C-ing the Genome: A Compendium of Chromosome Conformation Capture Methods to Study Higher-Order Chromatin Organization

Journal of Cellular Physiology

Volumn 231, Issue 1, 2016, Pages 31-35

  Barutcu, A Rasim ^a   Fritz, Andrew J ^b   Zaidi, Sayyed K ^b   van Wijnen, André J ^c   Lian, Jane B ^b   Stein, Janet L ^b   Nickerson, Jeffrey A ^a   Imbalzano, Anthony N ^a   Stein, Gary S ^b  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^c MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; CHROMOSOME ANALYSIS; CHROMOSOME CONFORMATION CAPTURE; CHROMOSOME CONFORMATION CAPTURE CARBON COPY; CHROMOSOME CONFORMATION CAPTURE METHOD; CHROMOSOME STRUCTURE; CONFORMATION; CROSS LINKING; FLUORESCENCE IN SITU HYBRIDIZATION; GENETIC DISTANCE; GENOME ANALYSIS; HAPLOTYPE; HUMAN; LIMIT OF DETECTION; LUCIFERASE ASSAY; MOLECULAR GENETICS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RESTRICTION FRAGMENT; REVIEW; TRANSCRIPTION REGULATION; ANIMAL; CHEMISTRY; CHROMATIN; DNA REPAIR; DNA REPLICATION; GENETICS; GENOME; MICROSCOPY; PHYSIOLOGY; PROCEDURES;

CHROMATIN; DNA;

ANIMALS; CHROMATIN; DNA; DNA REPAIR; DNA REPLICATION; GENOME; HUMANS; MICROSCOPY;

EID: 84942342259     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.25062     Document Type: Review

References (58)

