Protection of CpG islands from DNA methylation is DNA-encoded and evolutionarily conserved

Nucleic Acids Research

Volumn 44, Issue 14, 2016, Pages 6693-6706

  Long, Hannah K ^a,b,d   King, Hamish W ^a   Patient, Roger K ^b   Odom, Duncan T ^c   Klose, Robert J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; NUCLEOTIDE; TRANSCRIPTION FACTOR; PROTEIN BINDING;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CPG ISLAND; DNA BINDING; DNA METHYLATION; DNA SEQUENCE; GENE CONTROL; GENE INSERTION; GENETIC CONSERVATION; GENOMICS; HOST; HUMAN CHROMOSOME; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SPECIES DIFFERENCE; VERTEBRATE; ZEBRA FISH; ANIMAL; C57BL MOUSE; CELL LINE; CHROMOSOME 21; CONSERVED SEQUENCE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MALE; METABOLISM; MOLECULAR EVOLUTION; NUCLEOTIDE REPEAT; TRANSGENIC MOUSE;

ANIMALS; CELL LINE; CHROMOSOMES, HUMAN, PAIR 21; CONSERVED SEQUENCE; CPG ISLANDS; DNA; DNA METHYLATION; EVOLUTION, MOLECULAR; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REPETITIVE SEQUENCES, NUCLEIC ACID; SPECIES SPECIFICITY; TRANSCRIPTION FACTORS; VERTEBRATES;

EID: 84977487556     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw258     Document Type: Article

References (77)

1. Jones,P.A. (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet., 13, 484-492.
2. Klose,R.J. and Bird,A.P. (2006) Genomic DNA methylation: the mark and its mediators. Trends Biochem. Sci., 31, 89-97.
3. Sharif,J., Muto,M., Takebayashi,S., Suetake,I., Iwamatsu,A., Endo,T.A., Shinga,J., Mizutani-Koseki,Y., Toyoda,T., Okamura,K. et al. (2007) The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature, 450, 908-912.
4. Bird,A. (2002) DNA methylation patterns and epigenetic memory. Genes Dev., 16, 6-21.
5. Jones,P.A. and Liang,G. (2009) Rethinking how DNA methylation patterns are maintained. Nat. Rev. Genet., 10, 805-811.
6. Cooper,D.N., Taggart,M.H. and Bird,A.P. (1983) Unmethlated domains in vertebrate DNA. Nucleic Acids Res., 11, 647-658.
7. Bird,A., Taggart,M., Frommer,M., Miller,O.J. and Macleod,D. (1985) A fraction of the mouse genome that is derived from islands of nonmethylated, CpG-rich DNA. Cell, 40, 91-99.
8. Long,H.K., Sims,D., Heger,A., Blackledge,N.P., Kutter,C., Wright,M.L., Grutzner,F., Odom,D.T., Patient,R., Ponting,C.P. et al. (2013) Epigenetic conservation at gene regulatory elements revealed by non-methylated DNA profiling in seven vertebrates. eLife, 2, e00348.
9. Antequera,F. (2003) Structure, function and evolution of CpG island promoters. Cell. Mol. Life Sci.: CMLS, 60, 1647-1658.
10. Long,H.K., Blackledge,N.P. and Klose,R.J. (2013) ZF-CxxC domain-containing proteins, CpG islands and the chromatin connection. Biochem. Soc. Trans., 41, 727-740.
11. Blackledge,N.P., Zhou,J.C., Tolstorukov,M.Y., Farcas,A.M., Park,P.J. and Klose,R.J. (2010) CpG islands recruit a histone H3 lysine 36 demethylase. Mol. cell, 38, 179-190.
12. Thomson,J.P., Skene,P.J., Selfridge,J., Clouaire,T., Guy,J., Webb,S., Kerr,A.R., Deaton,A., Andrews,R., James,K.D. et al. (2010) CpG islands influence chromatin structure via the CpG-binding protein Cfp1. Nature, 464, 1082-1086.
13. Illingworth,R.S., Gruenewald-Schneider,U.,Webb,S., Kerr,A.R., James,K.D., Turner,D.J., Smith,C., Harrison,D.J., Andrews,R. and Bird,A.P. (2010) Orphan CpG islands identify numerous conserved promoters in the mammalian genome. PLoS Genet., 6, e1001134.
