Breaking TADs: How Alterations of Chromatin Domains Result in Disease

Trends in Genetics

Volumn 32, Issue 4, 2016, Pages 225-237

  Lupiáñez, Darío G ^a,b   Spielmann, Malte ^a,b   Mundlos, Stefan ^a,b  

^a MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

CRISPR Cas; Disease; Long range regulation; Structural variations; TAD; Topologically associating domains

Indexed keywords

CDK5 REGULATORY SUBUNIT ASSOCIATED PROTEIN 1 LIKE 1; COHESIN; DNA; EPHRIN RECEPTOR A4; FORKHEAD TRANSCRIPTION FACTOR; MEMBRANE BOUND O ACYLTRANSFERASE DOMAIN CONTAINING 1; OSTEOGENIC PROTEIN 1; PROTEIN; RNA POLYMERASE II; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR AP 2; TRANSCRIPTION FACTOR CTCF; TRANSCRIPTION FACTOR E2F3; TRANSCRIPTION FACTOR FOXG1; TRANSCRIPTION FACTOR PAX3; TRANSCRIPTION FACTOR SOX4; UNCLASSIFIED DRUG; WNT6 PROTEIN; CHROMATIN;

ACROPECTOROVERTEBRAL DYSGENESIS; ADULT ONSET DEMYELINATING LEUKODYSTROPHY; BONE DISEASE; CELL NUCLEUS; CHROMATIN STRUCTURE; CHROMOSOME STRUCTURE; CONGENITAL MALFORMATION; COPY NUMBER VARIATION; CRISPR CAS SYSTEM; DNA REPLICATION; DNA STRUCTURE; EMBRYO DEVELOPMENT; ENHANCER REGION; GENE CONTROL; GENE DELETION; GENE EXPRESSION; GENOME ANALYSIS; HOX GENE; HUMAN; LEUKODYSTROPHY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY SEQUENCE; RETT SYNDROME; REVIEW; RNA EDITING; TOPOLOGICALLY ASSOCIATING DOMAIN; CHEMISTRY; CHROMATIN; GENETIC PREDISPOSITION; GENETICS;

CHROMATIN; GENETIC PREDISPOSITION TO DISEASE; HUMANS;

EID: 84956894592     PISSN: 01689525     EISSN: 13624555     Source Type: Journal    
DOI: 10.1016/j.tig.2016.01.003     Document Type: Review

References (95)

1. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74. ENCODE Project Consortium.
2. Kothary R., et al. A transgene containing lacZ inserted into the dystonia locus is expressed in neural tube. Nature 1988, 335:435-437.
3. Kothary R., et al. Inducible expression of an hsp68-lacZ hybrid gene in transgenic mice. Development 1989, 105:707-714.
4. Visel A., et al. VISTA Enhancer Browser - a database of tissue-specific human enhancers. Nucleic Acids Res. 2007, 35:D88-D92.
5. de Laat W., Duboule D. Topology of mammalian developmental enhancers and their regulatory landscapes. Nature 2013, 502:499-506.
6. Bulger M., Groudine M. Functional and mechanistic diversity of distal transcription enhancers. Cell 2011, 144:327-339.
7. Cremer T., Cremer M. Chromosome territories. Cold Spring Harb. Perspect. Biol. 2010, 2:a003889.
8. Lieberman-Aiden E., et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 2009, 326:289-293.
9. Bickmore W.A., van Steensel B. Genome architecture: domain organization of interphase chromosomes. Cell 2013, 152:1270-1284.
10. Gibcus J.H., Dekker J. The hierarchy of the 3D genome. Mol. Cell 2013, 49:773-782.
11. de Wit E., de Laat W. A decade of 3C technologies: insights into nuclear organization. Genes Dev. 2012, 26:11-24.
12. Dekker J., et al. Capturing chromosome conformation. Science 2002, 295:1306-1311.
13. Palstra R.J., et al. The beta-globin nuclear compartment in development and erythroid differentiation. Nat. Genet. 2003, 35:190-194.
14. Lettice L.A., et al. A long-range Shh enhancer regulates expression in the developing limb and fin and is associated with preaxial polydactyly. Hum. Mol. Genet. 2003, 12:1725-1735.
15. Sagai T., et al. Elimination of a long-range cis-regulatory module causes complete loss of limb-specific Shh expression and truncation of the mouse limb. Development 2005, 132:797-803.
16. Marinic M., et al. An integrated holo-enhancer unit defines tissue and gene specificity of the Fgf8 regulatory landscape. Dev. Cell 2013, 24:530-542.
17. Montavon T., et al. A regulatory archipelago controls Hox genes transcription in digits. Cell 2011, 147:1132-1145.
18. Sanyal A., et al. The long-range interaction landscape of gene promoters. Nature 2012, 489:109-113.
19. Amano T., et al. Chromosomal dynamics at the Shh locus: limb bud-specific differential regulation of competence and active transcription. Dev. Cell 2009, 16:47-57.
20. Ghavi-Helm Y., et al. Enhancer loops appear stable during development and are associated with paused polymerase. Nature 2014, 512:96-100.
21. Nagano T., et al. Single-cell Hi-C reveals cell-to-cell variability in chromosome structure. Nature 2013, 502:59-64.
22. Giorgetti L., et al. Predictive polymer modeling reveals coupled fluctuations in chromosome conformation and transcription. Cell 2014, 157:950-963.
23. Dixon J.R., et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 2012, 485:376-380.
24. Nora E.P., et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 2012, 485:381-385.
25. Sexton T., et al. Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 2012, 148:458-472.
26. Rao S.S., et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 2014, 159:1665-1680.
27. Shen Y., et al. A map of the cis-regulatory sequences in the mouse genome. Nature 2012, 488:116-120.
28. Le Dily F., et al. Distinct structural transitions of chromatin topological domains correlate with coordinated hormone-induced gene regulation. Genes Dev. 2014, 28:2151-2162.
29. Symmons O., et al. Functional and topological characteristics of mammalian regulatory domains. Genome Res. 2014, 24:390-400.
30. Lupianez D.G., et al. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 2015, 161:1012-1025.
31. Pope B.D., et al. Topologically associating domains are stable units of replication-timing regulation. Nature 2014, 515:402-405.
32. Wijchers P.J., et al. Characterization and dynamics of pericentromere-associated domains in mice. Genome Res. 2015, 25:958-969.
33. Nora E.P., et al. Segmental folding of chromosomes: a basis for structural and regulatory chromosomal neighborhoods?. Bioessays 2013, 35:818-828.
34. Umbarger M.A., et al. The three-dimensional architecture of a bacterial genome and its alteration by genetic perturbation. Mol. Cell 2011, 44:252-264.
35. Duan Z., et al. A three-dimensional model of the yeast genome. Nature 2010, 465:363-367.
