEN MARKOV MODEL; HIGH THROUGHPUT CHROMOSOME CONFORMATION CAPTURE; HUMAN; MOLECULAR LIBRARY; NONHUMAN; POLYMERASE CHAIN REACTION; READ LEVEL FILTERING; READ PAIR LEVEL FILTERING; REVIEW; ANIMAL; CHEMISTRY; CHROMATIN; CHROMOSOME; GENE LOCUS; GENOMICS; MOUSE; PROCEDURES; SEQUENCE ALIGNMENT;

CHROMATIN;

ANIMALS; CHROMATIN; CHROMOSOMES; GENETIC LOCI; GENOMICS; HUMANS; MICE; SEQUENCE ALIGNMENT;

EID: 84940517744     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-015-0745-7     Document Type: Review

References (136)

1. Dekker J, Rippe K, Dekker M, Kleckner N.Capturing chromosome conformation. Science. 2002; 295(5558):1306-11.
2. Simonis M, Klous P, Splinter E, Moshkin Y, Willemsen R, de Wit E, et al.Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on-chip (4C). Nature Genetics. 2006; 38:1348-54.
3. Zhao Z, Tavoosidana G, Sjolinder M, Gondor A, Mariano P, Wang S, et al.Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- and interchromosomal interactions. Nat Genet. 2006; 38(11):1341-47.
4. van de Werken HJ, Landan G, Holwerda SJ, Hoichman M, Klous P, Chachik R, et al.Robust 4C-seq data analysis to screen for regulatory DNA interactions. Nat Methods. 2012; 9(10):969-72. doi: http://dx.doi.org/10.1038/nmeth.2173 .
5. Dostie J, Richmond TA, Arnaout RA, Selzer RR, Lee WL, Honan TA, et al.Chromosome Conformation Capture Carbon Copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res. 2006; 16(10):1299-309.
6. Fullwood MJ, Liu MH, Pan YF, Liu J, Xu H, Mohamed YB, et al.An oestrogen-receptor-alpha-bound human chromatin interactome. Nature. 2009; 462(7269):58-64.
7. 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(5950):289-93.
8. Duan Z, Andronescu M, Schutz K, McIlwain S, Kim YJ, Lee C, et al.A three-dimensional model of the yeast genome. Nature. 2010; 465:363-7.
9. Kalhor R, Tjong H, Jayathilaka N, Alber F, Chen L.Genome architectures revealed by tethered chromosome conformation capture and population-based modeling. Nat Biotechnol. 2011; 30(1):90-8.
10. Ferraiuolo MA, Rousseau M, Miyamoto C, Shenker S, Wang XQ, Nadler M, et al.The three-dimensional architecture of Hox cluster silencing. Nucleic Acids Res. 2010; 21:7472-84.
11. Zhang Y, Wong CH, Birnbaum RY, Li G, Favaro R, Ngan CY, et al.Chromatin connectivity maps reveal dynamic promoter-enhancer long-range associations. Nature. 2013; 504(7479):306-10.
12. Shen Y, Yue F, McCleary DF, Ye Z, Edsall L, Kuan S, et al.A map of the cis-regulatory sequences in the mouse genome. Nature. 2012; 488:116-20.
13. Sanyal A, Lajoie BR, Jain G, Dekker J.The long-range interaction landscape of gene promoters. Nature. 2012; 489(7414):109-13.
14. Li G, Ruan X, Auerbach RK, Sandhu KS, Zheng M, Wang P, et al.Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell. 2012; 148(1):84-98.
15. 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(7398):376-80.
16. Ay F, Bunnik EM, Varoquaux N, Bol SM, Prudhomme J, Vert JP, et al.Three-dimensional modeling of the P. falciparum genome during the erythrocytic cycle reveals a strong connection between genome architecture and gene expression. Genome Res. 2014; 24:974-88.
17. Ma W, Ay F, Lee C, Gulsoy G, Deng X, Cook S, et al.Fine-scale chromatin interaction maps reveal the cis-regulatory landscape of lincRNA genes in human cells. Nat Methods. 2015; 12(1):71-8.
18. Rao SS, Huntley MH, Durand NC, Stamenova EK, Bochkov ID, Robinson JT, et al.A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell. 2014; 59(7):1665-80.
19. Ryba T, Hiratani I, Lu J, Itoh M, Kulik M, Zhang J, et al.Evolutionarily conserved replication timing profiles predict long-range chromatin interactions and distinguish closely related cell types. Genome Res. 2010; 20(6):761-70.