14. Weber,M., Hellmann,I., Stadler,M.B., Ramos,L., Paabo,S., Rebhan,M. and Schubeler,D. (2007) Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nat. Genet., 39, 457-466.
15. Straussman,R., Nejman,D., Roberts,D., Steinfeld,I., Blum,B., Benvenisty,N., Simon,I., Yakhini,Z. and Cedar,H. (2009) Developmental programming of CpG island methylation profiles in the human genome. Nat. Struct. Mol. Biol., 16, 564-571.
16. Hodges,E., Molaro,A., Dos Santos,C.O., Thekkat,P., Song,Q., Uren,P.J., Park,J., Butler,J., Rafii,S., McCombie,W.R. et al. (2011) Directional DNA methylation changes and complex intermediate states accompany lineage specificity in the adult hematopoietic compartment. Mol. Cell, 44, 17-28.
17. Mohn,F., Weber,M., Rebhan,M., Roloff,T.C., Richter,J., Stadler,M.B., Bibel,M. and Schubeler,D. (2008) Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol. Cell, 30, 755-766.
18. Xie,W., Schultz,M.D., Lister,R., Hou,Z., Rajagopal,N., Ray,P., Whitaker,J.W., Tian,S., Hawkins,R.D., Leung,D. et al. (2013) Epigenomic analysis of multilineage differentiation of human embryonic stem cells. Cell, 153, 1134-1148.
19. Farthing,C.R., Ficz,G., Ng,R.K., Chan,C.F., Andrews,S., Dean,W., Hemberger,M. and Reik,W. (2008) Global mapping of DNA methylation in mouse promoters reveals epigenetic reprogramming of pluripotency genes. PLoS Genet., 4, e1000116.
20. Stadler,M.B., Murr,R., Burger,L., Ivanek,R., Lienert,F., Sch oler,A., Wirbelauer,C., Oakeley,E.J., Gaidatzis,D., Tiwari,V.K. et al. (2011) DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature, 480, 490-495.
21. Mendenhall,E.M., Koche,R.P., Truong,T., Zhou,V.W., Issac,B., Chi,A.S., Ku,M. and Bernstein,B.E. (2010) GC-Rich sequence elements recruit PRC2 in mammalian ES cells. PLoS Genet., 6, e1001244.
22. Lienert,F., Wirbelauer,C., Som,I., Dean,A., Mohn,F. and Schubeler,D. (2011) Identification of genetic elements that autonomously determine DNA methylation states. Nat. Genet., 43, 1091-1097.
23. Krebs,A.R., Dessus-Babus,S., Burger,L. and Schubeler,D. (2014) High-throughput engineering of a mammalian genome reveals building principles of methylation states at CG rich regions. eLife, 3, e04094.
24. Wachter,E., Quante,T., Merusi,C., Arczewska,A., Stewart,F., Webb,S. and Bird,A. (2014) Synthetic CpG islands reveal DNA sequence determinants of chromatin structure. eLife, 3, e03397.
25. Dickson,J., Gowher,H., Strogantsev,R., Gaszner,M., Hair,A., Felsenfeld,G. and West,A.G. (2010) VEZF1 elements mediate protection from DNA methylation. PLoS Genet., 6, e1000804.
26. Brandeis,M., Frank,D., Keshet,I., Siegfried,Z., Mendelsohn,M., Nemes,A., Temper,V., Razin,A. and Cedar,H. (1994) Sp1 elements protect a CpG island from de novo methylation. Nature, 371, 435-438.
27. Macleod,D., Charlton,J., Mullins,J. and Bird,A.P. (1994) Sp1 sites in the mouse aprt gene promoter are required to prevent methylation of the CpG island. Genes Dev., 8, 2282-2292.
28. O'Doherty,A., Ruf,S., Mulligan,C., Hildreth,V., Errington,M.L., Cooke,S., Sesay,A., Modino,S., Vanes,L., Hernandez,D. et al. (2005) An aneuploid mouse strain carrying human chromosome 21 with Down syndrome phenotypes. Science, 309, 2033-2037.
