An atlas of dynamic chromatin landscapes in mouse fetal development.
Animals
Chromatin
/ chemistry
Chromatin Immunoprecipitation Sequencing
Datasets as Topic
Disease
/ genetics
Enhancer Elements, Genetic
/ genetics
Female
Fetal Development
/ genetics
Gene Expression Regulation, Developmental
/ genetics
Genetic Variation
Histones
/ chemistry
Humans
Male
Mice
Mice, Inbred C57BL
Molecular Sequence Annotation
Organ Specificity
/ genetics
Regulatory Sequences, Nucleic Acid
/ genetics
Reproducibility of Results
Transposases
/ metabolism
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
07 2020
07 2020
Historique:
received:
08
08
2017
accepted:
11
06
2019
entrez:
31
7
2020
pubmed:
31
7
2020
medline:
12
1
2021
Statut:
ppublish
Résumé
The Encyclopedia of DNA Elements (ENCODE) project has established a genomic resource for mammalian development, profiling a diverse panel of mouse tissues at 8 developmental stages from 10.5 days after conception until birth, including transcriptomes, methylomes and chromatin states. Here we systematically examined the state and accessibility of chromatin in the developing mouse fetus. In total we performed 1,128 chromatin immunoprecipitation with sequencing (ChIP-seq) assays for histone modifications and 132 assay for transposase-accessible chromatin using sequencing (ATAC-seq) assays for chromatin accessibility across 72 distinct tissue-stages. We used integrative analysis to develop a unified set of chromatin state annotations, infer the identities of dynamic enhancers and key transcriptional regulators, and characterize the relationship between chromatin state and accessibility during developmental gene regulation. We also leveraged these data to link enhancers to putative target genes and demonstrate tissue-specific enrichments of sequence variants associated with disease in humans. The mouse ENCODE data sets provide a compendium of resources for biomedical researchers and achieve, to our knowledge, the most comprehensive view of chromatin dynamics during mammalian fetal development to date.
Identifiants
pubmed: 32728240
doi: 10.1038/s41586-020-2093-3
pii: 10.1038/s41586-020-2093-3
pmc: PMC7398618
mid: NIHMS1531728
doi:
Substances chimiques
Chromatin
0
Histones
0
Transposases
EC 2.7.7.-
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
744-751Subventions
Organisme : NHGRI NIH HHS
ID : U24 HG009397
Pays : United States
Organisme : Howard Hughes Medical Institute
Pays : United States
Organisme : NHGRI NIH HHS
ID : U54 HG006997
Pays : United States
Organisme : NHGRI NIH HHS
ID : UM1 HG009421
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA014195
Pays : United States
Commentaires et corrections
Type : ErratumIn
Type : ErratumIn
Références
Allis, C. D. & Jenuwein, T. The molecular hallmarks of epigenetic control. Nat. Rev. Genet. 17, 487–500 (2016).
pubmed: 27346641
Tessarz, P. & Kouzarides, T. Histone core modifications regulating nucleosome structure and dynamics. Nat. Rev. Mol. Cell Biol. 15, 703–708 (2014).
pubmed: 25315270
Shlyueva, D., Stampfel, G. & Stark, A. Transcriptional enhancers: from properties to genome-wide predictions. Nat. Rev. Genet. 15, 272–286 (2014).
Visel, A., Rubin, E. M. & Pennacchio, L. A. Genomic views of distant-acting enhancers. Nature 461, 199–205 (2009).
pubmed: 2923221
pmcid: 2923221
Shen, Y. et al. A map of the cis-regulatory sequences in the mouse genome. Nature 488, 116–120 (2012).
pubmed: 22763441
pmcid: 4041622
Ernst, J. et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473, 43–49 (2011).
pubmed: 21441907
pmcid: 3088773
He, Y. et al. Spatiotemporal DNA methylome dynamics of the developing mammalian fetus. Nature https://doi.org/10.1038/s41586-020-2119-x (2020).
Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y. & Greenleaf, W. J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213–1218 (2013).
pubmed: 3959825
pmcid: 3959825
Thurman, R. E. et al. The accessible chromatin landscape of the human genome. Nature 489, 75–82 (2012).
pubmed: 22955617
pmcid: 3721348
Yue, F. et al. A comparative encyclopedia of DNA elements in the mouse genome. Nature 515, 355–364 (2014).
pubmed: 4266106
pmcid: 4266106
Wu, J. et al. The landscape of accessible chromatin in mammalian preimplantation embryos. Nature 534, 652–657 (2016).
pubmed: 27309802
Zhang, B. et al. Allelic reprogramming of the histone modification H3K4me3 in early mammalian development. Nature 537, 553–557 (2016).
pubmed: 27626382
Kundaje, A. et al. Integrative analysis of 111 reference human epigenomes. Nature 518, 317–330 (2015).
pubmed: 25693563
pmcid: 4530010
IHEC. Reference epigenome standards. http://ihec-epigenomes.org/research/reference-epigenome-standards/ (2017).
Dahl, J. A. et al. Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition. Nature 537, 548–552 (2016).
doi: 10.1038/nature19360
pubmed: 27626377
pmcid: 6283663
Ernst, J. & Kellis, M. ChromHMM: automating chromatin-state discovery and characterization. Nat. Methods 9, 215–216 (2012).
pubmed: 22373907
pmcid: 3577932
Barski, A. et al. High-resolution profiling of histone methylations in the human genome. Cell 129, 823–837 (2007).
pubmed: 17512414
Lynch, M. & Conery, J. S. The origins of genome complexity. Science 302, 1401–1404 (2003).
pubmed: 14631042
McCulley, D. J. & Black, B. L. Transcription factor pathways and congenital heart disease. Curr. Top. Dev. Biol. 100, 253–277 (2012).
pubmed: 22449847
pmcid: 3684448
Costa, R. H., Kalinichenko, V. V. & Lim, L. Transcription factors in mouse lung development and function. Am. J. Physiol. Lung Cell. Mol. Physiol. 280, L823–L838 (2001).
pubmed: 11290504
Sheaffer, K. L. & Kaestner, K. H. Transcriptional networks in liver and intestinal development. Cold Spring Harb. Perspect. Biol. 4, a008284 (2012).
pubmed: 22952394
pmcid: 3428765
Jayewickreme, C. D. & Shivdasani, R. A. Control of stomach smooth muscle development and intestinal rotation by TF BARX1. Dev. Biol. 405, 21–32 (2015).
pubmed: 26057579
pmcid: 4529797
Dressler, G. R. Transcription factors in renal development: the WT1 and Pax-2 story. Semin. Nephrol. 15, 263–271 (1995).
pubmed: 7569406
Saksouk, N., Simboeck, E. & Déjardin, J. Constitutive heterochromatin formation and transcription in mammals. Epigenetics Chromatin 8, 3 (2015).
pubmed: 25788984
pmcid: 4363358
Bulut-Karslioglu, A. et al. Suv39h-dependent H3K9me3 marks intact retrotransposons and silences LINE elements in mouse embryonic stem cells. Mol. Cell 55, 277–290 (2014).
pubmed: 24981170
Zhu, J. et al. Genome-wide chromatin state transitions associated with developmental and environmental cues. Cell 152, 642–654 (2013).
pubmed: 23333102
pmcid: 3563935
Lehnertz, B. et al. Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin. Curr. Biol. 13, 1192–1200 (2003).
pubmed: 12867029
Blahnik, K. R. et al. Characterization of the contradictory chromatin signatures at the 3′ exons of zinc finger genes. PLoS ONE 6, e17121 (2011).
pubmed: 21347206
pmcid: 3039671
Mikkelsen, T. S. et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448, 553–560 (2007).
pubmed: 17603471
pmcid: 2921165
Ku, M. et al. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet. 4, e1000242 (2008).
pubmed: 18974828
pmcid: 2567431
Ferrai, C. et al. RNA polymerase II primes Polycomb-repressed developmental genes throughout terminal neuronal differentiation. Mol. Syst. Biol. 13, 946 (2017).
pubmed: 29038337
pmcid: 5658700
Brookes, E. et al. Polycomb associates genome-wide with a specific RNA polymerase II variant, and regulates metabolic genes in ESCs. Cell Stem Cell 10, 157–170 (2012).
pubmed: 22305566
pmcid: 3682187
Cusanovich, D. A. et al. A single-cell atlas of in vivo mammalian chromatin accessibility. Cell 174, 1309–1324.e18 (2018).
pubmed: 30078704
pmcid: 6158300
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).