20. Ay F, Bailey TL, Noble WS. Statistical confidence estimation for Hi-C data reveals regulatory chromatin contacts. Genome Res. 2014; 24:999-1011. Available from: http://noble.gs.washington.edu/proj/fit-hi-c .
21. Pope BD, Ryba T, Dileep V, Yue F, Wu W, Denas O, et al.Topologically associating domains are stable units of replication-timing regulation. Nature. 2014; 515(7527):402-5.
22. De S, Michor F.DNA replication timing and long-range DNA interactions predict mutational landscapes of cancer genomes. Nat Biotechnol. 2011; 29(12):1103-8.
23. Fudenberg G, Getz G, Meyerson M, Mirny LA. High order chromatin architecture shapes the landscape of chromosomal alterations in cancer. Nat Biotechnol. 2011; 29(12):1109-13.
24. Nagano T, Lubling Y, Stevens TJ, Schoenfelder S, Yaffe E, Dean W, et al.Single-cell Hi-C reveals cell-to-cell variability in chromosome structure. Nature. 2013; 502(7469):59-64.
25. Burton JN, Adey A, Patwardhan RP, Qiu R, Kitzman JO, Shendure J.Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions. Nat Biotechnol. 2013; 31(12):1119-25.
26. Kaplan N, Dekker J.High-throughput genome scaffolding from in vivo DNA interaction frequency. Nat Biotechnol. 2013; 31(12):1143-7.
27. Selvaraj S, RD J, Bansal V, Ren B.Whole-genome haplotype reconstruction using proximity-ligation and shotgun sequencing. Nat Biotechnol. 2013; 31(12):1111-8.
28. Marie-Nelly H, Marbouty M, Cournac A, Liti G, Fischer G, Zimmer C, et al.Filling annotation gaps in yeast genomes using genome-wide contact maps. Bioinformatics. 2014; 30(15):2105-13.
29. Varoquaux N, Liachko I, Ay F, Burton JN, Shendure J, Dunham M, et al.Accurate identification of centromere locations in yeast genomes using Hi-C. Nucleic Acids Research. 2015; 43(11):5331-9.
30. 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(3):458-72.
31. Tanizawa H, Iwasaki O, tanaka A, Capizzi JR, Wickramasignhe P, Lee M, et al.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.
32. Mizuguchi T, Fudenberg G, Mehta S, Belton JM, Taneja N, Folco HD, et al.Cohesin-dependent globules and heterochromatin shape 3D genome architecture in S. pombe. Nature. 2014; 516(7531):432-5.
33. Burton JN, Liachko I, Dunham MJ, Shendure J.Species-level deconvolution of metagenome assemblies with Hi-C-based contact probability maps. G3 (Bethesda). 2014; 4(7):1339-46.
34. Le TBK, Imakaev MV, Mirny LA, Laub MT. High-Resolution mapping of the spatial organization of a bacterial chromosome. Science. 2013; 342(6159):731-4.
35. Li L, Lyu X, Hou C, Takenaka N, Nguyen HQ, Ong CT, et al.Widespread rearrangement of 3D chromatin organization underlies polycomb-mediated stress-induced silencing. Molecular Cell. 2015; 58(2):216-31.
36. Hou C, Li L, Qin ZS, Corces VG. Gene density, transcription, and insulators contribute to the partition of the Drosophila genome into physical domains. Molecular Cell. 2012; 48(3):471-84.
37. Wang C, Liu C, Roqueiro D, Grimm D, Schwab R, Becker C, et al.Genome-wide analysis of local chromatin packing in Arabidopsis thaliana. Genome Res. 2015; 25(2):246-56.
38. Feng S, Cokus SJ, Schubert V, Zhai J, Pellegrini M, Jacobsen SE. Genome-wide Hi-C analyses in wild-type and mutants reveal high-resolution chromatin interactions in Arabidopsis. Mol Cell. 2014; 55(5):694-707.
39. Grigoriev A.Hi-C analysis in Arabidopsis identifies the KNOT, a structure with similarities to the flamenco locus of Drosophila. Mol Cell. 2014; 55(5):678-93.
40. Lemieux JE, Kyes SA, Otto TD, Feller AI, Eastman RT, Pinches RA, et al.Genome-wide profiling of chromosome interactions in Plasmodium falciparum characterizes nuclear architecture and reconfigurations associated with antigenic variation. Mol Microbiol. 2013; 90(3):519-37.
