DNA methylation signatures follow preformed chromatin compartments in cardiac myocytes

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Nothjunge, Stephan ^a,b   Nührenberg, Thomas G ^a,c   Grüning, Björn A ^b   Doppler, Stefanie A ^d   Preissl, Sebastian ^a,f   Schwaderer, Martin ^a,b   Rommel, Carolin ^a,b   Krane, Markus ^d,e   Hein, Lutz ^a,b   Gilsbach, Ralf ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY HEART CENTER FREIBURG BAD KROZINGEN   (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^f LUDWIG INSTITUTE FOR CANCER RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS AND CELL COMPONENTS; CHEMICAL REACTION; DIFFERENTIATION; DNA; GENETIC ANALYSIS; GENOME; MATURATION; METHYLATION; PIGMENT; REDUCTION;

CARDIAC MUSCLE CELL; CHROMATIN ASSEMBLY AND DISASSEMBLY; DIFFERENTIATION; DNA METHYLATION; EMBRYONIC STEM CELL; EPIGENETICS; GENOME; HUMAN; HUMAN CELL; MATURATION; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CELL LINE; CHROMATIN; CPG ISLAND; CYTOLOGY; DEFICIENCY; GENETICS; HISTONE CODE; KNOCKOUT MOUSE; METABOLISM; TRANSGENIC MOUSE;

DNA (CYTOSINE 5) METHYLTRANSFERASE;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; CHROMATIN; CPG ISLANDS; DNA (CYTOSINE-5-)-METHYLTRANSFERASES; DNA METHYLATION; EMBRYONIC STEM CELLS; EPIGENOMICS; HISTONE CODE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MYOCYTES, CARDIAC;

EID: 85034759607     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-01724-9     Document Type: Article

References (49)