29. Suster,M.L., Abe,G., Schouw,A. and Kawakami,K. (2011) Transposon-mediated BAC transgenesis in zebrafish. Nat. Protoc., 6, 1998-2021.
30. Blackledge,N.P., Long,H.K., Zhou,J.C., Kriaucionis,S., Patient,R. and Klose,R.J. (2012) Bio-CAP: a versatile and highly sensitive technique to purify and characterise regions of non-methylated DNA. Nucleic Acids Res., 40, e32.
31. Langmead,B., Trapnell,C., Pop,M. and Salzberg,S. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, R25.
32. Zhang,Y., Liu,T., Meyer,C., Eeckhoute,J., Johnson,D., Bernstein,B., Nusbaum,C., Myers,R., Brown,M., Li,W. et al. (2008) Model-based Analysis of ChIP-Seq (MACS). Genome Biol., 9, R137.
33. Gribble,S.M.,Wiseman,F.K., Clayton,S., Prigmore,E., Langley,E., Yang,F., Maguire,S., Fu,B., Rajan,D., Sheppard,O. et al. (2013) Massively parallel sequencing reveals the complex structure of an irradiated human chromosome on a mouse background in the Tc1 model of Down syndrome. PLoS One, 8, e60482.
34. Langmead,B. and Salzberg,S.L. (2012) Fast gapped-read alignment with Bowtie 2. Nat. Methods, 9, 357-359.
35. Kumar,S. and Subramanian,S. (2002) Mutation rates in mammalian genomes. Proc. Natl. Acad. Sci. U.S.A., 99, 803-808.
36. Ward,Michelle C., Wilson,Michael D., Barbosa-Morais,Nuno L., Schmidt,D., Stark,R., Pan,Q., Schwalie,Petra C., Menon,S., Lukk,M., Watt,S. et al. (2013) Latent regulatory potential of human-specific repetitive elements. Mol. Cell, 49, 262-272.
37. Krueger,F. and Andrews,S.R. (2011) Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics, 27, 1571-1572.
38. Illingworth,R., Kerr,A., Desousa,D., Jorgensen,H., Ellis,P., Stalker,J., Jackson,D., Clee,C., Plumb,R., Rogers,J. et al. (2008) A novel CpG island set identifies tissue-specific methylation at developmental gene loci. PLoS Biol., 6, e22.
39. Schmidt,D.,Wilson,M.D., Ballester,B., Schwalie,P.C., Brown,G.D., Marshall,A., Kutter,C., Watt,S., Martinez-Jimenez,C.P.,Mackay,S. et al. (2010) Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science, 328, 1036-1040.
40. Ke,M. and Raju,S. (2014) Comparative histology of human and cow, goat and sheep liver. J. Surg. Acad., 2, 10-13.
41. Baratta,J.L., Ngo,A., Lopez,B., Kasabwalla,N., Longmuir,K.J. and Robertson,R.T. (2009) Cellular organization of normal mouse liver: a histological, quantitative immunocytochemical, and fine structural analysis. Histochem. Cell Biol., 131, 713-726.
42. Wu,X., Schmidt,J.A., Avarbock,M.R., Tobias,J.W., Carlson,C.A., Kolon,T.F., Ginsberg,J.P. and Brinster,R.L. (2009) Prepubertal human spermatogonia and mouse gonocytes share conserved gene expression of germline stem cell regulatory molecules. Proce. Natl. Acad. Sci. U.S.A., 106, 21672-21677.
43. Sha,J., Zhou,Z., Li,J., Yin,L., Yang,H., Hu,G., Luo,M., Chan,H.C., Group,S.S. and Zhou,K. (2002) Identification of testis development and spermatogenesis-related genes in human and mouse testes using cDNA arrays. Mol. Hum. Reprod., 8, 511-517.
44. Anand,M. and Prasad,B.V. (2012) The computational analysis of human testis transcriptome reveals closer ties to pluripotency. J. Hum. Reprod. Sci., 5, 266-273.
