Transcription Factor Occupancy Can Mediate Active Turnover of DNA Methylation at Regulatory Regions

PLoS Genetics

Volumn 9, Issue 12, 2013, Pages

  Feldmann, Angelika ^a   Ivanek, Robert ^a,b   Murr, Rabih ^a   Gaidatzis, Dimos ^a,b   Burger, Lukas ^a,b   Schübeler, Dirk ^a,c  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CTCF;

ARTICLE; BINDING AFFINITY; BINDING SITE; CELL TYPE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DNA STRUCTURE; LOW METHYLATED REGION; PROTEIN DNA BINDING; PROTEIN MOTIF;

ANIMALS; BINDING SITES; CELL DIFFERENTIATION; CPG ISLANDS; CYTOSINE; DNA METHYLATION; DNA-BINDING PROTEINS; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION; GENOME; MICE; PROMOTER REGIONS, GENETIC; REGULATORY SEQUENCES, NUCLEIC ACID; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84892690160     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003994     Document Type: Article

References (58)

1. Okita K, Ichisaka T, Yamanaka S, (2007) Generation of germline-competent induced pluripotent stem cells. Nature 448: 313-317.
2. Silva J, Barrandon O, Nichols J, Kawaguchi J, Theunissen TW, et al. (2008) Promotion of reprogramming to ground state pluripotency by signal inhibition. PLoS Biol 6: e253.
3. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, et al. (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459: 108-112.
4. Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, et al. (2011) A unique chromatin signature uncovers early developmental enhancers in humans. Nature 470: 279-283.
5. Lupien M, Eeckhoute J, Meyer CA, Wang Q, Zhang Y, et al. (2008) FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription. Cell 132: 958-970.
6. Hodges E, Molaro A, Dos Santos CO, Thekkat P, Song Q, et al. (2011) Directional DNA methylation changes and complex intermediate states accompany lineage specificity in the adult hematopoietic compartment. Mol Cell 44: 17-28.
7. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, et al. (2011) DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480: 490-495.
8. Wiench M, John S, Baek S, Johnson TA, Sung MH, et al. (2011) DNA methylation status predicts cell type-specific enhancer activity. EMBO J 30: 3028-3039.
9. Burger L, Gaidatzis D, Schubeler D, Stadler MB, (2013) Identification of active regulatory regions from DNA methylation data. Nucleic Acids Res.
10. Hon GC, Rajagopal N, Shen Y, McCleary DF, Yue F, et al. (2013) Epigenetic memory at embryonic enhancers identified in DNA methylation maps from adult mouse tissues. Nat Genet.
11. Ziller MJ, Gu H, Muller F, Donaghey J, Tsai LT, et al. (2013) Charting a dynamic DNA methylation landscape of the human genome. Nature 500: 477-481.
12. Bhutani N, Burns DM, Blau HM, (2011) DNA demethylation dynamics. Cell 146: 866-872.
13. He YF, Li BZ, Li Z, Liu P, Wang Y, et al. (2011) Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333: 1303-1307.
14. Inoue A, Zhang Y, (2011) Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science 334: 194.
15. Kriaucionis S, Heintz N, (2009) The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324: 929-930.
16. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, et al. (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324: 930-935.
17. Pastor WA, Pape UJ, Huang Y, Henderson HR, Lister R, et al. (2011) Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature 473: 394-397.
18. Serandour AA, Avner S, Oger F, Bizot M, Percevault F, et al. Dynamic hydroxymethylation of deoxyribonucleic acid marks differentiation-associated enhancers. Nucleic Acids Res 40: 8255-8265.
19. Stroud H, Feng S, Morey Kinney S, Pradhan S, Jacobsen SE, (2011) 5-Hydroxymethylcytosine is associated with enhancers and gene bodies in human embryonic stem cells. Genome Biol 12: R54.
20. Szulwach KE, Li X, Li Y, Song CX, Han JW, et al. (2011) Integrating 5-hydroxymethylcytosine into the epigenomic landscape of human embryonic stem cells. PLoS Genet 7: e1002154.
21. Yu M, Hon GC, Szulwach KE, Song CX, Zhang L, et al. (2012) Base-resolution analysis of 5-hydroxymethylcytosine in the Mammalian genome. Cell 149: 1368-1380.
22. Globisch D, Munzel M, Muller M, Michalakis S, Wagner M, et al. (2010) Tissue distribution of 5-hydroxymethylcytosine and search for active demethylation intermediates. PLoS One 5: e15367.
23. Nestor CE, Ottaviano R, Reddington J, Sproul D, Reinhardt D, et al. Tissue type is a major modifier of the 5-hydroxymethylcytosine content of human genes. Genome Res 22: 467-477.
24. Bell AC, Felsenfeld G, (2000) Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405: 482-485.
25. Xie W, Barr CL, Kim A, Yue F, Lee AY, et al. (2012) Base-resolution analyses of sequence and parent-of-origin dependent DNA methylation in the mouse genome. Cell 148: 816-831.
26. Brinkman AB, Gu H, Bartels SJ, Zhang Y, Matarese F, et al. (2012) Sequential ChIP-bisulfite sequencing enables direct genome-scale investigation of chromatin and DNA methylation cross-talk. Genome Res 22: 1128-1138.