41. Zhang Y, McCord RP, Ho Y, Lajoie BR, Hildebrand DG, Simon AC, et al.Spatial organization of the mouse genome and its role in recurrent chromosomal translocations. Cell. 2012; 148:1-14.
42. Jin F, Li Y, Dixon JR, Selvaraj S, Ye Z, Lee AY, et al.A high-resolution map of the three-dimensional chromatin interactome in human cells. Nature. 2013; 503(7475):290-94.
43. Naumova N, Imakaev M, Fudenberg G, Zhan Y, Lajoie BR, Mirny LA, et al.Organization of the mitotic chromosome. Science. 2013; 342(6161):948-53.
44. Chen H, Chen J, Muir LA, Ronquist S, Meixner W, Ljungman M, et al.Functional organization of the human 4D Nucleome. Proc Natl Acad Sci U S A. 2015 Jun 30; 112(26):8002-7.
45. Ay F, Vu TH, Zeitz MJ, Varoquaux N, Carette JE, Vert JP, et al.Identifying multi-locus chromatin contacts in human cells using tethered multiple 3C. BMC Genomics. 2015; 16:121.
46. HiCUP: Hi-C User Pipeline. Available from: http://www.bioinformatics.babraham.ac.uk/projects/hicup .
47. Imakaev M, Fudenberg G, McCord RP, Naumova N, Goloborodko A, Lajoie BR, et al.Iterative correction of Hi-C data reveals hallmarks of chromosome organization. Nat Methods. 2012; 9:999-1003. Available from: http://mirnylab.bitbucket.org/hiclib .
48. Li H, Durbin R.Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics. 2010; 26(5):589-95.
49. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009; 10(3):R25.
50. Lajoie BR, Dekker J, Kaplan N.The Hitchhiker's guide to Hi-C analysis: practical guidelines. Methods. 2015; 72:65-75.
51. Picard. Available from: http://picard.sourceforge.net .
52. 3C/4C/5C/Hi-C/ChIA-PET software tools. Available from: omictools.com/3c-4c-5c-hi-c-chia-pet-c298-p1.html .
53. A non-exhaustive list of methods for 3D genomics. Available from: sgt.cnag.cat/3dg/methods .
54. Yaffe E, Tanay A. Probabilistic modeling of Hi-C contact maps eliminates systematic biases to characterize global chromosomal architecture. Nat Genet. 2011; 43:1059-65. Available from: http://compgenomics.weizmann.ac.il/tanay/?page_id=283 .
55. Hu M, Deng K, Selvaraj S, Qin Z, Ren B, Liu JS. HiCNorm: removing biases in Hi-C data via Poisson regression. Bioinformatics. 2012; 28(23):3131-3.
56. Cournac A, Marie-Nelly H, Marbouty M, Koszul R, Mozziconacci J.Normalization of a chromosomal contact map. BMC Genomics. 2012; 13:436.
57. Li W, Gong K, Li Q, Alber F, Zhou XJ. Hi-Corrector: a fast, scalable and memory-efficient package for normalizing large-scale Hi-C data. Bioinformatics. 2015; 31(6):960-2.
58. Yang EW, GDNorm JiangT.An Improved Poisson Regression Model for Reducing Biases in Hi-C Data. In: Proceedings of the 14th International Workshop of Algorithms in Bioinformatics. vol. 8701 of Lecture Notes in Computer Science. Berlin, Heidelberg: Springer-Verlag: 2014. p. 263-80.
59. Shavit Y, Lio' P.Combining a wavelet change point and the Bayes factor for analysing chromosomal interaction data. Mol Biosyst. 2014; 10(6):1576-85.
60. Sinkhorn R, Knopp P.Concerning nonnegative matrices and doubly stochastic matrices. Pac J Math. 1967; 21(2):343-8.
61. Knight P, Ruiz D.A fast algorithm for matrix balancing. IMA J Numer Anal. 2013; 33(3):1029-47.
62. HOMER: Analyzing Hi-C genome-wide interaction data. Available from: http://homer.salk.edu/homer/interactions .
63. Bickmore WA, van Steensel B. Genome Architecture: Domain Organization of Interphase Chromosomes. Cell. 2013; 152(6):1270-284.
64. Belmont AS. Large-scale chromatin organization: the good, the surprising, and the still perplexing. Curr Opin Cell Biol. 2014; 26C:69-78.
65. Sanyal A, Lajoie BR, Jain G, Dekker J.The long-range interaction landscape of gene promoters. Nature. 2012; 489:109-13.