36. Feng S., et al. Genome-wide Hi-C analyses in wild-type and mutants reveal high-resolution chromatin interactions in Arabidopsis. Mol. Cell 2014, 55:694-707.
37. Grob S., et al. Hi-C analysis in Arabidopsis identifies the KNOT, a structure with similarities to the flamenco locus of Drosophila. Mol. Cell 2014, 55:678-693.
38. Lonfat N., et al. Convergent evolution of complex regulatory landscapes and pleiotropy at Hox loci. Science 2014, 346:1004-1006.
39. Woltering J.M., et al. Conservation and divergence of regulatory strategies at Hox loci and the origin of tetrapod digits. PLoS Biol. 2014, 12:e1001773.
40. Lonfat N., Duboule D. Structure, function and evolution of topologically associating domains (TADs) at HOX loci. FEBS Lett. 2015, 589:2869-2876.
41. Raab J.R., et al. Human tRNA genes function as chromatin insulators. EMBO J. 2012, 31:330-350.
42. Hou C., et al. Gene density, transcription, and insulators contribute to the partition of the Drosophila genome into physical domains. Mol. Cell 2012, 48:471-484.
43. Van Bortle K., et al. Insulator function and topological domain border strength scale with architectural protein occupancy. Genome Biol. 2014, 15:R82.
44. Hadjur S., et al. Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus. Nature 2009, 460:410-413.
45. Hou C., et al. Cell type specificity of chromatin organization mediated by CTCF and cohesin. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:3651-3656.
46. Kurukuti S., et al. CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:10684-10689.
47. Mishiro T., et al. Architectural roles of multiple chromatin insulators at the human apolipoprotein gene cluster. EMBO J. 2009, 28:1234-1245.
48. Nativio R., et al. Cohesin is required for higher-order chromatin conformation at the imprinted IGF2-H19 locus. PLoS Genet. 2009, 5:e1000739.
49. Splinter E., et al. CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus. Genes Dev. 2006, 20:2349-2354.
50. Zuin J., et al. Cohesin and CTCF differentially affect chromatin architecture and gene expression in human cells. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:996-1001.
51. Rubio E.D., et al. CTCF physically links cohesin to chromatin. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:8309-8314.
52. Phillips-Cremins J.E., et al. Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 2013, 153:1281-1295.
53. Parelho V., et al. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 2008, 132:422-433.
54. Wendt K.S., et al. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 2008, 451:796-801.
55. Seitan V.C., et al. Cohesin-based chromatin interactions enable regulated gene expression within preexisting architectural compartments. Genome Res. 2013, 23:2066-2077.
56. Sofueva S., et al. Cohesin-mediated interactions organize chromosomal domain architecture. EMBO J. 2013, 32:3119-3129.
57. Vietri Rudan M., et al. Comparative Hi-C reveals that CTCF underlies evolution of chromosomal domain architecture. Cell Rep. 2015, 10:1297-1309.
58. Yusufzai T.M., Felsenfeld G. The 5'-HS4 chicken beta-globin insulator is a CTCF-dependent nuclear matrix-associated element. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:8620-8624.
59. Guo Y., et al. CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function. Cell 2015, 162:900-910.
60. Gomez-Marin C., et al. Evolutionary comparison reveals that diverging CTCF sites are signatures of ancestral topological associating domains borders. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:7542-7547.
61. Narendra V., et al. Transcription. CTCF establishes discrete functional chromatin domains at the Hox clusters during differentiation. Science 2015, 347:1017-1021.
62. Tsujimura T., et al. A discrete transition zone organizes the topological and regulatory autonomy of the adjacent tfap2c and bmp7 genes. PLoS Genet. 2015, 11:e1004897.
63. Gilissen C., et al. Genome sequencing identifies major causes of severe intellectual disability. Nature 2014, 511:344-347.
64. Benko S., et al. Disruption of a long distance regulatory region upstream of SOX9 in isolated disorders of sex development. J. Med. Genet. 2011, 48:825-830.
65. Fernandez B.A., et al. Holoprosencephaly and cleidocranial dysplasia in a patient due to two position-effect mutations: case report and review of the literature. Clin. Genet. 2005, 68:349-359.
