An interspecies analysis reveals a key role for unmethylated CpG dinucleotides in vertebrate Polycomb complex recruitment

EMBO Journal

Volumn 31, Issue 2, 2012, Pages 317-329

  Lynch, Magnus D ^a   Smith, Andrew J H ^a,b   De Gobbi, Marco ^a   Flenley, Maria ^a   Hughes, Jim R ^a   Vernimmen, Douglas ^a   Ayyub, Helena ^a   Sharpe, Jacqueline A ^a   Sloane Stanley, Jacqueline A ^a   Sutherland, Linda ^c   Meek, Stephen ^c   Burdon, Tom ^c   Gibbons, Richard J ^a   Garrick, David ^a   Higgs, Douglas R ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

chromatin bivalency; CpG islands; Polycomb; stem cells; transcriptional regulation

Indexed keywords

CPG DINUCLEOTIDE; DINUCLEOTIDE; DNA METHYLTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHROMATIN; CHROMOSOME; CONTROLLED STUDY; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; ORTHOLOGY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; TRANSCRIPTION INITIATION;

ALPHA-GLOBINS; ANIMALS; CELLS, CULTURED; CHROMATIN; CHROMOSOME MAPPING; CHROMOSOMES, HUMAN, PAIR 16; CPG ISLANDS; DNA METHYLATION; DNA, RECOMBINANT; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION; HUMANS; MICE; MICE, TRANSGENIC; PLURIPOTENT STEM CELLS; RECOMBINATION, GENETIC; REGULATORY SEQUENCES, NUCLEIC ACID; REPRESSOR PROTEINS; SPECIES SPECIFICITY; TRANSCRIPTION, GENETIC;

VERTEBRATA;

EID: 84857190178     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.399     Document Type: Article

References (44)

