Genome-wide mapping and analysis of chromosome architecture

Nature Reviews Molecular Cell Biology

Volumn 17, Issue 12, 2016, Pages 743-755

  Schmitt, Anthony D ^a   Hu, Ming ^b,c   Ren, Bing ^d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATIN; CHROMOSOME STRUCTURE; CONFORMATION; GENE MAPPING; GENOME ANALYSIS; HIGH THROUGHPUT SCREENING; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; REVIEW; STATISTICAL BIAS; THREE DIMENSIONAL IMAGING; ANIMAL; CHROMOSOMAL MAPPING; CHROMOSOME; COMPUTER SIMULATION; HUMAN; MOLECULAR MODEL; ULTRASTRUCTURE;

CHROMATIN;

ANIMALS; CHROMATIN; CHROMOSOME MAPPING; CHROMOSOMES; COMPUTER SIMULATION; HUMANS; MODELS, MOLECULAR;

EID: 84984804790     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm.2016.104     Document Type: Review

References (119)

1. ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74 (2012).
2. Roadmap Epigenomics Consortium et al. Integrative analysis of 111 reference human epigenomes. Nature 518, 317-330 (2015).
3. Bickmore W. A, & van Steensel B. Genome architecture: domain organization of interphase chromosomes. Cell 152, 1270-1284 (2013).
4. de Laat W, & Duboule D. Topology of mammalian developmental enhancers and their regulatory landscapes. Nature 502, 499-506 (2013).
5. de Wit E, & de Laat W. A decade of 3C technologies: insights into nuclear organization. Genes Dev. 26, 11-24 (2012).
6. Dixon J. R, et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376-380 (2012).
7. Gorkin D. U, Leung D, & Ren B. The 3D genome in transcriptional regulation and pluripotency. Cell Stem Cell 14, 762-775 (2014).
8. Levine M, Cattoglio C, & Tjian R. Looping back to leap forward: transcription enters a new era. Cell 157, 13-25 (2014).
9. Nora E. P, Dekker J, & Heard E. Segmental folding of chromosomes: a basis for structural and regulatory chromosomal neighborhoods?. Bioessays 35, 818-828 (2013).
10. Nora E. P, et al. Spatial partitioning of the regulatory landscape of the X inactivation centre. Nature 485, 381-385 (2012).
11. Phillips-Cremins J. E, et al. Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 153, 1281-1295 (2013).
12. Deng W, et al. Reactivation of developmentally silenced globin genes by forced chromatin looping. Cell 158, 849-860 (2014).
13. Deng W, et al. Controlling long-range genomic interactions at a native locus by targeted tethering of a looping factor. Cell 149, 1233-1244 (2012).
14. Kim A, & Dean A. Chromatin loop formation in the β-globin locus and its role in globin gene transcription. Mol. Cells 34, 1-5 (2012).
15. Krivega I, & Dean A. Enhancer and promoter interactions-long distance calls. Curr. Opin. Genet. Dev. 22, 79-85 (2012).
16. Plank J. L, & Dean A. Enhancer function: mechanistic and genome-wide insights come together. Mol. Cell 55, 5-14 (2014).
17. Dowen J. M, et al. Control of cell identity genes occurs in insulated neighborhoods in mammalian chromosomes. Cell 159, 374-387 (2014).
18. Heidari N, et al. Genome-wide map of regulatory interactions in the human genome. Genome Res. 24, 1905-1917 (2014).
19. Jin F, et al. A high-resolution map of the three-dimensional chromatin interactome in human cells. Nature 503 290-294 (2013).
20. Li G, et al. Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell 148, 84-98 (2012).
21. Sanyal A, Lajoie B. R, Jain G, & Dekker J. The long range interaction landscape of gene promoters. Nature 489, 109-113 (2012).
22. Lieberman-Aiden E, et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289-293 (2009).
23. Fullwood M. J, et al. An oestrogen-receptor-α-bound human chromatin interactome. Nature 462, 58-64 (2009).
24. Kalhor R, Tjong H, Jayathilaka N, Alber F, & Chen L. Genome architectures revealed by tethered chromosome conformation capture and population-based modeling. Nat. Biotechnol. 30, 90-98 (2012).
