Formation of new chromatin domains determines pathogenicity of genomic duplications

Nature

Volumn 538, Issue 7624, 2016, Pages 265-269

  Franke, Martin ^a,b   Ibrahim, Daniel M ^a,b,c   Andrey, Guillaume ^a   Schwarzer, Wibke ^d   Heinrich, Verena ^a,b   Schöpflin, Robert ^a   Kraft, Katerina ^a,b   Kempfer, Rieke ^a   Jerković, Ivana ^a,b   Chan, Wing Lee ^b   Spielmann, Malte ^a,b   Timmermann, Bernd ^a   Wittler, Lars ^a   Kurth, Ingo ^e,f   Cambiaso, Paola ^g   Zuffardi, Orsetta ^h   Houge, Gunnar ⁱ   Lambie, Lindsay ^j   Brancati, Francesco ^k,l   Pombo, Ana ^c,m   Vingron, Martin ^a   Spitz, Francois ^d   Mundlos, Stefan ^a,b,c   more..

^a MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c BERLIN INSTITUTE OF HEALTH   (Germany)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^e JENA UNIVERSITY HOSPITAL   (Germany)

^f UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^g BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^h UNIVERSITY OF PAVIA   (Italy)

ⁱ HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^j UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^k UNIVERSITY OF L'AQUILA   (Italy)

^l LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

^m MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

more..

Author keywords

[No Author keywords available]

Indexed keywords

INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1; TRANSCRIPTION FACTOR SOX9; DNA; SOX9 PROTEIN, MOUSE;

CANCER; CELLS AND CELL COMPONENTS; CHROMOSOME; GENE EXPRESSION; GENETIC ANALYSIS; GENOME; MOLECULAR ANALYSIS; PATHOGENICITY; PATHOLOGY; PHENOTYPE; RODENT;

ALLELE; ANIMAL CELL; ARTICLE; CHROMATIN STRUCTURE; CONFORMATION; CONTROLLED STUDY; CRISPR CAS SYSTEM; EMBRYO; GENE; GENE DUPLICATION; GENE EXPRESSION; GENE LOCATION; GENE LOCUS; GENETIC ANALYSIS; GENETIC STABILITY; HUMAN; HUMAN CELL; KCNJ2 GENE; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; SINGLE NUCLEOTIDE POLYMORPHISM; SOX9 GENE; UPREGULATION; ABNORMALITIES; ANIMAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; COPY NUMBER VARIATION; DISEASES; FACIES; FEMALE; FIBROBLAST; FINGER; FOOT MALFORMATION; GENETICS; GENOMICS; HAND MALFORMATION; MALE;

MUS;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DISEASE; DNA; DNA COPY NUMBER VARIATIONS; FACIES; FEMALE; FIBROBLASTS; FINGERS; FOOT DEFORMITIES, CONGENITAL; GENE DUPLICATION; GENE EXPRESSION; GENOMICS; HAND DEFORMITIES, CONGENITAL; MALE; MICE; PHENOTYPE; SOX9 TRANSCRIPTION FACTOR;

EID: 84991727599     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature19800     Document Type: Article

References (37)