27. Statham AL, Robinson MD, Song JZ, Coolen MW, Stirzaker C, et al. (2012) Bisulfite sequencing of chromatin immunoprecipitated DNA (BisChIP-seq) directly informs methylation status of histone-modified DNA. Genome Res 22: 1120-1127.
28. Rhee HS, Pugh BF, Comprehensive genome-wide protein-DNA interactions detected at single-nucleotide resolution. Cell 147: 1408-1419.
29. Huang Y, Pastor WA, Shen Y, Tahiliani M, Liu DR, et al. (2010) The behaviour of 5-hydroxymethylcytosine in bisulfite sequencing. PLoS One 5: e8888.
30. Jin SG, Kadam S, Pfeifer GP, (2010) Examination of the specificity of DNA methylation profiling techniques towards 5-methylcytosine and 5-hydroxymethylcytosine. Nucleic Acids Res 38: e125.
31. Ficz G, Branco MR, Seisenberger S, Santos F, Krueger F, et al. (2011) Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 473: 398-402.
32. Williams K, Christensen J, Pedersen MT, Johansen JV, Cloos PA, et al. (2011) TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 473: 343-348.
33. Wu H, D'Alessio AC, Ito S, Xia K, Wang Z, et al. (2011) Dual functions of Tet1 in transcriptional regulation in mouse embryonic stem cells. Nature 473: 389-393.
34. Bibel M, Richter J, Lacroix E, Barde YA, (2007) Generation of a defined and uniform population of CNS progenitors and neurons from mouse embryonic stem cells. Nat Protoc 2: 1034-1043.
35. Fedoriw AM, Stein P, Svoboda P, Schultz RM, Bartolomei MS, (2004) Transgenic RNAi reveals essential function for CTCF in H19 gene imprinting. Science 303: 238-240.
36. Heath H, Ribeiro de Almeida C, Sleutels F, Dingjan G, van de Nobelen S, et al. (2008) CTCF regulates cell cycle progression of alphabeta T cells in the thymus. EMBO J 27: 2839-2850.
37. Hirayama T, Tarusawa E, Yoshimura Y, Galjart N, Yagi T, (2012) CTCF is required for neural development and stochastic expression of clustered Pcdh genes in neurons. Cell Rep 2: 345-357.
38. Soshnikova N, Montavon T, Leleu M, Galjart N, Duboule D, (2010) Functional analysis of CTCF during mammalian limb development. Dev Cell 19: 819-830.
39. Schmidt D, Schwalie PC, Wilson MD, Ballester B, Goncalves A, et al. (2012) Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell 148: 335-348.
40. Tan L, Xiong L, Xu W, Wu F, Huang N, et al. Genome-wide comparison of DNA hydroxymethylation in mouse embryonic stem cells and neural progenitor cells by a new comparative hMeDIP-seq method. Nucleic Acids Res.
41. Ding J, Xu H, Faiola F, Ma'ayan A, Wang J, (2012) Oct4 links multiple epigenetic pathways to the pluripotency network. Cell Res 22: 155-167.
42. Serandour AA, Avner S, Percevault F, Demay F, Bizot M, et al. (2011) Epigenetic switch involved in activation of pioneer factor FOXA1-dependent enhancers. Genome Res 21: 555-565.
43. Fu Y, Sinha M, Peterson CL, Weng Z, (2008) The insulator binding protein CTCF positions 20 nucleosomes around its binding sites across the human genome. PLoS Genet 4: e1000138.
44. Frauer C, Hoffmann T, Bultmann S, Casa V, Cardoso MC, et al. Recognition of 5-hydroxymethylcytosine by the Uhrf1 SRA domain. PLoS One 6: e21306.
45. Kubosaki A, Tomaru Y, Furuhata E, Suzuki T, Shin JW, et al. CpG site-specific alteration of hydroxymethylcytosine to methylcytosine beyond DNA replication. Biochem Biophys Res Commun 426: 141-147.
46. Shen L, Wu H, Diep D, Yamaguchi S, D'Alessio AC, et al. (2013) Genome-wide Analysis Reveals TET- and TDG-Dependent 5-methylcytosine Oxidation Dynamics. Cell 153.
47. Song CX, Szulwach KE, Dai Q, Fu Y, Mao SQ, et al. (2013) Genome-wide profiling of 5-Formylcytosine reveals its roles in epigenetic priming. Cell.
48. Valinluck V, Sowers LC, (2007) Endogenous cytosine damage products alter the site selectivity of human DNA maintenance methyltransferase DNMT1. Cancer Res 67: 946-950.
49. Mellen M, Ayata P, Dewell S, Kriaucionis S, Heintz N, MeCP2 binds to 5hmC enriched within active genes and accessible chromatin in the nervous system. Cell 151: 1417-1430.
50. Yildirim O, Li R, Hung JH, Chen PB, Dong X, et al. Mbd3/NURD complex regulates expression of 5-hydroxymethylcytosine marked genes in embryonic stem cells. Cell 147: 1498-1510.
51. Baubec T, Ivanek R, Lienert F, Schubeler D, Methylation-Dependent and-Independent Genomic Targeting Principles of the MBD Protein Family. Cell 153: 480-492.
52. Spruijt CG, Gnerlich F, Smits AH, Pfaffeneder T, Jansen PW, et al. Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell 152: 1146-1159.
53. Jones PA, (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13: 484-492.
54. Schubeler D, Molecular biology. Epigenetic islands in a genetic ocean. Science 338: 756-757.
55. Deaton AM, Bird A, (2011) CpG islands and the regulation of transcription. Genes Dev 25: 1010-1022.
56. Mohn F, Weber M, Schubeler D, Roloff TC, (2009) Methylated DNA immunoprecipitation (MeDIP). Methods Mol Biol 507: 55-64.
57. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
58. Arnold P, Scholer A, Pachkov M, Balwierz PJ, Jorgensen H, et al. Modeling of epigenome dynamics identifies transcription factors that mediate Polycomb targeting. Genome Res 23: 60-73.