25. Hughes J. R, et al. Analysis of hundreds of cis-regulatory landscapes at high resolution in a single, high-Throughput experiment. Nat. Genet. 46, 205-212 (2014).
26. Kolovos P, et al. Targeted chromatin capture (T2C): a novel high resolution high throughput method to detect genomic interactions and regulatory elements. Epigenetics Chromatin 7, 10 (2014).
27. Rao S. S, et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159 1665-1680 (2014).
28. Selvaraj S, R. Dixon J, Bansal V, & Ren B. Whole genome haplotype reconstruction using proximity-ligation and shotgun sequencing. Nat. Biotechnol. 31, 1111-1118 (2013).
29. Selvaraj S, Schmitt A. D, Dixon J. R, & Ren B. Complete haplotype phasing of the MHC and KIR loci with targeted HaploSeq. BMC Genomics 16, 900 (2015).
30. de Vree P. J, et al. Targeted sequencing by proximity ligation for comprehensive variant detection and local haplotyping. Nat. Biotechnol. 32, 1019-1025 (2014).
31. Burton J. N, et al. Chromosome-scale scaffolding of de novo genome assemblies based on chromatin interactions. Nat. Biotechnol. 31, 1119-1125 (2013).
32. Kaplan N, & Dekker J. High-Throughput genome scaffolding from in vivo DNA interaction frequency. Nat. Biotechnol. 31, 1143-1147 (2013).
33. Marie-Nelly H, et al. High-quality genome (re)assembly using chromosomal contact data. Nat. Commun. 5, 5695 (2014).
34. Beitel C. W, et al. Strain- And plasmid-level deconvolution of a synthetic metagenome by sequencing proximity ligation products. PeerJ 2, e415 (2014).
35. Burton J. N, Liachko I, Dunham M. J, & Shendure J. Species-level deconvolution of metagenome assemblies with Hi C based contact probability maps. G3 (Bethesda) 4, 1339-1346 (2014).
36. Marbouty M, et al. Metagenomic chromosome conformation capture (meta3C) unveils the diversity of chromosome organization in microorganisms. eLife 3, e03318 (2014).
37. Duan Z, et al. A three-dimensional model of the yeast genome. Nature 465 363-367 (2010).
38. Nagano T, et al. Single-cell Hi C reveals cell to cell variability in chromosome structure. Nature 502, 59-64 (2013).
39. Snyder M. W, Adey A, Kitzman J. O, & Shendure J. Haplotype-resolved genome sequencing: experimental methods and applications. Nat. Rev. Genet. 16, 344-358 (2015).
40. Flot J. F, Marie-Nelly H, & Koszul R. Contact genomics: scaffolding and phasing (meta)genomes using chromosome 3D physical signatures. FEBS Lett. 589, 2966-2974 (2015).
41. Imakaev M. V, Fudenberg G, & Mirny L. A. Modeling chromosomes: beyond pretty pictures. FEBS Lett. 589, 3031-3036 (2015).
42. Serra F, et al. Restraint-based three-dimensional modeling of genomes and genomic domains. FEBS Lett. 589, 2987-2995 (2015).
43. Dekker J, Rippe K, Dekker M, & Kleckner N. Capturing chromosome conformation. Science 295, 1306-1311 (2002).
44. Cullen K. E, Kladde M. P, & Seyfred M. A. Interaction between transcription regulatory regions of prolactin chromatin. Science 261, 203-206 (1993).
45. Zhao Z, et al. Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra- And interchromosomal interactions. Nat. Genet. 38, 1341-1347 (2006).
46. van de Werken H. J, et al. Robust 4C seq data analysis to screen for regulatory DNA interactions. Nat. Methods 9, 969-972 (2012).
47. Sexton T, et al. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148, 458-472 (2012).
48. Deng X, et al. Bipartite structure of the inactive mouse X chromosome. Genome Biol. 16, 152 (2015).
49. Ma W, et al. Fine-scale chromatin interaction maps reveal the cis-regulatory landscape of human lincRNA genes. Nat. Methods 12, 71-78 (2015).