1. Adli M, Zhu J, Bernstein BE (2010) Genome-wide chromatin maps derived from limited numbers of hematopoietic progenitors. Nat Methods 7: 615-618
2. Anguita E, Hughes J, Heyworth C, Blobel GA, Wood WG, Higgs DR (2004) Globin gene activation during haemopoiesis is driven by protein complexes nucleated by GATA-1 and GATA-2. EMBO J 23: 2841-2852 (Pubitemid 39013556)
3. Antequera F, Bird A (1993) Number of CpG islands and genes in human and mouse. Proc Natl Acad Sci USA 90: 11995-11999 (Pubitemid 24008767)
4. Azuara V, Perry P, Sauer S, Spivakov M, Jorgensen HF, John RM, Gouti M, Casanova M, Warnes G, Merkenschlager M, Fisher AG (2006) Chromatin signatures of pluripotent cell lines. Nat Cell Biol 8: 532-538
5. Barna M, Merghoub T, Costoya JA, Ruggero D, Branford M, Bergia A, Samori B, Pandolfi PP (2002) Plzf mediates transcriptional repression of HoxD gene expression through chromatin remodeling. Dev Cell 3: 499-510 (Pubitemid 35256063)
6. Bernstein BE, Kamal M, Lindblad-Toh K, Bekiranov S, Bailey DK, Huebert DJ, McMahon S, Karlsson EK, Kulbokas III EJ, Gingeras TR, Schreiber SL, Lander ES (2005) Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120: 169-181 (Pubitemid 40174761)
7. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A,Wernig M, Plath K, Jaenisch R,Wagschal A, Feil R, Schreiber SL, Lander ES (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326
8. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, Levine SS, Wernig M, Tajonar A, Ray MK, Bell GW, Otte AP, Vidal M, Gifford DK, Young RA, Jaenisch R (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349-353 (Pubitemid 44050199)
9. Buehr M, Meek S, Blair K, Yang J, Ure J, Silva J, McLay R, Hall J, Ying QL, Smith A (2008) Capture of authentic embryonic stem cells from rat blastocysts. Cell 135: 1287-1298
10. Caretti G, Di Padova M, Micales B, Lyons GE, Sartorelli V (2004) The Polycomb Ezh2 methyltransferase regulates muscle gene expression and skeletal muscle differentiation. Genes Dev 18: 2627-2638 (Pubitemid 39453102)
11. Coller HA, Kruglyak L (2008) Genetics. It's the sequence, stupid!. Science 322: 380-381
12. De Gobbi M, Garrick D, Lynch M, Vernimmen D, Hughes JR, Goardon N, Luc S, Lower KM, Sloane-Stanley JA, Pina C, Soneji S, Renella R, Enver T, Taylor S, Jacobsen SE, Vyas P, Gibbons RJ, Higgs DR (2011) Generation of bivalent chromatin domains during cell fate decisions. Epigenetics Chromatin 4: 9
13. Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD, Epstein CB, Zhang X, Wang L, Issner R, Coyne M, Ku M, Durham T, Kellis M, Bernstein BE (2011) Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473: 43-49
14. Garrick D, De Gobbi M, Samara V, Rugless M, Holland M, Ayyub H, Lower K, Sloane-Stanley J, Gray N, Koch C, Dunham I, Higgs DR (2008) The role of the polycomb complex in silencing alpha-globin gene expression in nonerythroid cells. Blood 112: 3889-3899
15. Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331: 76-79
16. Hughes JR, Cheng JF, Ventress N, Prabhakar S, Clark K, Anguita E, De Gobbi M, de Jong P, Rubin E, Higgs DR (2005) Annotation of cis-regulatory elements by identification, subclassification, and functional assessment of multispecies conserved sequences. Proc Natl Acad Sci USA 102: 9830-9835 (Pubitemid 40993653)
17. Kim H, Kang K, Kim J (2009) AEBP2 as a potential targeting protein for Polycomb Repression Complex PRC2. Nucleic Acids Res 37: 2940-2950
18. Ku M, Koche RP, Rheinbay E, Mendenhall EM, Endoh M, Mikkelsen TS, Presser A, Nusbaum C, Xie X, Chi AS, Adli M, Kasif S, Ptaszek LM, Cowan CA, Lander ES, Koseki H, Bernstein BE (2008) Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet 4: e1000242
19. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, Chevalier B, Johnstone SE, Cole MF, Isono K, Koseki H, Fuchikami T, Abe K, Murray HL, Zucker JP, Yuan B, Bell GW, Herbolsheimer E, Hannett NM, Sun K et al (2006) Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125: 301-313 (Pubitemid 44313811)
20. Lindroth AM, Park YJ, McLean CM, Dokshin GA, Persson JM, Herman H, Pasini D, Miro X, Donohoe ME, Lee JT, Helin K, Soloway PD (2008) Antagonism between DNA and H3K27 methylation at the imprinted Rasgrf1 locus. PLoS Genet 4: e1000145
21. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, Edsall L, Antosiewicz-Bourget J, Stewart R, Ruotti V, Millar AH, Thomson JA, Ren B, Ecker JR (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462: 315-322
