Characterization of hundreds of regulatory landscapes in developing limbs reveals two regimes of chromatin folding

Genome Research

Volumn 27, Issue 2, 2017, Pages 223-233

  Andrey, Guillaume ^a   Schöpflin, Robert ^a   Jerković, Ivana ^a   Heinrich, Verena ^a   Ibrahim, Daniel M ^a,b   Paliou, Christina ^a   Hochradel, Myriam ^a   Timmermann, Bernd ^a   Haas, Stefan ^a   Vingron, Martin ^a   Mundlos, Stefan ^a,b  

^a MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BMP PROTEIN; COL1A1 PROTEIN; FGF PROTEIN; HOX PROTEIN; MYOD1 PROTEIN; PROTEIN; RA PROTEIN; RNA; TRANSCRIPTION FACTOR CTCF; TRANSCRIPTION FACTOR RUNX; TRANSCRIPTION FACTOR SOX; TRANSCRIPTION FACTOR SOX9; TRANSCRIPTION FACTOR TBX; UNCLASSIFIED DRUG; WNT PROTEIN; HISTONE; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CHROMATIN; EMBRYO DEVELOPMENT; ENHANCER REGION; FORELIMB; GENE EXPRESSION; GENE LOCUS; HINDLIMB; HISTONE MODIFICATION; LIMB DEVELOPMENT; MESENCEPHALON; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RNA SEQUENCE; THREE DIMENSIONAL IMAGING; ANIMAL; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIMB; TRANSCRIPTION INITIATION;

ANIMALS; BINDING SITES; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; ENHANCER ELEMENTS, GENETIC; EXTREMITIES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONES; MICE; PROMOTER REGIONS, GENETIC; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 85013025290     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.213066.116     Document Type: Article

References (56)