50. Hsieh T. H, et al. Mapping nucleosome resolution chromosome folding in yeast by micro C. Cell 162, 108-119 (2015).
51. Simonis M, et al. Nuclear organization of active and inactive chromatin domains uncovered by chromosome conformation capture-on chip (4C). Nat. Genet. 38, 1348-1354 (2006).
52. Dostie J, et al. Chromosome conformation capture carbon copy (5C): a massively parallel solution for mapping interactions between genomic elements. Genome Res. 16, 1299-1309 (2006).
53. Martin P, et al. Capture Hi C reveals novel candidate genes and complex long-range interactions with related autoimmune risk loci. Nat. Commun. 6, 10069 (2015).
54. Mifsud B, et al. Mapping long-range promoter contacts in human cells with high-resolution capture Hi C. Nat. Genet. 47, 598-606 (2015).
55. Sahlen P, et al. Genome-wide mapping of promoter-Anchored interactions with close to single-enhancer resolution. Genome Biol. 16, 156 (2015).
56. Schoenfelder S, et al. The pluripotent regulatory circuitry connecting promoters to their long-range interacting elements. Genome Res. 25, 582-597 (2015).
57. Schoenfelder S, et al. Polycomb repressive complex PRC1 spatially constrains the mouse embryonic stem cell genome. Nat. Genet. 47, 1179-1186 (2015).
58. Dryden N. H, et al. Unbiased analysis of potential targets of breast cancer susceptibility loci by Capture Hi C. Genome Res. 24, 1854-1868 (2014).
59. Jager R, et al. Capture Hi C identifies the chromatin interactome of colorectal cancer risk loci. Nat. Commun. 6, 6178 (2015).
60. Sanborn A. L, et al. Chromatin extrusion explains key features of loop and domain formation in wild-Type and engineered genomes. Proc. Natl Acad. Sci. USA 112, E6456-E6465 (2015).
61. Schmitt M. W, et al. Sequencing small genomic targets with high efficiency and extreme accuracy. Nat. Methods 12, 423-425 (2015).
62. Dixon J. R, et al. Chromatin architecture reorganization during stem cell differentiation. Nature 518, 331-336 (2015).
63. Fraser J, et al. Hierarchical folding and reorganization of chromosomes are linked to transcriptional changes in cellular differentiation. Mol. Syst. Biol. 11, 852 (2015).
64. Leung D, et al. Integrative analysis of haplotype-resolved epigenomes across human tissues. Nature 518, 350-354 (2015).
65. Nagano T, et al. Comparison of Hi C results using in solution versus in nucleus ligation. Genome Biol. 16, 175 (2015).
66. Seitan V. C, et al. Cohesin-based chromatin interactions enable regulated gene expression within preexisting architectural compartments. Genome Res. 23, 2066-2077 (2013).
67. Sofueva S, et al. Cohesin-mediated interactions organize chromosomal domain architecture. EMBO J. 32, 3119-3129 (2013).
68. Zuin J, et al. Cohesin and CTCF differentially affect chromatin architecture and gene expression in human cells. Proc. Natl Acad. Sci. USA 111, 996-1001 (2014).
69. Belton J. M, et al. Hi C: a comprehensive technique to capture the conformation of genomes. Methods 58, 268-276 (2012).
70. van Berkum N. L, et al. Hi C: a method to study the three-dimensional architecture of genomes. J. Vis. Exp. 39, 1869 (2010).
71. Comet I, Schuettengruber B, Sexton T, & Cavalli G. A chromatin insulator driving three-dimensional Polycomb response element (PRE) contacts and Polycomb association with the chromatin fiber. Proc. Natl Acad. Sci. USA 108, 2294-2299 (2011).
72. van de Werken H. J, et al. 4C technology: protocols and data analysis. Methods Enzymol. 513, 89-112 (2012).
73. Adey A, et al. Rapid, low-input, low-bias construction of shotgun fragment libraries by high-density in vitro transposition. Genome Biol. 11, R119 (2010).