22. Margueron R, Reinberg D (2011) The Polycomb complex PRC2 and its mark in life. Nature 469: 343-349
23. Meek S, Buehr M, Sutherland L, Thomson A, Mullins JJ, Smith AJ, Burdon T (2010) Efficient gene targeting by homologous recombination in rat embryonic stem cells. PLoS One 5: e14225
24. Mendenhall EM, Koche RP, Truong T, Zhou VW, Issac B, Chi AS, Ku M, Bernstein BE (2010) GC-rich sequence elements recruit PRC2 in mammalian ES cells. PLoS Genet 6: e1001244
25. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, BrockmanW, Kim TK, Koche RP, LeeW, Mendenhall E, O'Donovan A, Presser A, Russ C, Xie X, Meissner A, Wernig M, Jaenisch R, Nusbaum C et al (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553-560 (Pubitemid 47206934)
26. Pal-Bhadra M, Bhadra U, Birchler JA (1997) Cosuppression in Drosophila: gene silencing of Alcohol dehydrogenase by white-Adh transgenes is Polycomb dependent. Cell 90: 479-490 (Pubitemid 27347238)
27. Pandey RR, Mondal T, Mohammad F, Enroth S, Redrup L, Komorowski J, Nagano T, Mancini-Dinardo D, Kanduri C (2008) Kcnq1ot1 antisense noncoding RNA mediates lineage-specific transcriptional silencing through chromatin-level regulation. Mol Cell 32: 232-246
28. Pennacchio LA, Rubin EM (2001) Genomic strategies to identify mammalian regulatory sequences. Nat Rev Genet 2: 100-109 (Pubitemid 33674001)
29. Puschendorf M, Terranova R, Boutsma E, Mao X, Isono K, Brykczynska U, Kolb C, Otte AP, Koseki H, Orkin SH, van Lohuizen M, Peters AH (2008) PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos. Nat Genet 40: 411-420 (Pubitemid 351450889)
30. Raymond CS, Soriano P (2007) High-efficiency FLP and PhiC31 site-specific recombination in mammalian cells. PLoS One 2: e162
31. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, Chang HY (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129: 1311-1323 (Pubitemid 46962090)
32. Ruvinsky I, Ruvkun G (2003) Functional tests of enhancer conservation between distantly related species. Development 130: 5133-5142 (Pubitemid 37369673)
33. Sing A, Pannell D, Karaiskakis A, Sturgeon K, Djabali M, Ellis J, Lipshitz HD, Cordes SP (2009) A vertebrate Polycomb response element governs segmentation of the posterior hindbrain. Cell 138: 885-897
34. Swiezewski S, Liu F, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462: 799-802
35. Thomas KR, Capecchi MR (1987) Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51: 503-512
36. Thomson JP, Skene PJ, Selfridge J, Clouaire T, Guy J, Webb S, Kerr AR, Deaton A, Andrews R, James KD, Turner DJ, Illingworth R, Bird A (2010) CpG islands influence chromatin structure via the CpG-binding protein Cfp1. Nature 464: 1082-1086
37. Vyas P, Vickers MA, Simmons DL, Ayyub H, Craddock CF, Higgs DR (1992) Cis-acting sequences regulating expression of the human alpha-globin cluster lie within constitutively open chromatin. Cell 69: 781-793
38. Wallace HA, Marques-Kranc F, Richardson M, Luna-Crespo F, Sharpe JA, Hughes J, Wood WG, Higgs DR, Smith AJ (2007) Manipulating the mouse genome to engineer precise functional syntenic replacements with human sequence. Cell 128: 197-209 (Pubitemid 46048892)
39. Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, Agarwala R, Ainscough R, Alexandersson M, An P, Antonarakis SE, Attwood J, Baertsch R, Bailey J, Barlow K, Beck S, Berry E, Birren B, Bloom T, Bork P et al (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520-562 (Pubitemid 35477048)
40. Wilson MD, Barbosa-Morais NL, Schmidt D, Conboy CM, Vanes L, Tybulewicz VL, Fisher EM, Tavare S, Odom DT (2008) Speciesspecific transcription in mice carrying human chromosome 21. Science 322: 434-438
41. Woo CJ, Kharchenko PV, Daheron L, Park PJ, Kingston RE (2010) A region of the human HOXD cluster that confers Polycomb-group responsiveness. Cell 140: 99-110
42. Wu H, Coskun V, Tao J, Xie W, Ge W, Yoshikawa K, Li E, Zhang Y, Sun YE (2010) Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 329: 444-448
43. Yap KL, Li S, Munoz-Cabello AM, Raguz S, Zeng L, Mujtaba S, Gil J, Walsh MJ, Zhou MM (2010) Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol Cell 38: 662-674
44. Zhao J, Sun BK, Erwin JA, Song JJ, Lee JT (2008) Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 322: 750-756