45. Milne,T.A., Dou,Y., Martin,M.E., Brock,H.W., Roeder,R.G. and Hess,J.L. (2005) MLL associates specifically with a subset of transcriptionally active target genes. Proc. Natl. Acad. Sci. U.S.A., 102, 14765-14770.
46. Lander,E.S., Linton,L.M., Birren,B., Nusbaum,C., Zody,M.C., Baldwin,J., Devon,K., Dewar,K., Doyle,M., FitzHugh,W. et al. (2001) Initial sequencing and analysis of the human genome. Nature, 409, 860-921.
47. Hancks,D.C. and Kazazian Jr,H.H. (2012) Active human retrotransposons: variation and disease. Curr. Opin. Genet. Dev., 22, 191-203.
48. Deininger,P. (2011) Alu elements: know the SINEs. Genome Biol., 12, 236.
49. Coulondre,C., Miller,J.H., Farabaugh,P.J. and Gilbert,W. (1978) Molecular basis of base substitution hotspots in Escherichia coli. Nature, 274, 775-780.
50. Shen,J.C., Rideout,W.M. 3rd and Jones,P.A. (1994) The rate of hydrolytic deamination of 5-methylcytosine in double-stranded DNA. Nucleic Acids Res., 22, 972-976.
51. Takai,D. and Jones,P.A. (2002) Comprehensive analysis of CpG islands in human chromosomes 21 and 22. Proc. Natl. Acad. Sci. U.S.A., 99, 3740-3745.
52. Fazzari,M.J. and Greally,J.M. (2004) Epigenomics: beyond CpG islands. Nat. Rev. Genet., 5, 446-455.
53. Illingworth,R.S. and Bird,A.P. (2009) CpG islands-'a rough guide'. FEBS Lett., 583, 1713-1720.
54. Lister,R., Pelizzola,M., Dowen,R.H., Hawkins,R.D., Hon,G., Tonti-Filippini,J., Nery,J.R., Lee,L., Ye,Z., Ngo,Q.M. et al. (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature, 462, 315-322.
55. Feldmann,A., Ivanek,R., Murr,R., Gaidatzis,D., Burger,L. and Schübeler,D. (2013) Transcription factor occupancy can mediate active turnover of DNA methylation at regulatory regions. PLoS Genet., 9, e1003994.
56. Aravin,A.A. and Bourc'his,D. (2008) Small RNA guides for de novo DNA methylation in mammalian germ cells. Genes Dev., 22, 970-975.
57. Molaro,A., Falciatori,I., Hodges,E., Aravin,A.A.,Marran,K., Rafii,S., McCombie,W.R., Smith,A.D. and Hannon,G.J. (2014) Two waves of de novo methylation during mouse germ cell development. Genes Dev., 28, 1544-1549.
58. Thomas,J.H. and Schneider,S.E. (2011) Coevolution of retroelements and tandem zinc finger genes. Genome Res., 21, 1800-1812.
59. Rowe,H.M., Friedli,M., Offner,S., Verp,S., Mesnard,D.,Marquis,J., Aktas,T. and Trono,D. (2013) De novo DNA methylation of endogenous retroviruses is shaped by KRAB-ZFPs/KAP1 and ESET. Development, 140, 519-529.
60. Shin Voo,K., Carlone,D.L., Jacobsen,B.M., Flodin,A. and Skalnik,D.G. (2000) Cloning of a mammalian transcriptional activator that binds unmethylated CpG motifs and shares a CXXC domain with DNA methyltransferase, human trithorax, and methyl-CpG binding domain protein 1. Mol. Cell. Biol., 20, 2108-2121.
61. Ooi,S.K., Qiu,C., Bernstein,E., Li,K., Jia,D., Yang,Z., Erdjument-Bromage,H., Tempst,P., Lin,S.P., Allis,C.D. et al. (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature, 448, 714-717.
62. Morselli,M., Pastor,W.A., Montanini,B., Nee,K., Ferrari,R., Fu,K., Bonora,G., Rubbi,L., Clark,A.T., Ottonello,S. et al. (2015) In vivo targeting of de novo DNA methylation by histone modifications in yeast and mouse. eLife, 4, e06205.
