MeCP2 binds to 5hmC enriched within active genes and accessible chromatin in the nervous system

Cell

Volumn 151, Issue 7, 2012, Pages 1417-1430

  Mellén, Marian ^a   Ayata, Pinar ^a   Dewell, Scott ^a   Kriaucionis, Skirmantas ^b   Heintz, Nathaniel ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; 5 METHYLCYTOSINE; DNA; METHYL CPG BINDING PROTEIN 2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CELL TYPE; CENTRAL NERVOUS SYSTEM; CHROMATIN; CHROMATIN STRUCTURE; CONTROLLED STUDY; EPIGENETICS; EUCHROMATIN; GENE EXPRESSION PROFILING; GENE MUTATION; GENETIC ANALYSIS; HETEROCHROMATIN; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; QUANTITATIVE ANALYSIS; RETT SYNDROME;

EID: 84871563384     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.11.022     Document Type: Article

References (58)

1. N.L. Adkins, and P.T. Georgel MeCP2: structure and function Biochem. Cell Biol. 89 2011 1 11
2. R.E. Amir, I.B. Van den Veyver, M. Wan, C.Q. Tran, U. Francke, and H.Y. Zoghbi Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2 Nat. Genet. 23 1999 185 188
3. S. Anders, and W. Huber Differential expression analysis for sequence count data Genome Biol. 11 2010 R106
4. A. Bebbington, A. Anderson, D. Ravine, S. Fyfe, M. Pineda, N. de Klerk, B. Ben-Zeev, N. Yatawara, A. Percy, W.E. Kaufmann, and H. Leonard Investigating genotype-phenotype relationships in Rett syndrome using an international data set Neurology 70 2008 868 875
5. S. Ben-Shachar, M. Chahrour, C. Thaller, C.A. Shaw, and H.Y. Zoghbi Mouse models of MeCP2 disorders share gene expression changes in the cerebellum and hypothalamus Hum. Mol. Genet. 18 2009 2431 2442
6. M. Bostick, J.K. Kim, P.O. Estève, A. Clark, S. Pradhan, and S.E. Jacobsen UHRF1 plays a role in maintaining DNA methylation in mammalian cells Science 317 2007 1760 1764
7. M.J. Booth, M.R. Branco, G. Ficz, D. Oxley, F. Krueger, W. Reik, and S. Balasubramanian Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution Science 336 2012 934 937
8. F.J. Campoy, R.R. Meehan, S. McKay, J. Nixon, and A. Bird Binding of histone H1 to DNA is indifferent to methylation at CpG sequences J. Biol. Chem. 270 1995 26473 26481
9. M. Chahrour, and H.Y. Zoghbi The story of Rett syndrome: from clinic to neurobiology Neuron 56 2007 422 437
10. M. Chahrour, S.Y. Jung, C. Shaw, X. Zhou, S.T. Wong, J. Qin, and H.Y. Zoghbi MeCP2, a key contributor to neurological disease, activates and represses transcription Science 320 2008 1224 1229
11. S.P. Chandler, D. Guschin, N. Landsberger, and A.P. Wolffe The methyl-CpG binding transcriptional repressor MeCP2 stably associates with nucleosomal DNA Biochemistry 38 1999 7008 7018
12. W.G. Chen, Q. Chang, Y. Lin, A. Meissner, A.E. West, E.C. Griffith, R. Jaenisch, and M.E. Greenberg Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2 Science 302 2003 885 889
13. S. Cohen, H.W. Gabel, M. Hemberg, A.N. Hutchinson, L.A. Sadacca, D.H. Ebert, D.A. Harmin, R.S. Greenberg, V.K. Verdine, and Z. Zhou Genome-wide activity-dependent MeCP2 phosphorylation regulates nervous system development and function Neuron 72 2011 72 85
14. S. Cortellino, J. Xu, M. Sannai, R. Moore, E. Caretti, A. Cigliano, M. Le Coz, K. Devarajan, A. Wessels, and D. Soprano Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair Cell 146 2011 67 79
15. N.C. Derecki, J.C. Cronk, Z. Lu, E. Xu, S.B. Abbott, P.G. Guyenet, and J. Kipnis Wild-type microglia arrest pathology in a mouse model of Rett syndrome Nature 484 2012 105 109
16. J.P. Doyle, J.D. Dougherty, M. Heiman, E.F. Schmidt, T.R. Stevens, G. Ma, S. Bupp, P. Shrestha, R.D. Shah, and M.L. Doughty Application of a translational profiling approach for the comparative analysis of CNS cell types Cell 135 2008 749 762
17. R.C. Gentleman, V.J. Carey, D.M. Bates, B. Bolstad, M. Dettling, S. Dudoit, B. Ellis, L. Gautier, Y. Ge, and J. Gentry Bioconductor: open software development for computational biology and bioinformatics Genome Biol. 5 2004 R80