74. Williamson I, et al. Anterior-posterior differences in HoxD chromatin topology in limb development. Development 139, 3157-3167 (2012).
75. Bickmore W. A. The spatial organization of the human genome. Annu. Rev. Genomics Hum. Genet. 14, 67-84 (2013).
76. Williamson I, et al. Spatial genome organization: contrasting views from chromosome conformation capture and fluorescence in situ hybridization. Genes Dev. 28, 2778-2791 (2014).
77. Yaffe E, & Tanay A. Probabilistic modeling of Hi C contact maps eliminates systematic biases to characterize global chromosomal architecture. Nat. Genet. 43, 1059-1065 (2011).
78. Hu M, et al. HiCNorm: removing biases in Hi C data via Poisson regression. Bioinformatics 28, 3131-3133 (2012).
79. Imakaev M, et al. Iterative correction of Hi C data reveals hallmarks of chromosome organization. Nat. Methods 9, 999-1003 (2012).
80. Servant N, et al. HiC-Pro: an optimized and flexible pipeline for Hi C data processing. Genome Biol. 16, 259 (2015).
81. Li W, Gong K, Li Q, Alber F, & Zhou X. J. Hi Corrector: a fast, scalable and memory-efficient package for normalizing large-scale Hi C data. Bioinformatics 31, 960-962 (2015).
82. Knopp P, & Sinkhorn R. Concerning nonnegative matrices and doubly stochastic matrices. Pacif. J. Math. 21, 343-348 (1967).
83. Knight P. A, & Ruiz D. A fast algorithm for matrix balancing. IMA J. Numer. Analysis 33, 1029-1047 (2012).
84. Shavit Y, & Lio P. Combining a wavelet change point and the Bayes factor for analysing chromosomal interaction data. Mol. Biosyst. 10, 1576-1585 (2014).
85. Cairns J, et al. CHiCAGO: robust detection of DNA looping interactions in capture Hi C data. Genome Biol. 17, 127 (2015).
86. Cournac A, Marie-Nelly H, Marbouty M, Koszul R, & Mozziconacci J. Normalization of a chromosomal contact map. BMC Genomics 13, 436 (2012).
87. Dekker J, & Heard E. Structural and functional diversity of topologically associating domains. FEBS Lett. 589, 2877-2884 (2015).
88. Filippova D, Patro R, Duggal G, & Kingsford C. Identification of alternative topological domains in chromatin. Algorithms Mol. Biol. 9, 14 (2014).
89. Levy-Leduc C, Delattre M, Mary-Huard T, & Robin S. Two-dimensional segmentation for analyzing Hi C data. Bioinformatics 30, i386-i392 (2014).
90. Crane E, et al. Condensin-driven remodelling of X chromosome topology during dosage compensation. Nature 523, 240-244 (2015).
91. Ay F, Bailey T. L, & Noble W. S. Statistical confidence estimation for Hi C data reveals regulatory chromatin contacts. Genome Res. 24, 999-1011 (2014).
92. Mifsud B, et al. GOTHiC, a simple probabilistic model to resolve complex biases and to identify real interactions in Hi C data. Preprint at bioRxiv http://dx.doi.org/10.1101/023317 (2015).
93. Xu Z, et al. A hidden Markov random field based Bayesian method for the detection of long-range chromosomal intereactions in Hi C data. Bioinformatics 32, 650-656 (2015).
94. Lun A. T, & Smyth G. K. diffHic: a bioconductor package to detect differential genomic interactions in Hi C data. BMC Bioinformatics 16, 258 (2015).
95. Robinson M. D, McCarthy D. J, & Smyth G. K. edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140 (2010).
96. Nagano T, et al. Single-cell Hi C for genome-wide detection of chromatin interactions that occur simultaneously in a single cell. Nat. Protoc. 10, 1986-2003 (2015).
97. Dekker J. The three C s of chromosome conformation capture: controls, controls, controls. Nat. Methods 3, 17-21 (2006).