1. Nora, E. P. et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485, 381-385 (2012).
2. Dixon, J. R. et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376-380 (2012).
3. Lupiáñez, D. G. et al. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161, 1012-1025 (2015).
4. Symmons, O. et al. Functional and topological characteristics of mammalian regulatory domains. Genome Res. 24, 390-400 (2014).
5. 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).
6. Benko, S. et al. Disruption of a long distance regulatory region upstream of SOX9 in isolated disorders of sex development. J. Med. Genet. 48, 825-830 (2011).
7. Wagner, T. et al. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 79, 1111-1120 (1994).
8. Kurth, I. et al. Duplications of noncoding elements 5' of SOX9 are associated with brachydactyly-anonychia. Nature Genet. 41, 862-863 (2009).
9. Gordon, C. T. et al. Long-range regulation at the SOX9 locus in development and disease. J. Med. Genet. 46, 649-656 (2009).
10. Kim, G.-J. et al. Copy number variation of two separate regulatory regions upstream of SOX9 causes isolated 46,XY or 46,XX disorder of sex development. J. Med. Genet. 52, 240-247 (2015).
11. Sekido, R. & Lovell-Badge, R. Sex determination involves synergistic action of SRY and SF1 on a specific Sox9 enhancer. Nature 453, 930-934 (2008).
12. Dahal, G. R. et al. An inwardly rectifying K+ channel is required for patterning. Development 139, 3653-3664 (2012).
13. Mundlos, S. The brachydactylies: a molecular disease family. Clin. Genet. 76, 123-136 (2009).
14. 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).
15. Guo, Y. et al. CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function. Cell 162, 900-910 (2015).
16. Lupski, J. R. Genomic rearrangements and sporadic disease. Nature Genet. 39 (Suppl), S43-S47 (2007).
17. Stephens, P. J. et al. Complex landscapes of somatic rearrangement in human breast cancer genomes. Nature 462, 1005-1010 (2009).
18. Ohno, S. Evolution by Gene Duplication (Springer, 1970).
19. Katju, V. & Bergthorsson, U. Copy-number changes in evolution: rates, fitness effects and adaptive significance. Front. Genet. 4, 273 (2013).
20. Kraft, K. et al. Deletions, inversions, duplications: engineering of structural variants using CRISPR/Cas in Mice. Cell Reports 10, 833-839 (2015).
21. Artus, J. & Hadjantonakis, A.-K. in Transgenic Mouse Methods and Protocols Vol. 693 Methods in Molecular Biology (eds Hofker, M. H. & van Deursen, J.) Ch. 3, 37-56 (Humana Press, 2011).
22. Ruf, S. et al. Large-scale analysis of the regulatory architecture of the mouse genome with a transposon-associated sensor. Nature Genet. 43, 379-386 (2011).
23. Hooper, M., Hardy, K., Handyside, A., Hunter, S. & Monk, M. HPRT-deficient (Lesch-Nyhan) mouse embryos derived from germline colonization by cultured cells. Nature 326, 292-295 (1987).
24. Nagy, K. & Nichols, J. in Advanced Protocols for Animal Transgenesis (eds Pease, S. & Saunders, T. L.) Ch. 18, 431-455 (Springer, 2011).
25. van de Werken, H. J. G. et al. in Methods in Enzymology Vol. 513 (eds Wu, C. & Allis, D. C.) 89-112 (Academic Press, 2012).
26. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
27. McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303 (2010).
28. Wingett, S. et al. HiCUP: pipeline for mapping and processing Hi-C data. F1000Res. 4, 1310 (2015).
29. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359 (2012).
30. Zhou, X. et al. Exploring long-range genome interactions using the WashU Epigenome Browser. Nature Methods 10, 375-376 (2013).
31. Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15-21 (2013).
32. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
33. Bhatia, S. et al. Functional assessment of disease-associated regulatory variants in vivo using a versatile dual colour transgenesis strategy in zebrafish. PLoS Genet. 11, e1005193 (2015).
34. Benko, S. et al. Highly conserved non-coding elements on either side of SOX9 associated with Pierre Robin sequence. Nature Genet. 41, 359-364 (2009).
35. Visel, A., Minovitsky, S., Dubchak, I. & Pennacchio, L. A. VISTA Enhancer Browser - a database of tissue-specific human enhancers. Nucleic Acids Res. 35, D88-D92 (2007).
36. Gordon, C. T. et al. Identification of novel craniofacial regulatory domains located far upstream of SOX9 and disrupted in Pierre Robin sequence. Hum. Mutat. 35, 1011-1020 (2014).
37. Yao, B. et al. The SOX9 upstream region prone to chromosomal aberrations causing campomelic dysplasia contains multiple cartilage enhancers. Nucleic Acids Res. 43, 5394-5408 (2015).