1. Lieberman-Aiden, E. et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289-293 (2009).
2. Nora, E. P. et al. Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485, 381-385 (2012).
3. Dixon, J. R. et al. Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376-380 (2012).
4. Haarhuis, J. H. I. et al. The cohesin release factor WAPL restricts chromatin loop extension. Cell 169, 693-707.e614 (2017).
5. Dixon, J. R., Gorkin, D. U. & Ren, B. Chromatin domains: the unit of chromosome organization. Mol. Cell 62, 668-680 (2016).
6. Wang, S. et al. Spatial organization of chromatin domains and compartments in single chromosomes. Science 353, 598-602 (2016).
7. 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).
8. Liu, X. S. et al. Editing DNA methylation in the mammalian genome. Cell 167, 233-247 e217 (2016).
9. Fortin, J. P. & Hansen, K. D. Reconstructing A/B compartments as revealed by Hi-C using long-range correlations in epigenetic data. Genome Biol. 16, 180 (2015).
10. Keown, C. L. et al. Allele-specific non-CG DNA methylation marks domains of active chromatin in female mouse brain. Proc. Natl Acad. Sci. USA 114, E2882-E2890 (2017).
11. Berman, B. P. et al. Regions of focal DNA hypermethylation and long-range hypomethylation in colorectal cancer coincide with nuclear lamina-associated domains. Nat. Genet. 44, 40-46 (2011).
12. Ke, Y. et al. 3D chromatin structures of mature gametes and structural reprogramming during mammalian embryogenesis. Cell 170, 367-381 e320 (2017).
13. Smith, Z. D. & Meissner, A. DNA methylation: roles in mammalian development. Nat. Rev. Genet. 14, 204-220 (2013).
14. Stadler, M. B. et al. DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480, 490-495 (2011).
15. Domcke, S. et al. Competition between DNA methylation and transcription factors determines binding of NRF1. Nature 528, 575-579 (2015).
16. Tsumura, A. et al. Maintenance of self-renewal ability of mouse embryonic stem cells in the absence of DNA methyltransferases Dnmt1, Dnmt3a and Dnmt3b. Genes Cells 11, 805-814 (2006).
17. Nührenberg, T. G. et al. Cardiac myocyte de novo DNA methyltransferases 3a/3b are dispensable for cardiac function and remodeling after chronic pressure overload in mice. PLoS ONE 10, e0131019 (2015).
18. Gilsbach, R. et al. Dynamic DNA methylation orchestrates cardiomyocyte development, maturation and disease. Nat. Commun. 5, 5288 (2014).
19. Preissl, S. et al. Deciphering the epigenetic code of cardiac myocyte transcription. Circ. Res. 117, 413-423 (2015).
20. Bergmann, O. et al. Identification of cardiomyocyte nuclei and assessment of ploidy for the analysis of cell turnover. Exp. Cell Res. 317, 188-194 (2011).
21. Gaidatzis, D. et al. DNA sequence explains seemingly disordered methylation levels in partially methylated domains of Mammalian genomes. PLoS Genet. 10, e1004143 (2014).
22. Wu, S. M. et al. Developmental origin of a bipotential myocardial and smooth muscle cell precursor in the mammalian heart. Cell 127, 1137-1150 (2006).
23. Ernst, J. & Kellis, M. ChromHMM: automating chromatin-state discovery and characterization. Nat. Methods 9, 215-216 (2012).
24. Lei, H. et al. De novo DNA cytosine methyltransferase activities in mouse embryonic stem cells. Development 122, 3195-3205 (1996).
25. Liao, J. et al. Targeted disruption of DNMT1, DNMT3A and DNMT3B in human embryonic stem cells. Nat. Genet. 47, 469-478 (2015).
26. Guo, J. U. et al. Distribution, recognition and regulation of non-CpG methylation in the adult mammalian brain. Nat. Neurosci. 17, 215-222 (2014).
27. Lister, R. et al. Global epigenomic reconfiguration during mammalian brain development. Science 341, 1237905 (2013).
28. Baubec, T. et al. Genomic profiling of DNA methyltransferases reveals a role for DNMT3B in genic methylation. Nature 520, 243-247 (2015).
29. Wang, H. et al. Widespread plasticity in CTCF occupancy linked to DNA methylation. Genome Res. 22, 1680-1688 (2012).
30. Burger, L., Gaidatzis, D., Schübeler, D. & Stadler, M. B. Identification of active regulatory regions from DNA methylation data. Nucleic Acids Res. 41, e155 (2013).
31. Lister, R. et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462, 315-322 (2009).
32. Lister, R. et al. Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 471, 68-73 (2011).
33. Tahiliani, M. et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930-935 (2009).
34. 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, E6456-6465 (2015).
35. Fudenberg, G. et al. Formation of chromosomal domains by loop extrusion. Cell Rep. 15, 2038-2049 (2016).
36. Nora, E. P. et al. Targeted degradation of CTCF decouples local insulation of chromosome domains from genomic compartmentalization. Cell 169, 930-944 e922 (2017).
37. Hassan-Zadeh, V., Rugg-Gunn, P. & Bazett-Jones, D. P. DNA methylation is dispensable for changes in global chromatin architecture but required for chromocentre formation in early stem cell differentiation. Chromosoma 126, 605-614 (2017).
38. Feldmann, A. et al. Transcription factor occupancy can mediate active turnover of DNA methylation at regulatory regions. PLoS Genet. 9, e1003994 (2013).
39. Doppler, S. A. et al. Myeloid zinc finger 1 (Mzf1) differentially modulates murine cardiogenesis by interacting with an Nkx2.5 cardiac enhancer. PLoS ONE 9, e113775 (2014).
40. Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576-589 (2010).
41. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359 (2012).
42. Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
43. Ramirez, F. et al. High-resolution TADs reveal DNA sequences underlying genome organization in flies. Preprint at bioRxiv https://doi.org/10.1101/115063 (2017).
44. Ramirez, F., Dundar, F., Diehl, S., Gruning, B. A. & Manke, T. deepTools: a flexible platform for exploring deep-sequencing data. Nucleic Acids Res. 42, W187-191 (2014).
45. Bindea, G. et al. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 25, 1091-1093 (2009).
46. Kranzhöfer, D. K. et al. 5′-Hydroxymethylcytosine precedes loss of CpG methylation in enhancers and genes undergoing activation in cardiomyocyte maturation. PLoS ONE 11, e0166575 (2016).
47. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
48. Krueger, F. & Andrews, S. R. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 27, 1571-1572 (2011).
49. Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15-21 (2013).