Dixon, J. R., Gorkin, D. U. & Ren, B. Chromatin domains: the unit of chromosome organization. Mol. Cell 62, 668–680 (2016).
pubmed: 27259200
pmcid: 5371509
Maurano, M. T. et al. Systematic localization of common disease-associated variation in regulatory DNA. Science 337, 1190–1195 (2012).
pubmed: 3771521
pmcid: 3771521
Hindorff, L. A. et al. Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc. Natl Acad. Sci. USA 106, 9362–9367 (2009).
pubmed: 19474294
pmcid: 2687147
Preissl, S. et al. Single-nucleus analysis of accessible chromatin in developing mouse forebrain reveals cell-type-specific transcriptional regulation. Nat. Neurosci. 21, 432–439 (2018).
pubmed: 29434377
pmcid: 5862073
Nord, A. S. et al. Rapid and pervasive changes in genome-wide enhancer usage during mammalian development. Cell 155, 1521–1531 (2013).
pubmed: 24360275
pmcid: 3989111
Hnisz, D. et al. Super-enhancers in the control of cell identity and disease. Cell 155, 934–947 (2013).
pubmed: 24119843
pmcid: 24119843
Avilion, A. A. et al. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 17, 126–140 (2003).
pubmed: 12514105
pmcid: 195970
Shimozaki, K. Sox2 transcription network acts as a molecular switch to regulate properties of neural stem cells. World J. Stem Cells 6, 485–490 (2014).
pubmed: 25258670
pmcid: 4172677
Uittenbogaard, M., Baxter, K. K. & Chiaramello, A. NeuroD6 genomic signature bridging neuronal differentiation to survival via the molecular chaperone network. J. Neurosci. Res. 88, 33–54 (2010).
pubmed: 19610105
pmcid: 2784025
Barbosa, A. C. et al. MEF2C, a TF that facilitates learning and memory by negative regulation of synapse numbers and function. Proc. Natl Acad. Sci. 105, 9391–9396 (2008).
pubmed: 18599438
pmcid: 2453723
Dixon, J. R. et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376–380 (2012).
pubmed: 22495300
pmcid: 22495300
Lupiáñez, D. G. et al. Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161, 1012–1025 (2015).
pubmed: 25959774
pmcid: 4791538
Franke, M. et al. Formation of new chromatin domains determines pathogenicity of genomic duplications. Nature 538, 265–269 (2016).
pubmed: 27706140
Andrey, G. et al. Characterization of hundreds of regulatory landscapes in developing limbs reveals two regimes of chromatin folding. Genome Res. 27, 223–233 (2017).
pubmed: 27923844
pmcid: 5287228
DeMare, L. E. et al. The genomic landscape of cohesin-associated chromatin interactions. Genome Res. 23, 1224–1234 (2013).
pubmed: 23704192
pmcid: 3730097
Schoenfelder, S. et al. The pluripotent regulatory circuitry connecting promoters to their long-range interacting elements. Genome Res. 25, 582–597 (2015).
pubmed: 25752748
pmcid: 4381529
GTEx Consortium. The genotype-tissue expression (GTEx) project. Nat. Genet. 45, 580–585 (2013).
Kothary, R. et al. Inducible expression of an hsp68-lacZ hybrid gene in transgenic mice. Development 105, 707–714 (1989).
pubmed: 2557196
The Encode Project Consortium et al. Expanded encyclopedias of DNA elements in the human and mouse genomes. Nature https://doi.org/10.1038/s41586-020-2493-4 (2020).