66. Dai Z, Dai X.Nuclear colocalization of transcription factor target genes strengthens coregulation in yeast. Nucleic Acids Res. 2012; 40(1):27-36.
67. Witten DM, Noble WS. On the assessment of statistical significance of three-dimensional colocalization of sets of genomic elements. Nucleic Acids Res. 2012; 40(9):3849-55.
68. Paulsen J, Lien TG, Sandve GK, Holden L, Borgan O, Glad IK, et al.Handling realistic assumptions in hypothesis testing of 3D co-localization of genomic elements. Nucleic Acids Res. 2013; 41(10):5164-74.
69. Paulsen J, Sandve GK, Gundersen S, Lien TG, Trengereid K, Hovig E.HiBrowse: multi-purpose statistical analysis of genome-wide chromatin 3D organization. Bioinformatics. 2014; 30(11):1620-2.
70. Capurso D, Segal MR. Distance-based assessment of the localization of functional annotations in 3D genome reconstructions. BMC Genomics. 2014 18; 15:992.
71. Lachner M, O'Sullivan RJ, Jenuwein T.An epigenetic road map for histone lysine methylation. J Cell Sci. 2003; 116(11):2117-24.
72. Pauler FM, Sloane MA, Huang R, Regha K, Koerner MV, Tamir I, et al.H3K27me3 forms BLOCs over silent genes and intergenic regions and specifies a histone banding pattern on a mouse autosomal chromosome. Genome Res. 2009; 19(2):221-33.
73. Wen B, Wu H, Shinkai Y, Irizarry RA, Feinberg AP. Large organized chromatin K9-modifications (LOCKs) distinguish differentiated from embryonic stem cells. Nat Genet. 2009; 41(2):246.
74. Hiratani I, Ryba T, Itoh M, Yokochi T, Schwaiger M, Chang CW, et al.Global reorganization of replication domains during embryonic stem cell differentiation. PLoS Biol. 2008; e245:6.
75. 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.
76. Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, et al.Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature. 2008; 453(7197):948-51.
77. van Koningsbruggen S, Gierlinski M, Schofield P, Martin D, Barton G, Ariyurek Y, et al.High-resolution whole-genome sequencing reveals that specific chromatin domains from most human chromosomes associate with nucleoli. Mol Biol Cell. 2010; 21(21):3735-48.
78. Day N, Hemmaplardh A, Thurman RE, Stamatoyannopoulos JA, Noble WS. Unsupervised segmentation of continuous genomic data. Bioinformatics. 2007; 23(11):1424-6.
79. Hoffman MM, Buske OJ, Wang J, Weng Z, Bilmes JA, Noble WS. Unsupervised pattern discovery in human chromatin structure through genomic segmentation. Nat Methods. 2012; 9(5):473-6.
80. Ernst J, Kellis M.Discovery and characterization of chromatin states for systematic annotation of the human genome. Nat Biotechnol. 2010; 28(8):817-25.
81. Thurman RE, Day N, Noble WS, Stamatoyannopoulos JA. Identification of higher-order functional domains in the human ENCODE regions. Genome Res. 2007; 17:917-27.
82. Lian H, Thompson W, Thurman RE, Stamatoyannopoulos JA, Noble WS, Lawrence C.Automated mapping of large-scale chromatin structure in ENCODE. Bioinformatics. 2008; 24(17):1911-6.
83. Filion GJ, van Bemmel JG, Braunschweig U, Talhout W, Kind J, Ward LD, et al.Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell. 2010; 143(2):212-24.
84. 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(7398):381-5.
85. Steensel BV, Dekker J.Genomics tools for unraveling chromosome architecture. Nat Biotechnol. 2010; 28:1089-95.
86. Libbrecht M, Ay F, Hoffman MM, Gilbert DM, Bilmes JA, Noble WS. Joint annotation of chromatin state and chromatin conformation reveals relationships among domain types and identifies domains of cell-type-specific expression. Genome Res. 2015; 25(4):544-57.
87. Filippova D, Patro R, Duggal G, Kingsford C. Identification of alternative topological domains in chromatin. Algorithms Mol Biol. 2014; 9:14.
88. Lévy-Leduc C, Delattre M, Mary-Huard T, Robin S. Two-dimensional segmentation for analyzing Hi-C data. Bioinformatics. 2014 1; 30(17):i386-92.
89. Sexton T, Cavalli G.The role of chromosome domains in shaping the functional genome. Cell. 2015; 160(6):1049-59.
90. Dekker J, Marti-Renom MA, Mirny LA. Exploring the three-dimensional organization of genomes: interpreting chromatin interaction data. Nat Rev Genet. 2013; 14(6):390-403.