1. Acemel RD, Tena JJ, Irastorza-Azcarate I, Marletaz F, Gomez-Marin C, de la Calle-Mustienes E, Bertrand S, Diaz SG, Aldea D, Aury JM, et al. 2016. A single three-dimensional chromatin compartment in amphioxus indicates a stepwise evolution of vertebrate Hox bimodal regulation. Nat Genet 48: 336-341.
2. Andrey G, Montavon T, Mascrez B, Gonzalez F, Noordermeer D, Leleu M, Trono D, Spitz F, Duboule D. 2013. A switch between topological domains underlies HoxD genes collinearity in mouse limbs. Science 340: 1234167.
3. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K. 2007. High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837.
4. Bell DM, Leung KK, Wheatley SC, Ng LJ, Zhou S, Ling KW, Sham MH, Koopman P, Tam PP, Cheah KS. 1997. SOX9 directly regulates the type-II collagen gene. Nat Genet 16: 174-178.
5. Birnbaum RY, Everman DB, Murphy KK, Gurrieri F, Schwartz CE, Ahituv N. 2012. Functional characterization of tissue-specific enhancers in the DLX5/6 locus. Hum Mol Genet 21: 4930-4938.
6. Cairns J, Freire-Pritchett P, Wingett SW, Varnai C, Dimond A, Plagnol V, Zerbino D, Schoenfelder S, Javierre BM, Osborne C, et al. 2016. CHiCAGO: robust detection of DNA looping interactions in Capture Hi-C data. Genome Biol 17: 127.
7. de Laat W, Duboule D. 2013. Topology of mammalian developmental enhancers and their regulatory landscapes. Nature 502: 499-506.
8. Dekker J, Rippe K, Dekker M, Kleckner N. 2002. Capturing chromosome conformation. Science 295: 1306-1311.
9. Denholtz M, Bonora G, Chronis C, Splinter E, de Laat W, Ernst J, Pellegrini M, Plath K. 2013. Long-range chromatin contacts in embryonic stem cells reveal a role for pluripotency factors and Polycomb proteins in genome organization. Cell Stem Cell 13: 602-616.
10. Diez-Roux G, Banfi S, Sultan M, Geffers L, Anand S, Rozado D, Magen A, Canidio E, Pagani M, Peluso I, et al. 2011. A high-resolution anatomical atlas of the transcriptome in the mouse embryo. PLoS Biol 9: e1000582.
11. 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.
12. Dixon JR, Jung I, Selvaraj S, Shen Y, Antosiewicz-Bourget JE, Lee AY, Ye Z, Kim A, Rajagopal N, Xie W, et al. 2015. Chromatin architecture reorganization during stem cell differentiation. Nature 518: 331-336.
13. Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, Batut P, Chaisson M, Gingeras TR. 2013. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29: 15-21.
14. Florini JR, Ewton DZ, Coolican SA. 1996. Growth hormone and the insulinlike growth factor system in myogenesis. Endocr Rev 17: 481-517.
15. Fudenberg G, Imakaev M, Lu C, Goloborodko A, Abdennur N, Mirny LA. 2016. Formation of chromosomal domains by loop extrusion. Cell Rep 15: 2038-2049.
16. Ghavi-Helm Y, Klein FA, Pakozdi T, Ciglar L, Noordermeer D, Huber W, Furlong EE. 2014. Enhancer loops appear stable during development and are associated with paused polymerase. Nature 512: 96-100.
17. Giorgetti L, Galupa R, Nora EP, Piolot T, Lam F, Dekker J, Tiana G, Heard E. 2014. Predictive polymer modeling reveals coupled fluctuationsinchromosome conformation and transcription. Cell 157: 950-963.
18. Giorgetti L, Lajoie BR, Carter AC, Attia M, Zhan Y, Xu J, Chen CJ, Kaplan N, Chang HY, Heard E, et al. 2016. Structural organization of the inactive X chromosome in the mouse. Nature 535: 575-579.
19. Hadjur S, Williams LM, Ryan NK, Cobb BS, Sexton T, Fraser P, Fisher AG, Merkenschlager M. 2009. Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus. Nature 460: 410-413.
20. Hagege H, Klous P, Braem C, Splinter E, Dekker J, Cathala G, de Laat W, Forne T. 2007. Quantitative analysis of chromosome conformation capture assays (3C-qPCR). Nat Protoc 2: 1722-1733.
21. Hansen P, Hecht J, Ibrahim DM, Krannich A, Truss M, Robinson PN. 2015. Saturation analysis of ChIP-seq data for reproducible identification of binding peaks. Genome Res 25: 1391-1400.
22. Hughes JR, Roberts N, McGowan S, Hay D, Giannoulatou E, Lynch M, De Gobbi M, Taylor S, Gibbons R, Higgs DR. 2014. Analysis of hundreds of cis-regulatory landscapes at high resolution in a single, high-throughput experiment. Nat Genet 46: 205-212.
23. Joshi O, Wang SY, Kuznetsova T, Atlasi Y, Peng T, Fabre PJ, Habibi E, Shaik J, Saeed S, Handoko L, et al. 2015. Dynamic reorganization of extremely long-range promoter-promoter interactions between two states of pluripotency. Cell Stem Cell 17: 748-757.
24. Kharchenko PV, Tolstorukov MY, Park PJ. 2008. Design and analysis of ChIP-seq experiments for DNA-binding proteins. Nat Biotechnol 26: 1351-1359.
25. Kowalczyk MS, Hughes JR, Garrick D, Lynch MD, Sharpe JA, Sloane-Stanley JA, McGowan SJ, De Gobbi M, Hosseini M, Vernimmen D, et al. 2012. Intragenic enhancers act as alternative promoters. Mol Cell 45: 447-458.
26. La Manno G, Gyllborg D, Codeluppi S, Nishimura K, Salto C, Zeisel A, Borm LE, Stott SR, Toledo EM, Villaescusa JC, et al. 2016. Molecular diversity of midbrain development in mouse, human, and stem cells. Cell 167: 566-580.e519.
27. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357-359.