66. Lauderdale J.D., et al. 3' Deletions cause aniridia by preventing PAX6 gene expression. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:13755-13759.
67. Wagner T., et al. Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9. Cell 1994, 79:1111-1120.
68. Spielmann M., Mundlos S. Structural variations, the regulatory landscape of the genome and their alteration in human disease. Bioessays 2013, 35:533-543.
69. Niedermaier M., et al. An inversion involving the mouse Shh locus results in brachydactyly through dysregulation of Shh expression. J. Clin. Invest. 2005, 115:900-909.
70. Lettice L.A., et al. Enhancer-adoption as a mechanism of human developmental disease. Hum. Mutat. 2011, 32:1492-1499.
71. Spielmann M., et al. Homeotic arm-to-leg transformation associated with genomic rearrangements at the PITX1 locus. Am. J. Hum. Genet. 2012, 91:629-635.
72. Seoighe D.M., et al. A chromosomal 5q31.1 gain involving PITX1 causes Liebenberg syndrome. Am. J. Med. Genet. A 2014, 164A:2958-2960.
73. Ibn-Salem J., et al. Deletions of chromosomal regulatory boundaries are associated with congenital disease. Genome Biol. 2014, 15:423.
74. Ariani F., et al. FOXG1 is responsible for the congenital variant of Rett syndrome. Am. J. Hum. Genet. 2008, 83:89-93.
75. Kortum F., et al. The core FOXG1 syndrome phenotype consists of postnatal microcephaly, severe mental retardation, absent language, dyskinesia, and corpus callosum hypogenesis. J. Med. Genet. 2011, 48:396-406.
76. Allou L., et al. 14q12 and severe Rett-like phenotypes: new clinical insights and physical mapping of FOXG1-regulatory elements. Eur. J. Hum. Genet. 2012, 20:1216-1223.
77. Giorgio E., et al. A large genomic deletion leads to enhancer adoption by the lamin B1 gene: a second path to autosomal dominant adult-onset demyelinating leukodystrophy (ADLD). Hum. Mol. Genet. 2015, 24:3143-3154.
78. Brussino A., et al. A family with autosomal dominant leukodystrophy linked to 5q23.2-q23.3 without lamin B1 mutations. Eur. J. Neurol. 2010, 17:541-549.
79. Flottmann R., et al. Microdeletions on 6p22.3 are associated with mesomelic dysplasia Savarirayan type. J. Med. Genet. 2015, 52:476-483.
80. Groschel S., et al. A single oncogenic enhancer rearrangement causes concomitant EVI1 and GATA2 deregulation in leukemia. Cell 2014, 157:369-381.
81. Northcott P.A., et al. Enhancer hijacking activates GFI1 family oncogenes in medulloblastoma. Nature 2014, 511:428-434.
82. van Arensbergen J., et al. In search of the determinants of enhancer-promoter interaction specificity. Trends Cell Biol. 2014, 24:695-702.
83. Zabidi M.A., et al. Enhancer-core-promoter specificity separates developmental and housekeeping gene regulation. Nature 2014, 518:556-559.
84. Noordermeer D., et al. Variegated gene expression caused by cell-specific long-range DNA interactions. Nat. Cell Biol. 2011, 13:944-951.
85. Tolhuis B., et al. Looping and interaction between hypersensitive sites in the active beta-globin locus. Mol. Cell 2002, 10:1453-1465.
86. Wang H., et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 2013, 153:910-918.
87. Seruggia D., Montoliu L. The new CRISPR-Cas system: RNA-guided genome engineering to efficiently produce any desired genetic alteration in animals. Transgenic Res. 2014, 23:707-716.
88. Kraft K., et al. Deletions, inversions, duplications: engineering of structural variants using CRISPR/Cas in mice. Cell Rep. 2015, 10:833-839.
89. Mali P., et al. Cas9 as a versatile tool for engineering biology. Nat. Methods 2013, 10:957-963.
90. Sternberg S.H., Doudna J.A. Expanding the biologist's toolkit with CRISPR-Cas9. Mol. Cell 2015, 58:568-574.
91. Simonis M., et al. High-resolution identification of balanced and complex chromosomal rearrangements by 4C technology. Nat. Methods 2009, 6:837-842.
92. Selvaraj S., et al. Whole-genome haplotype reconstruction using proximity-ligation and shotgun sequencing. Nat. Biotechnol. 2013, 31:1111-1118.
93. Splinter E., et al. Determining long-range chromatin interactions for selected genomic sites using 4C-seq technology: from fixation to computation. Methods 2012, 58:221-230.
94. Williams R.L., et al. fourSig: a method for determining chromosomal interactions in 4C-seq data. Nucleic Acids Res. 2014, 42:e68.
95. Gheldof N., et al. Structural variation-associated expression changes are paralleled by chromatin architecture modifications. PLoS ONE 2013, 8:e79973.