91. Nora EP, Dekker J, Heard E.Segmental folding of chromosomes: a basis for structural and regulatory chromosomal neighborhoods?Bioessays. 2013; 35(9):818-28.
92. Rosa A, Zimmer C.Computational models of large-scale genome architecture. Int Rev Cell Mol Biol. 2014; 307:275-349.
93. 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(7):1295-305.
94. Tokuda N, Terada TP, Sasai M.Dynamical modeling of three-dimensional genome organization in interphase budding yeast. Biophys J. 2012; 102(2):296-304.
95. Wong H, Marie-Nelly H, Herbert S, Carrivain P, Blanc H, Koszul R, et al.A predictive computational model of the dynamic 3D interphase yeast nucleus. Curr Biol. 2012; 22(20):1881-90.
96. Wong H, Arbona JM, Zimmer C.How to build a yeast nucleus. Nucleus. 2013; 4(5):361-6.
97. Gu rsoy G, Xu Y, Liang J.Computational predictions of structures of multichromosomes of budding yeast. Conf Proc IEEE Eng Med Biol Soc. 2014; 2014:3945-8.
98. Mirny LA. The fractal globule as a model of chromatin architecture in the cell. Chromosome Res. 2011; 19(1):37-51.
99. Serra F, Di Stefano M, Spill YG, Cuartero Y, Goodstadt M, Baù D, et al.Restraint-based three-dimensional modeling of genomes and genomic domains; 2015 May 14. doi: http://dx.doi.org/10.1016/j.febslet.2015.05.012 .
100. Marti-Renom MA, Mirny LA. Bridging the resolution gap in structural modeling of 3D genome organization. PLoS Comput Biol. 2011; 7(7):e1.002125.
101. Varoquaux N, Ay F, Noble WS, Vert JP. A statistical approach for inferring the 3D structure of the genome. Bioinformatics. 2014; 30(12):i26-i33.
102. Wang S, Xu J, Zeng J.Inferential modeling of 3D chromatin structure. Nucleic Acids Res. 2015; 43(8):e54.
103. Zhang Z, Li G, Toh KC, Sung WK. 3D chromosome modeling with semi-definite programming and Hi-C data. J Comput Biol. 2013; 20(11):831-46.
104. Ben-Elazar S, Yakhini Z, Yanai I. Spatial localization of co-regulated genes exceeds genomic gene clustering in the Saccharomyces cerevisiae genome. Nucleic Acids Res. 2013; 41(4):2191-201.
105. Bau D, Sanyal A, Lajoie BR, Capriotti E, Byron M, Lawrence JB, et al.The three-dimensional folding of the aα-globin gene domain reveals formation of chromatin globules. Nat Struct Mol Biol. 2011; 18(1):107-14.
106. Lesne A, Riposo J, Roger P, Cournac A, Mozziconacci J. 3D genome reconstruction from chromosomal contacts. Nat Methods. 2014; 11(11):1141-3.
107. Kruskal J. Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika. 1964; 29:1-27.
108. Rousseau M, Fraser J, Ferraiuolo M, Dostie J, Blanchette M. Three-dimensional modeling of chromatin structure from interaction frequency data using Markov chain Monte Carlo sampling. BMC Bioinformatics. 2011; 12(1):414.
109. Giorgetti L, Galupa R, Nora EP, Piolot T, Lam F, Dekker J, et al.Predictive polymer modeling reveals coupled fluctuations in chromosome conformation and transcription. Cell. 2014; 157(4):950-63.
110. Hu M, Deng K, Qin Z, Dixon J, Selvaraj S, Fang J, et al.Bayesian inference of spatial organizations of chromosomes. PLoS Comput Biol. 2013; 9(1):e1002893.
111. Peng C, Fu LY, Dong PF, Deng ZL, Li JX, Wang XT, et al.The sequencing bias relaxed characteristics of Hi-C derived data and implications for chromatin 3D modeling. Nucleic Acids Res. 2013; 41(19):e183.
112. Trieu T, Cheng J.Large-scale reconstruction of 3D structures of human chromosomes from chromosomal contact data. Nucleic Acids Res. 2014; 42(7):e52.
113. Karolchik D, Barber GP, Casper J, Clawson H, Cline MS, Diekhans M, et al.The UCSC Genome Browser database: 2014 update. Nucleic Acids Res. 2014; 42(D1):D764-70.