18. R.P. Ghosh, R.A. Horowitz-Scherer, T. Nikitina, L.S. Shlyakhtenko, and C.L. Woodcock MeCP2 binds cooperatively to its substrate and competes with histone H1 for chromatin binding sites Mol. Cell. Biol. 30 2010 4656 4670
19. M.L. Gonzales, S. Adams, K.W. Dunaway, and J.M. LaSalle Phosphorylation of distinct sites in MeCP2 modifies cofactor associations and the dynamics of transcriptional regulation Mol. Cell. Biol. 32 2012 2894 2903
20. J. Guy, B. Hendrich, M. Holmes, J.E. Martin, and A. Bird A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome Nat. Genet. 27 2001 322 326
21. J. Guy, H. Cheval, J. Selfridge, and A. Bird The role of MeCP2 in the brain Annu. Rev. Cell Dev. Biol. 27 2011 631 652
22. M. Heiman, A. Schaefer, S. Gong, J.D. Peterson, M. Day, K.E. Ramsey, M. Suárez-Fariñas, C. Schwarz, D.A. Stephan, and D.J. Surmeier A translational profiling approach for the molecular characterization of CNS cell types Cell 135 2008 738 748
23. S. Ito, L. Shen, Q. Dai, S.C. Wu, L.B. Collins, J.A. Swenberg, C. He, and Y. Zhang Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine Science 333 2011 1300 1303
24. S.-G. Jin, S. Kadam, and G.P. Pfeifer Examination of the specificity of DNA methylation profiling techniques towards 5-methylcytosine and 5-hydroxymethylcytosine Nucleic Acids Res. 38 2010 e125
25. M.A. Karymov, M. Tomschik, S.H. Leuba, P. Caiafa, and J. Zlatanova DNA methylation-dependent chromatin fiber compaction in vivo and in vitro: requirement for linker histone FASEB J. 15 2001 2631 2641
26. R.J. Klose, and A.P. Bird MeCP2 behaves as an elongated monomer that does not stably associate with the Sin3a chromatin remodeling complex J. Biol. Chem. 279 2004 46490 46496
27. S. Kriaucionis, and N. Heintz The nuclear DNA base 5- hydroxymethylcytosine is present in Purkinje neurons and the brain Science 324 2009 929 930
28. S. Kudo, Y. Nomura, M. Segawa, N. Fujita, M. Nakao, C. Schanen, and M. Tamura Heterogeneity in residual function of MeCP2 carrying missense mutations in the methyl CpG binding domain J. Med. Genet. 40 2003 487 493
29. W. Lange Cell number and cell density in the cerebellar cortex of man and some other mammals Cell Tissue Res. 157 1975 115 124
30. D.T. Lioy, S.K. Garg, C.E. Monaghan, J. Raber, K.D. Foust, B.K. Kaspar, P.G. Hirrlinger, F. Kirchhoff, J.M. Bissonnette, N. Ballas, and G. Mandel A role for glia in the progression of Rett's syndrome Nature 475 2011 497 500
31. L. Lopez-Serra, E. Ballestar, M.F. Fraga, M. Alaminos, F. Setien, and M. Esteller A profile of methyl-CpG binding domain protein occupancy of hypermethylated promoter CpG islands of tumor suppressor genes in human cancer Cancer Res. 66 2006 8342 8346
32. A. Mortazavi, B.A. Williams, K. McCue, L. Schaeffer, and B. Wold Mapping and quantifying mammalian transcriptomes by RNA-Seq Nat. Methods 5 2008 621 628
33. M. Münzel, D. Globisch, T. Brückl, M. Wagner, V. Welzmiller, S. Michalakis, M. Müller, M. Biel, and T. Carell Quantification of the sixth DNA base hydroxymethylcytosine in the brain Angew. Chem. Int. Ed. Engl. 49 2010 5375 5377
34. S.L. Palay, and V. Chan-Palay Cerebellar Cortex: Cytology and Organization 1974 Springer-Verlag New York ISBN: 0387062289
35. W.A. Pastor, U.J. Pape, Y. Huang, H.R. Henderson, R. Lister, M. Ko, E.M. McLoughlin, Y. Brudno, S. Mahapatra, and P. Kapranov Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells Nature 473 2011 394 397
36. M. Rutlin, and S.B. Nelson MeCP2: phosphorylated locally, acting globally Neuron 72 2011 3 5
37. P.J. Skene, R.S. Illingworth, S. Webb, A.R. Kerr, K.D. James, D.J. Turner, R. Andrews, and A.P. Bird Neuronal MeCP2 is expressed at near histone-octamer levels and globally alters the chromatin state Mol. Cell 37 2010 457 468
38. C.X. Song, K.E. Szulwach, Y. Fu, Q. Dai, C. Yi, X. Li, Y. Li, C.H. Chen, W. Zhang, and X. Jian Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine Nat. Biotechnol. 29 2011 68 72