1. Amano T, Sagai T, Tanabe H, Mizushina Y, Nakazawa H, Shiroishi T. 2009. Chromosomal dynamics at the Shh locus: limb bud-specific differential regulation of competence and active transcription. Dev Cell 16:47-57.
2. Belton JM, McCord RP, Gibcus JH, Naumova N, Zhan Y, Dekker J. 2012. Hi-C: A comprehensive technique to capture the conformation of genomes. Methods 58:268-276.
3. Bolzer A, Kreth G, Solovei I, Koehler D, Saracoglu K, Fauth C, Muller S, Eils R, Cremer C, Speicher MR, Cremer T. 2005. Three-dimensional maps of all chromosomes in human male fibroblast nuclei and prometaphase rosettes. PLoS Biol 3:e157.
4. Branco MR, Pombo A. 2006. Intermingling of chromosome territories in interphase suggests role in translocations and transcription-dependent associations. PLoS Biol 4:e138.
5. Cremer T, Cremer C, Baumann H, Luedtke EK, Sperling K, Teuber V, Zorn C. 1982. Rabl's model of the interphase chromosome arrangement tested in Chinese hamster cells by premature chromosome condensation and laser-UV-microbeam experiments. Hum Genet 60:46-56.
6. Cremer T, Cremer M, Dietzel S, Muller S, Solovei I, Fakan S. 2006. Chromosome territories-a functional nuclear landscape. Curr Opinin Cell Biol 18:307-316.
7. Cullen KE, Kladde MP, Seyfred MA. 1993. Interaction between transcription regulatory regions of prolactin chromatin. Science 261:203-206.
8. de Wit E, de Laat W. 2012. A decade of 3C technologies: Insights into nuclear organization. Genes Dev 26:11-24.
9. Dekker J 2006. The three 'C' s of chromosome conformation capture: Controls, controls, controls. Nat Methods 3:17-21.
10. Dekker J, Marti-Renom MA, Mirny LA. 2013. Exploring the three-dimensional organization of genomes: Interpreting chromatin interaction data. Nat Rev Genet 14:390-403.
11. Dekker J, Rippe K, Dekker M, Kleckner N. 2002. Capturing chromosome conformation. Science 295:1306-1311.
12. Dixon JR, Jung I, Selvaraj S, Shen Y, Antosiewicz-Bourget JE, Lee AY, Ye Z, Kim A, Rajagopal N, Xie W, Diao Y, Liang J, Zhao H, Lobanenkov VV, Ecker JR, Thomson JA, Ren B. 2015. Chromatin architecture reorganization during stem cell differentiation. Nature 518:331-336.
13. Dixon JR, Selvaraj S, Yue F, Kim A, Li Y, Shen Y, Hu M, Liu JS, Ren B. 2012. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485:376-380.
14. Dostie J, Richmond TA, Arnaout RA, Selzer RR, Lee WL, Honan TA, Rubio ED, Krumm A, Lamb J, Nusbaum C, Green RD, Dekker J. 2006. Chromosome Conformation Capture Carbon Copy (5C): A massively parallel solution for mapping interactions between genomic elements. Genome Res 16:1299-1309.
15. Dryden NH, Broome LR, Dudbridge F, Johnson N, Orr N, Schoenfelder S, Nagano T, Andrews S, Wingett S, Kozarewa I, Assiotis I, Fenwick K, Maguire SL, Campbell J, Natrajan R, Lambros M, Perrakis E, Ashworth A, Fraser P, Fletcher O. 2014. Unbiased analysis of potential targets of breast cancer susceptibility loci by Capture Hi-C. Genome Res 24:1854-1868.
16. Ferraiuolo MA, Sanyal A, Naumova N, Dekker J, Dostie J. 2012. From cells to chromatin: Capturing snapshots of genome organization with 5C technology. Methods 58:255-267.
17. Fullwood MJ, Liu MH, Pan YF, Liu J, Xu H, Mohamed YB, Orlov YL, Velkov S, Ho A, Mei PH, Chew EG, Huang PY, Welboren WJ, Han Y, Ooi HS, Ariyaratne PN, Vega VB, Luo Y, Tan PY, Choy PY, Wansa KD, Zhao B, Lim KS, Leow SC, Yow JS, Joseph R, Li H, Desai KV, Thomsen JS, Lee YK, Karuturi RK, Herve T, Bourque G, Stunnenberg HG, Ruan X, Cacheux-Rataboul V, Sung WK, Liu ET, Wei CL, Cheung E, Ruan Y. 2009. An oestrogen-receptor-alpha-bound human chromatin interactome. Nature 462:58-64.
18. Furlan-Magaril M, Varnai C, Nagano T, Fraser P. 2015. 3D genome architecture from populations to single cells. Curr Opin Genet Dev 31:36-41.
19. Gibcus JH, Dekker J. 2013. The hierarchy of the 3D genome. Mol Cell 49:773-782.
20. Giorgetti L, Galupa R, Nora EP, Piolot T, Lam F, Dekker J, Tiana G, Heard E. 2014. Predictive polymer modeling reveals coupled fluctuations in chromosome conformation and transcription. Cell 157:950-963.