He, Y. et al. Improved regulatory element prediction based on tissue-specific local epigenomic signatures. Proc. Natl Acad. Sci. USA 114, E1633–E1640 (2017).
pubmed: 28193886
pmcid: 5338528
Sethi, A. et al. Supervised enhancer prediction with epigenetic pattern recognition and targeted validation. Nat. Methods https://doi.org/10.1038/s41592-020-0907-8 (2020).
Sisu, C. et al. Transcriptional activity and strain-specific history of mouse pseudogenes. Nat. Commun. https://doi.org/10.1038/s41467-020-17157-w (2020).
Zhang, K., Wang, M., Zhao, Y. & Wang, W. Taiji: system-level identification of key transcription factors reveals transcriptional waves in mouse embryonic development. Science Adv. 5, eaav32622019 (2019).
Ngo, V. et al. Epigenomic analysis reveals DNA motifs regulating histone modifications in human and mouse. Proc. Natl Acad. Sci. USA 116, 3668–3677 (2019).
pubmed: 30755522
pmcid: 6397554
Wang, Y. et al. Pulmonary alveolar type I cell population consists of two distinct subtypes that differ in cell fate. Proc. Natl Acad. Sci. USA 115, 2407–2412 (2018).
pubmed: 29463737
pmcid: 5877944
Pers, T. H., Timshel, P. & Hirschhorn, J. N. SNPsnap: a web-based tool for identification and annotation of matched SNPs. Bioinformatics 31, 418–420 (2015).
pubmed: 25316677
Li, Y. I. et al. RNA splicing is a primary link between genetic variation and disease. Science 352, 600–604 (2016).
pubmed: 27126046
pmcid: 5182069
Sloan, C. A. et al. ENCODE data at the ENCODE portal. Nucleic Acids Res. 44, D726–D732 (2016).
pubmed: 26527727
Marinov, G. K., Kundaje, A., Park, P. J. & Wold, B. J. Large-scale quality analysis of published ChIP–seq data. G3 (Bethesda) 4, 209–223 (2014).
Ramírez, F., Dündar, F., Diehl, S., Grüning, B. A. & Manke, T. deepTools: a flexible platform for exploring deep-sequencing data. Nucleic Acids Res. 42, W187–W191 (2014).
pubmed: 24799436
pmcid: 4086134
Auton, A. et al. A global reference for human genetic variation. Nature 526, 68–74 (2015).
pubmed: 26432245
pmcid: 26432245
Purcell, S. et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575 (2007).
pubmed: 1950838
pmcid: 1950838
Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).
pubmed: 20110278
pmcid: 20110278
McLean, C. Y. et al. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28, 495–501 (2010).
pubmed: 20436461
pmcid: 4840234
Harrow, J. et al. GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res. 22, 1760–1774 (2012).
pubmed: 22955987
pmcid: 3431492
Online Mendelian Inheritance in Man https://www.omim.org/ (2017).
Wingender, E., Schoeps, T. & Dönitz, J. TFClass: an expandable hierarchical classification of human TFs. Nucleic Acids Res. 41, D165–D170 (2013).
pubmed: 23180794
Wilson, D., Charoensawan, V., Kummerfeld, S. K. & Teichmann, S. A. DBD–taxonomically broad TF predictions: new content and functionality. Nucleic Acids Res. 36, D88–D92 (2008).
pubmed: 18073188
The Gene Ontology Consortium. Gene ontology: tool for the unification of biology. Nat. Genet. 25, 25–29 (2000).
pmcid: 3037419
Ritchie, M. E. et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015).
pubmed: 4402510
pmcid: 4402510
Bailey, T. L. et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37, W202–W208 (2009).
pubmed: 2703892
pmcid: 2703892
Whyte, W. A. et al. Master TFs and mediator establish super-enhancers at key cell identity genes. Cell 153, 307–319 (2013).
pubmed: 23582322
pmcid: 23582322
Lovén, J. et al. Selective inhibition of tumor oncogenes by disruption of super-enhancers. Cell 153, 320–334 (2013).
pubmed: 23582323
pmcid: 3760967
Cotney, J. et al. Chromatin state signatures associated with tissue-specific gene expression and enhancer activity in the embryonic limb. Genome Res. 22, 1069–1080 (2012).