98. Hagege H, et al. Quantitative analysis of chromosome conformation capture assays (3C qPCR). Nat. Protoc. 2, 1722-1733 (2007).
99. Louwers M, Splinter E, van Driel R, de Laat W, & Stam M. Studying physical chromatin interactions in plants using chromosome conformation capture (3C). Nat. Protoc. 4, 1216-1229 (2009).
100. Naumova N, Smith E. M, Zhan Y, & Dekker J. Analysis of long-range chromatin interactions using chromosome conformation capture. Methods 58, 192-203 (2012).
101. Ribeiro de Almeida C, et al. The DNA-binding protein CTCF limits proximal V? recombination and restricts ? enhancer interactions to the immunoglobulin ? light chain locus. Immunity 35, 501-513 (2011).
102. Sqtadhouders R, et al. Multiplexed chromosome conformation capture sequencing for rapid genome-scale high-resolution detection of long-range chromatin interactions. Nat. Protoc. 8, 509-524 (2013).
103. Wurtele H, & Chartrand P. Genome-wide scanning of HoxB1 associated loci in mouse ES cells using an open-ended chromosome conformation capture methodology. Chromosome Res. 14, 477-495 (2006).
104. Harismendy O, et al. 9p21 DNA variants associated with coronary artery disease impair interferon-gamma signalling response. Nature 470 264-268 (2011).
105. Gondor A, Rougier C, & Ohlsson R. High-resolution circular chromosome conformation capture assay. Nat. Protoc. 3, 303-313 (2008).
106. Splinter E, et al. The inactive X chromosome adopts a unique three-dimensional conformation that is dependent on Xist RNA. Genes Dev. 25, 1371-1383 (2011).
107. Gheldof N, Leleu M, Noordermeer D, Rougemont J, & Reymond A. Detecting long-range chromatin interactions using the chromosome conformation capture sequencing (4C seq) method. Methods Mol. Biol. 786, 211-225 (2012).
108. Splinter E, de Wit E, van de Werken H. J, Klous P, & de Laat W. Determining long-range chromatin interactions for selected genomic sites using 4C seq technology: from fixation to computation. Methods 58, 221-230 (2012).
109. Schoenfelder S, et al. Preferential associations between co regulated genes reveal a transcriptional interactome in erythroid cells. Nat. Genet. 42, 53-61 (2010).
110. Sexton T, et al. Sensitive detection of chromatin coassociations using enhanced chromosome conformation capture on chip. Nat. Protoc. 7, 1335-1350 (2012).
111. Ling J. Q, et al. CTCF mediates interchromosomal colocalization between Igf2/H19 and Wsb1/Nf1. Science 312, 269-272 (2006).
112. Ling J, & Hoffman A. R. Associated chromosome trap for identifying long-range DNA interactions. J. Vis. Exp. 50, 2621 (2011).
113. Dostie J, Zhan Y, & Dekker J. Chromosome conformation capture carbon copy technology. Curr. Protoc. Mol. Biol. http://dx.doi.org/10.1002/.0471142727.mb2114s80 (2007).
114. Ferraiuolo M. A, Sanyal A, Naumova N, Dekker J, & Dostie J. From cells to chromatin: capturing snapshots of genome organization with 5C technology. Methods 58, 255-267 (2012).
115. Fraser J, Ethier S. D, Miura H, & Dostie J. A. Torrent of data: mapping chromatin organization using 5C and high-Throughput sequencing. Methods Enzymol. 513, 113-141 (2012).
116. Umbarger M. A. Chromosome conformation capture assays in bacteria. Methods 58, 212-220 (2012).
117. Rodley C. D, Bertels F, Jones B, & O'Sullivan J. M. Global identification of yeast chromosome interactions using genome conformation capture. Fungal Genet. Biol. 46, 879-886 (2009).
118. Duan Z, et al. A genome-wide 3C method for characterizing the three-dimensional architectures of genomes. Methods 58 277-288 (2012).
119. Tanizawa H, et al. Mapping of long-range associations throughout the fission yeast genome reveals global genome organization linked to transcriptional regulation. Nucleic Acids Res. 38, 8164-8177 (2010).