21. Handoko L, Xu H, Li G, Ngan CY, Chew E, Schnapp M, Lee CW, Ye C, Ping JL, Mulawadi F, Wong E, Sheng J, Zhang Y, Poh T, Chan CS, Kunarso G, Shahab A, Bourque G, Cacheux-Rataboul V, Sung WK, Ruan Y, Wei CL. 2011. CTCF-mediated functional chromatin interactome in pluripotent cells. Nat Genet 43:630-638.
22. Harada A, Mallappa C, Okada S, Butler JT, Baker SP, Lawrence JB, Ohkawa Y, Imbalzano AN. 2015. Spatial re-organization of myogenic regulatory sequences temporally controls gene expression. Nucleic Acids Res 43:2008-2021.
23. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. 2010. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 38:576-589.
24. Jin F, Li Y, Dixon JR, Selvaraj S, Ye Z, Lee AY, Yen CA, Schmitt AD, Espinoza CA, Ren B. 2013. A high-resolution map of the three-dimensional chromatin interactome in human cells. Nature 503:290-294.
25. Kaikkonen MU, Niskanen H, Romanoski CE, Kansanen E, Kivela AM, Laitalainen J, Heinz S, Benner C, Glass CK, Yla-Herttuala S. 2014. Control of VEGF-A transcriptional programs by pausing and genomic compartmentalization. Nucleic Acids Res 42:12570-12584.
26. Kalhor R, Tjong H, Jayathilaka N, Alber F, Chen L. 2012. Genome architectures revealed by tethered chromosome conformation capture and population-based modeling. Nat Biotechnol 30:90-98.
27. Lajoie BR, Dekker J, Kaplan N. 2015. The Hitchhiker's guide to Hi-C analysis: Practical guidelines. Methods 72:65-75.
28. Le Dily F, Bau D, Pohl A, Vicent GP, Serra F, Soronellas D, Castellano G, Wright RH, Ballare C, Filion G, Marti-Renom MA, Beato M. 2014. Distinct structural transitions of chromatin topological domains correlate with coordinated hormone-induced gene regulation. Genes Dev 28:2151-2162.
29. Li G, Ruan X, Auerbach RK, Sandhu KS, Zheng M, Wang P, Poh HM, Goh Y, Lim J, Zhang J, Sim HS, Peh SQ, Mulawadi FH, Ong CT, Orlov YL, Hong S, Zhang Z, Landt S, Raha D, Euskirchen G, Wei CL, Ge W, Wang H, Davis C, Fisher-Aylor KI, Mortazavi A, Gerstein M, Gingeras T, Wold B, Sun Y, Fullwood MJ, Cheung E, Liu E, Sung WK, Snyder M, Ruan Y. 2012. Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell 148:84-98.
30. 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. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326:289-293.
31. McCord RP, Nazario-Toole A, Zhang H, Chines PS, Zhan Y, Erdos MR, Collins FS, Dekker J, Cao K. 2013. Correlated alterations in genome organization, histone methylation, and DNA-lamin A/C interactions in Hutchinson-Gilford progeria syndrome. Genome Res 23:260-269.
32. Montavon T, Soshnikova N, Mascrez B, Joye E, Thevenet L, Splinter E, de Laat W, Spitz F, Duboule D. 2011. A regulatory archipelago controls Hox genes transcription in digits. Cell 147:1132-1145.
33. Nagano T, Lubling Y, Stevens TJ, Schoenfelder S, Yaffe E, Dean W, Laue ED, Tanay A, Fraser P. 2013. Single-cell Hi-C reveals cell-to-cell variability in chromosome structure. Nature 502:59-64.
34. Naumova N, Imakaev M, Fudenberg G, Zhan Y, Lajoie BR, Mirny LA, Dekker J. 2013. Organization of the mitotic chromosome. Science 342:948-953.
35. Naumova N, Smith EM, Zhan Y, Dekker J. 2012. Analysis of long-range chromatin interactions using Chromosome Conformation Capture. Methods 58:192-203.
36. Noordermeer D, Leleu M, Splinter E, Rougemont J, De Laat W, Duboule D. 2011. The dynamic architecture of Hox gene clusters. Science 334:222-225.
37. Nora EP, Dekker J, Heard E. 2013. Segmental folding of chromosomes: A basis for structural and regulatory chromosomal neighborhoods?. BioEssays 35:818-828.
38. Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I, Servant N, Piolot T, van Berkum NL, Meisig J, Sedat J, Gribnau J, Barillot E, Bluthgen N, Dekker J, Heard E. 2012. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485:381-385.
39. Phillips-Cremins JE, Sauria ME, Sanyal A, Gerasimova TI, Lajoie BR, Bell JS, Ong CT, Hookway TA, Guo C, Sun Y, Bland MJ, Wagstaff W, Dalton S, McDevitt TC, Sen R, Dekker J, Taylor J, Corces VG. 2013. Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 153:1281-1295.