63. Hu,J.-L., Zhou,B.O., Zhang,R.-R., Zhang,K.-L., Zhou,J.-Q. and Xu,G.-L. (2009) The N-terminus of histone H3 is required for de novo DNA methylation in chromatin. Proc. Natl. Acad. Sci. U.S.A., 106, 22187-22192.
64. Farcas,A.M., Blackledge,N.P., Sudbery,I., Long,H.K., McGouran,J.F., Rose,N.R., Lee,S., Sims,D., Cerase,A., Sheahan,T.W. et al. (2012) KDM2B links the Polycomb Repressive Complex 1 (PRC1) to recognition of CpG islands. eLife, 1, e00205.
65. Blackledge,N.P., Farcas,A.M., Kondo,T., King,H.W.,McGouran,J.F., Hanssen,L.L., Ito,S., Cooper,S., Kondo,K., Koseki,Y. et al. (2014) Variant PRC1 complex-dependent H2A ubiquitylation drives PRC2 recruitment and polycomb domain formation. Cell, 157, 1445-1459.
66. Boulard,M., Edwards,J.R. and Bestor,T.H. (2015) FBXL10 protects Polycomb-bound genes from hypermethylation. Nat. Genet., 47, 479-485.
67. He,J., Shen,L., Wan,M., Taranova,O.,Wu,H. and Zhang,Y. (2013) Kdm2b maintains murine embryonic stem cell status by recruiting PRC1 complex to CpG islands of developmental genes. Nat. Cell Biol., 15, 373-384.
68. Wu,X., Johansen,J.V. and Helin,K. (2013) Fbxl10/Kdm2b recruits polycomb repressive complex 1 to CpG islands and regulates H2A ubiquitylation. Mol. Cell, 49, 1134-1146.
69. Williams,K., Christensen,J., Pedersen,M.T., Johansen,J.V., Cloos,P.A.C., Rappsilber,J. and Helin,K. (2011) TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature, 473, 343-348.
70. Wu,H., D'Alessio,A.C., Ito,S., Xia,K., Wang,Z., Cui,K., Zhao,K., Eve Sun,Y. and Zhang,Y. (2011) Dual functions of Tet1 in transcriptional regulation in mouse embryonic stem cells. Nature, 473, 389-393.
71. Xu,Y., Wu,F., Tan,L., Kong,L., Xiong,L., Deng,J., Barbera,A.J., Zheng,L., Zhang,H., Huang,S. et al. (2011) Genome-wide regulation of 5hmC, 5mC, and gene expression by Tet1 hydroxylase in mouse embryonic stem cells. Mol. Cell, 42, 451-464.
72. Branco,M.R., Ficz,G. and Reik,W. (2012) Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat. Rev. Genet., 13, 7-13.
73. Sheaffer,K.L., Kim,R., Aoki,R., Elliott,E.N., Schug,J., Burger,L., Schübeler,D. and Kaestner,K.H. (2014) DNA methylation is required for the control of stem cell differentiation in the small intestine. Genes Dev., 28, 652-664.
74. Taberlay,P.C., Statham,A.L., Kelly,T.K., Clark,S.J. and Jones,P.A. (2014) Reconfiguration of nucleosome-depleted regions at distal regulatory elements accompanies DNA methylation of enhancers and insulators in cancer. Genome Res., 24, 1421-1432.
75. Ziller,M.J., Gu,H., Muller,F., Donaghey,J., Tsai,L.T.Y., Kohlbacher,O., De Jager,P.L., Rosen,E.D., Bennett,D.A., Bernstein,B.E. et al. (2013) Charting a dynamic DNA methylation landscape of the human genome. Nature, 500, 477-481.
76. Schaub,M.A., Boyle,A.P., Kundaje,A., Batzoglou,S. and Snyder,M. (2012) Linking disease associations with regulatory information in the human genome. Genome Res., 22, 1748-1759.
77. Rasmussen,K.D., Jia,G., Johansen,J.V., Pedersen,M.T., Rapin,N., Bagger,F.O., Porse,B.T., Bernard,O.A., Christensen,J. and Helin,K. (2015) Loss of TET2 in hematopoietic cells leads to DNA hypermethylation of active enhancers and induction of leukemogenesis. Genes Dev., 29, 910-922.