39. K.E. Szulwach, X. Li, Y. Li, C.-X. Song, H. Wu, Q. Dai, H. Irier, A.K. Upadhyay, M. Gearing, and A.I. Levey 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging Nat. Neurosci. 14 2011 1607 1616
40. A. Szwagierczak, S. Bultmann, C.S. Schmidt, F. Spada, and H. Leonhardt Sensitive enzymatic quantification of 5-hydroxymethylcytosine in genomic DNA Nucleic Acids Res. 38 2010 e181
41. M. Tahiliani, K.P. Koh, Y. Shen, W.A. Pastor, H. Bandukwala, Y. Brudno, S. Agarwal, L.M. Iyer, D.R. Liu, L. Aravind, and A. Rao Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1 Science 324 2009 930 935
42. J. Tao, and H. Wu Deciphering Rett Syndrome with mouse genetics, epigenomics, and human neurons Int. Rev. Neurobiol. 89 2009 147 160
43. A.A. Thambirajah, M.K. Ng, L.J. Frehlick, A. Li, J.J. Serpa, E.V. Petrotchenko, B. Silva-Moreno, K.K. Missiaen, C.H. Borchers, and J. Adam Hall MeCP2 binds to nucleosome free (linker DNA) regions and to H3K9/H3K27 methylated nucleosomes in the brain Nucleic Acids Res. 40 2012 2884 2897
44. V. Valinluck, H.-H. Tsai, D.K. Rogstad, A. Burdzy, A. Bird, and L.C. Sowers Oxidative damage to methyl-CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2) Nucleic Acids Res. 32 2004 4100 4108
45. M. Weber, J.J. Davies, D. Wittig, E.J. Oakeley, M. Haase, W.L. Lam, and D. Schübeler Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells Nat. Genet. 37 2005 853 862
46. O. Yildirim, R. Li, J.-H. Hung, P.B. Chen, X. Dong, L.-S. Ee, Z. Weng, O.J. Rando, and T.G. Fazzio Mbd3/NURD complex regulates expression of 5-hydroxymethylcytosine marked genes in embryonic stem cells Cell 147 2011 1498 1510
47. M. Yu, G.C. Hon, K.E. Szulwach, C.X. Song, L. Zhang, A. Kim, X. Li, Q. Dai, Y. Shen, and B. Park Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome Cell 149 2012 1368 1380
48. Campoy, F.J.; Meehan, R.R.; McKay, S.; Nixon, J.; and Bird, A. (1995). Binding of histone H1 to DNA is indifferent to methylation at CpG sequences. J. Biol. Chem. 270, 26473-26481.
49. Chavez, L.; Jozefczuk, J.; Grimm, C.; Dietrich, J.; Timmermann, B.; Lehrach, H.; Herwig, R.; and Adjaye, J. (2010). Computational analysis of genome-wide DNA methylation during the differentiation of human embryonic stem cells along the endodermal lineage. Genome Res. 20, 1441-1450.
50. Heiman, M.; Schaefer, A.; Gong, S.; Peterson, J.D.; Day, M.; Ramsey, K.E.; Suárez-Fariñas, M.; Schwarz, C.; Stephan, D.A.; Surmeier, D.J.; et al. (2008). A translational profiling approach for the molecular characterization of CNS cell types. Cell 135, 738-748.
51. Klose, R.J.; and Bird, A.P. (2004). MeCP2 behaves as an elongated monomer that does not stably associate with the Sin3a chromatin remodeling complex. J. Biol. Chem. 279, 46490-46496.
52. Kriaucionis, S.; and Heintz, N. (2009). The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324, 929-930.
53. Lein, E.S.; Hawrylycz, M.J.; Ao, N.; Ayres, M.; Bensinger, A.; Bernard, A.; Boe, A.F.; Boguski, M.S.; Brockway, K.S.; Byrnes, E.J.; et al. (2007). Genome-wide atlas of gene expression in the adult mouse brain. Nature 445, 168-176.
54. Morgan, M.; Anders, S.; Lawrence, M.; Aboyoun, P.; Pagès, H.; and Gentleman, R. (2009). ShortRead: a bioconductor package for input, quality assessment and exploration of high-throughput sequence data. Bioinformatics 25, 2607-2608.
55. Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
56. Saldanha, A.J. (2004). Java Treeview - extensible visualization of microarray data. Bioinformatics 20, 3246-3248.
57. Shevchenko, A.; Wilm, M.; Vorm, O.; and Mann, M. (1996). Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858.
58. Silva, J.C.; Gorenstein, M.V.; Li, G.Z.; Vissers, J.P.; and Geromanos, S.J. (2006). Absolute quantification of proteins by LCMSE: a virtue of parallel MS acquisition. Mol. Cell. Proteomics 5, 144-156.