28. Lawrence M, Huber W, Pages H, Aboyoun P, Carlson M, Gentleman R, Morgan MT, Carey VJ. 2013. Software for computing and annotating genomic ranges. PLoS Comput Biol 9: e1003118.
29. Lee TI, Johnstone SE, Young RA. 2006. Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat Protoc 1: 729-748.
30. Lettice LA, Heaney SJ, Purdie LA, Li L, de Beer P, Oostra BA, Goode D, Elgar G, Hill RE, de Graaff E. 2003. A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Hum Mol Genet 12: 1725-1735.
31. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO, et al. 2009. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326: 289-293.
32. Londhe P, Davie JK. 2011. Γ interferon modulates myogenesis through the major histocompatibility complex class II transactivator, CIITA. Mol Cell Biol 31: 2854-2866.
33. Lonfat N, Duboule D. 2015. Structure, function and evolution of topologically associating domains (TADs) at HOX loci. FEBS Lett 589(20 Pt A): 2869-2876.
34. Lonfat N, Montavon T, Darbellay F, Gitto S, Duboule D. 2014. Convergent evolution of complex regulatory landscapes and pleiotropy at Hox loci. Science 346: 1004-1006.
35. Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15: 550.
36. Lupianez DG, Kraft K, Heinrich V, Krawitz P, Brancati F, Klopocki E, Horn D, Kayserili H, Opitz JM, Laxova R, et al. 2015. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161: 1012-1025.
37. Mammana A, Chung HR. 2015. Chromatin segmentation based on a probabilistic model for read counts explains a large portion of the epigenome. Genome Biol 16: 151.
38. Merkenschlager M, Nora EP. 2016. CTCF and cohesin in genome folding and transcriptional gene regulation. Annu Rev Genomics Hum Genet 17: 17-43.
39. 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.
40. Montavon T, Thevenet L, Duboule D. 2012. Impact of copy number variations (CNVs) on long-range gene regulation at the HoxD locus. Proc Natl Acad Sci 109: 20204-20211.
41. Nitzsche A, Paszkowski-Rogacz M, Matarese F, Janssen-Megens EM, Hubner NC, Schulz H, de Vries I, Ding L, Huebner N, Mann M, et al. 2011. RAD21 cooperates with pluripotency transcription factors in the maintenance of embryonic stem cell identity. PLoS One 6: e19470.
42. 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.
43. Noordermeer D, Leleu M, Schorderet P, Joye E, Chabaud F, Duboule D. 2014. Temporal dynamics and developmental memory of 3D chromatin architecture at Hox gene loci. eLife 3: e02557.
44. Nora EP, Lajoie BR, Schulz EG, Giorgetti L, Okamoto I, Servant N, Piolot T, van Berkum NL, Meisig J, Sedat J, et al. 2012. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485: 381-385.
45. Osterwalder M, Speziale D, Shoukry M, Mohan R, Ivanek R, Kohler M, Beisel C, Wen X, Scales SJ, Christoffels VM, et al. 2014. HAND2 targets define a network of transcriptional regulators that compartmentalize the early limb bud mesenchyme. Dev Cell 31: 345-357.
46. Phillips-Cremins JE, Sauria ME, Sanyal A, Gerasimova TI, Lajoie BR, Bell JS, Ong CT, Hookway TA, Guo C, Sun Y, et al. 2013. Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 153: 1281-1295.
47. Rao SS, Huntley MH, Durand NC, Stamenova EK, Bochkov ID, Robinson JT, Sanborn AL, Machol I, Omer AD, Lander ES, et al. 2014. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159: 1665-1680.
48. Sanborn AL, Rao SS, Huang SC, Durand NC, Huntley MH, Jewett AI, Bochkov ID, Chinnappan D, Cutkosky A, Li J, et al. 2015. Chromatin extrusion explains key features of loop and domain formation inwild-type and engineered genomes. Proc Natl Acad Sci 112: E6456-E6465.
49. Schoenfelder S, Sugar R, Dimond A, Javierre BM, Armstrong H, Mifsud B, Dimitrova E, Matheson L, Tavares-Cadete F, Furlan-Magaril M, et al. 2015. Polycomb repressive complex PRC1 spatially constrains the mouse embryonic stem cell genome. Nat Genet 47: 1179-1186.
50. Seitan VC, Faure AJ, Zhan Y, McCord RP, Lajoie BR, Ing-Simmons E, Lenhard B, Giorgetti L, Heard E, Fisher AG, et al. 2013. Cohesin-based chromatin interactions enable regulated gene expression within preexisting architectural compartments. Genome Res 23: 2066-2077.
51. Sexton T, Yaffe E, Kenigsberg E, Bantignies F, Leblanc B, Hoichman M, Parrinello H, Tanay A, Cavalli G. 2012. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148: 458-472.
52. Tang Z, Luo OJ, Li X, Zheng M, Zhu JJ, Szalaj P, Trzaskoma P, Magalska A, Wlodarczyk J, Ruszczycki B, et al. 2015. CTCF-mediated human 3D genome architecture reveals chromatin topology for transcription. Cell 163: 1611-1627.
53. Vieux-Rochas M, Fabre PJ, Leleu M, Duboule D, Noordermeer D. 2015. Clustering of mammalian Hox genes with other H3K27me3 targets within an active nuclear domain. Proc Natl Acad Sci 112: 4672-4677.
54. Visel A, Minovitsky S, Dubchak I, Pennacchio LA. 2007. VISTA Enhancer Browser - a database of tissue-specific human enhancers. Nucleic Acids Res 35: D88-D92.
55. Wingett S, Ewels P, Furlan-Magaril M, Nagano T, Schoenfelder S, Fraser P, Andrews S. 2015. HiCUP: pipeline for mapping and processing Hi-C data. F1000Res 4: 1310.
56. Zeller R, Lopez-Rios J, Zuniga A. 2009. Vertebrate limb bud development: moving towards integrative analysis of organogenesis. Nat Rev Genet 10: 845-858.