pubmed: 22421546
pmcid: 3371702
Smedley, D. et al. The BioMart community portal: an innovative alternative to large, centralized data repositories. Nucleic Acids Res. 43, W589–W598 (2015).
pubmed: 25897122
pmcid: 4489294
GTEx Consortium. The Genotype-Tissue Expression (GTEx) pilot analysis: multitissue gene regulation in humans. Science 348, 648–660 (2015).
pmcid: 4547484
Fishilevich, S. et al. GeneHancer: genome-wide integration of enhancers and target genes in GeneCards. Database (Oxford) 2017, (2017).
Cao, Q. et al. Reconstruction of enhancer-target networks in 935 samples of human primary cells, tissues and cell lines. Nat. Genet. 49, 1428–1436 (2017).
pubmed: 28869592
Roy, S. et al. A predictive modeling approach for cell line-specific long-range regulatory interactions. Nucleic Acids Res. 43, 8694–8712 (2015).
pubmed: 26338778
pmcid: 4605315
Pennacchio, L. A. et al. In vivo enhancer analysis of human conserved non-coding sequences. Nature 444, 499–502 (2006).
Hinrichs, A. S. et al. The UCSC Genome Browser Database: update 2006. Nucleic Acids Res. 34, D590–D598 (2006).
pubmed: 16381938
Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
pubmed: 19261174
pmcid: 2690996
Day, D. S., Luquette, L. J., Park, P. J. & Kharchenko, P. V. Estimating enrichment of repetitive elements from high-throughput sequence data. Genome Biol. 11, R69 (2010).
pubmed: 20584328
pmcid: 2911117
Criscione, S. W., Zhang, Y., Thompson, W., Sedivy, J. M. & Neretti, N. Transcriptional landscape of repetitive elements in normal and cancer human cells. BMC Genomics 15, 583 (2014).
pubmed: 25012247
pmcid: 4122776
Paudyal, A. et al. The novel mouse mutant, chuzhoi, has disruption of Ptk7 protein and exhibits defects in neural tube, heart and lung development and abnormal planar cell polarity in the ear. BMC Dev. Biol. 10, 87 (2010).
pubmed: 20704721
pmcid: 2930600
Landt, S. G. et al. ChIP–seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res. 22, 1813–1831 (2012).
pubmed: 22955991
pmcid: 3431496
England, J. & Loughna, S. Heavy and light roles: myosin in the morphogenesis of the heart. Cell. Mol. Life Sci. 70, 1221–1239 (2013).
pubmed: 22955375
Kaucka, M. et al. Analysis of neural crest-derived clones reveals novel aspects of facial development. Sci. Adv. 2, e1600060 (2016).
pubmed: 27493992
pmcid: 4972470
Gillis, J. A. & Hall, B. K. A shared role for sonic hedgehog signalling in patterning chondrichthyan gill arch appendages and tetrapod limbs. Development 143, 1313–1317 (2016).
pubmed: 27095494
Voigt, P., Tee, W. W. & Reinberg, D. A double take on bivalent promoters. Genes Dev. 27, 1318–1338 (2013).
pubmed: 23788621
pmcid: 3701188
Aranda, S., Mas, G. & Di Croce, L. Regulation of gene transcription by Polycomb proteins. Sci. Adv. 1, e1500737 (2015).
pubmed: 26665172
pmcid: 4672759
Lettice, L. A. et al. Disruption of a long-range cis-acting regulator for Shh causes preaxial polydactyly. Proc. Natl Acad. Sci. USA 99, 7548–7553 (2002).
pubmed: 12032320
pmcid: 124279
Canver, M. C. et al. BCL11A enhancer dissection by Cas9-mediated in situ saturating mutagenesis. Nature 527, 192–197 (2015).
pubmed: 4644101
pmcid: 4644101
He, P. et al. The changing mouse embryo transcriptome at whole tissue and single-cell resolution. Nature 583, 760–767 (2020).
pubmed: 32728245
pmcid: 7410830