114. Hubbard T, Andrews D, Caccamo M, Cameron G, Chen Y, Clamp M, et al.Ensembl 2005. Nucleic Acids Res. 2005; 33(Database issue):D447-53.
115. Nicol JW, Helt GA, Blanchard S, Raja A, Loraine AE. The Integrated Genome Browser: free software for distribution and exploration of genome-scale datasets. Bioinformatics. 2009; 25(20):2730-31.
116. Zhou X, Maricque B, Xie M, Li D, Sundaram V, Martin EA, et al.The Human Epigenome Browser at Washington University. Nat Methods. 2011; 8(12):989-90.
117. Zhou X, Lowdon RF, Li D, Lawson HA, Madden PAF, Costello JT, et al.Exploring long-range genome interactions using the WashU EpiGenome Browser. Nat Methods. 2013; 10:375-6.
118. The 3D Genome Browser. Available from: http://www.3dgenome.org .
119. Asbury TM, Mitman M, Tang J, Zheng WJ. Genome3D: A viewer-model framework for integrating and visualizing multi-scale epigenomic information within a three-dimensional genome. BMC Bioinformatics. 2010; 11:444.
120. Tools for modeling and analyzing 3D genomes. Available from: http://sgt.cnag.cat/3dg.
121. Servant N, Lajoie BR, Nora EP, Giorgetti L, Chen CJ, Heard E, et al.HiTC: exploration of high-throughput 'C' experiments. Bioinformatics. 2012; 28(21):2843-4. Available from: http://www.bioconductor.org/packages/release/bioc/html/HiTC.html .
122. HiCdat: Hi-C data analysis tool. Available from: https://github.com/MWSchmid/HiCdat .
123. Sefer E, Duggal G, Kingsford C. Deconvolution of Ensemble Chromatin Interaction Data Reveals the Latent Mixing Structures in Cell Subpopulations. In: Proceedings of the Nineteenth Annual International Conference on Computational Molecular Biology of Lecture Notes in Bioinformatics. Zwitzerland: Springer International Publishing. 2015;9029:293-308.
124. Junier I, Spill YG, Marti-Renom MA, Beato M, Le Dily F. On the demultiplexing of chromosome capture conformation data: FEBS Letters; 2015 Jun 6. doi: http://dx.doi.org/10.1016/j.febslet.2015.05.049 .
125. Lan X, Witt H, Katsumura K, Ye Z, Wang Q, Bresnick EH, et al.Integration of Hi-C and ChIP-seq data reveals distinct types of chromatin linkages. Nucleic Acids Res. 2012; 40(16):7690-704.
126. Rickman DS, Soong TD, Moss B, Mosquera JM, Dlabal J, Terry S, et al.Oncogene-mediated alterations in chromatin conformation. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109(23):9083-88.
127. Le Dily F, Baù D, Pohl A, Vicent GP, Serra F, Soronellas D, et al. Distinct structural transitions of chromatin topological domains correlate with coordinated hormone-induced gene regulation. Genes Dev. 2014; 28(19):2151-62.
128. Narendra V, Rocha PP, An D, Raviram R, Skok JA, Mazzoni EO, et al.Transcription. CTCF establishes discrete functional chromatin domains at the Hox clusters during differentiation. Science. 2015 27; 347(6225):1017-21.
129. Lupiáñez DG, Kraft K, Heinrich V, Krawitz P, Brancati F, Klopocki E, et al.Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell. 2015 21; 161(5):1012-25.
130. ENCODE Project Consortium. An Integrated Encyclopedia of DNA Elements in the Human Genome. Nature. 2012; 489:57-74.
131. HiC-inspector: a toolkit for high-throughput chromosome capture data. Available from: https://github.com/HiC-inspector .
132. Hwang YC, Lin CF, Valladares O, Malamon J, Kuksa PP, Zheng Q, et al.HIPPIE: a high-throughput identification pipeline for promoter interacting enhancer elements. Bioinformatics. 2015; 31(8):1290-2.
133. HiC-Box: Hi-C contact data processing, from reads alignment to 3D structure reconstruction. Available from: https://github.com/koszullab/HiC-Box .
134. HiC-Pro: An optimized and flexible pipeline for Hi-C data processing. Available from: https://github.com/nservant/HiC-Pro .
135. GOTHiC: Binomial test for Hi-C data analysis. Available from: http://www.bioconductor.org/packages/release/bioc/html/GOTHiC.html .
136. HiFive: a Python package for normalization and analysis of chromatin structural data produced using either the 5C of HiC assay. Available from: http://bxlab-hifive.readthedocs.org .