40. Rao SS, Huntley MH, Durand NC, Stamenova EK, Bochkov ID, Robinson JT, Sanborn AL, Machol I, Omer AD, Lander ES, Aiden EL. 2014. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159:1665-1680.
41. Rousseau M, Ferraiuolo MA, Crutchley JL, Wang XQ, Miura H, Blanchette M, Dostie J. 2014. Classifying leukemia types with chromatin conformation data. Genome Biol 15:R60.
42. Sanyal A, Lajoie BR, Jain G, Dekker J. 2012. The long-range interaction landscape of gene promoters. Nature 489:109-113.
43. Schoenfelder S, Furlan-Magaril M, Mifsud B, Tavares-Cadete F, Sugar R, Javierre BM, Nagano T, Katsman Y, Sakthidevi M, Wingett SW, Dimitrova E, Dimond A, Edelman LB, Elderkin S, Tabbada K, Darbo E, Andrews S, Herman B, Higgs A, LeProust E, Osborne CS, Mitchell JA, Luscombe NM, Fraser P. 2015. The pluripotent regulatory circuitry connecting promoters to their long-range interacting elements. Genome Res 25:582-597.
44. Seitan VC, Faure AJ, Zhan Y, McCord RP, Lajoie BR, Ing-Simmons E, Lenhard B, Giorgetti L, Heard E, Fisher AG, Flicek P, Dekker J, Merkenschlager M. 2013. Cohesin-based chromatin interactions enable regulated gene expression within preexisting architectural compartments. Genome Res 23:2066-2077.
45. Sexton T, Kurukuti S, Mitchell JA, Umlauf D, Nagano T, Fraser P. 2012. Sensitive detection of chromatin coassociations using enhanced chromosome conformation capture on chip. Nat Protoc 7:1335-1350.
46. Simonis M, Klous P, Splinter E, Moshkin Y, Willemsen R, de Wit E, van Steensel B, 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.
47. Simonis M, Kooren J, de Laat W. 2007. An evaluation of 3C-based methods to capture DNA interactions. Nat Methods 4:895-901.
48. Spilianakis CG, Lalioti MD, Town T, Lee GR, Flavell RA. 2005. Interchromosomal associations between alternatively expressed loci. Nature 435:637-645.
49. Splinter E, de Wit E, van de Werken HJ, Klous P, de Laat W. 2012. Determining long-range chromatin interactions for selected genomic sites using 4C-seq technology: From fixation to computation. Methods 58:221-230.
50. Tiwari VK, Cope L, McGarvey KM, Ohm JE, Baylin SB. 2008. A novel 6C assay uncovers Polycomb-mediated higher order chromatin conformations. Genome Res 18:1171-1179.
51. van de Werken HJ, de Vree PJ, Splinter E, Holwerda SJ, Klous P, de Wit E, de Laat W. 2012. 4C technology: Protocols and data analysis. Methods Enzymol 513:89-112.
52. Vietri Rudan M, Barrington C, Henderson S, Ernst C, Odom DT, Tanay A, Hadjur S. 2015. Comparative Hi-C reveals that CTCF underlies evolution of chromosomal domain architecture. Cell Rep 10:1297-1309.
53. Wei Z, Gao F, Kim S, Yang H, Lyu J, An W, Wang K, Lu W. 2013. Klf4 organizes long-range chromosomal interactions with the oct4 locus in reprogramming and pluripotency. Cell Stem Cell 13:36-47.
54. Williamson I, Berlivet S, Eskeland R, Boyle S, Illingworth RS, Paquette D, Dostie J, Bickmore WA. 2014. Spatial genome organization: Contrasting views from chromosome conformation capture and fluorescence in situ hybridization. Genes Dev 28:2778-2791.
55. Wurtele H, Chartrand P. 2006. Genome-wide scanning of HoxB1-associated loci in mouse ES cells using an open-ended Chromosome Conformation Capture methodology. Chromosome Res 14:477-495.
56. Zeitz MJ, Ay F, Heidmann JD, Lerner PL, Noble WS, Steelman BN, Hoffman AR. 2013. Genomic interaction profiles in breast cancer reveal altered chromatin architecture. PLoS ONE 8:e73974.
57. Zhang Y, McCord RP, Ho YJ, Lajoie BR, Hildebrand DG, Simon AC, Becker MS, Alt FW, Dekker J. 2012. Spatial organization of the mouse genome and its role in recurrent chromosomal translocations. Cell 148:908-921.
58. Zhao Z, Tavoosidana G, Sjolinder M, Gondor A, Mariano P, Wang S, Kanduri C, Lezcano M, Sandhu KS, Singh U, Pant V, Tiwari V, Kurukuti S, Ohlsson R. 2006. Circular chromosome conformation capture (4C) uncovers extensive networks of epigenetically regulated intra-and interchromosomal interactions. Nat Genet 38:1341-1347.