Base-resolution analyses of sequence and parent-of-origin dependent DNA methylation in the mouse genome

Cell

Volumn 148, Issue 4, 2012, Pages 816-831

  Xie, Wei ^a   Barr, Cathy L ^b,c   Kim, Audrey ^a   Yue, Feng ^a   Lee, Ah Young ^a   Eubanks, James ^b   Dempster, Emma L ^b,d   Ren, Bing ^a,e  

^a LUDWIG INSTITUTE FOR CANCER RESEARCH   (United States)

^b UNIVERSITY HEALTH NETWORK   (Canada)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE; DINUCLEOTIDE; MICRORNA;

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BASE PAIRING; DNA METHYLATION; EMBRYO DEVELOPMENT; EPIGENETICS; GENE EXPRESSION; GENOME IMPRINTING; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEQUENCE ANALYSIS;

EID: 84857331867     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2011.12.035     Document Type: Article

References (84)

1. L. Avila, R.K. Yuen, D. Diego-Alvarez, M.S. Peñaherrera, R. Jiang, and W.P. Robinson Evaluating DNA methylation and gene expression variability in the human term placenta Placenta 31 2010 1070 1077
2. T. Babak, B. Deveale, C. Armour, C. Raymond, M.A. Cleary, D. van der Kooy, J.M. Johnson, and L.P. Lim Global survey of genomic imprinting by transcriptome sequencing Curr. Biol. 18 2008 1735 1741
3. M.S. Bartolomei, and A.C. Ferguson-Smith Mammalian genomic imprinting Cold Spring Harb. Perspect. Biol. 3 2011 10.1101/cshperspect.a002592
4. A. Bird DNA methylation patterns and epigenetic memory Genes Dev. 16 2002 6 21 (Pubitemid 34049633)
5. F. Chedin, M.R. Lieber, and C.L. Hsieh The DNA methyltransferase-like protein DNMT3L stimulates de novo methylation by Dnmt3a Proc. Natl. Acad. Sci. USA 99 2002 16916 16921 (Pubitemid 36034073)
6. T. Chen, and E. Li Structure and function of eukaryotic DNA methyltransferases Curr. Top. Dev. Biol. 60 2004 55 89 (Pubitemid 39752359)
7. P.Y. Chen, S. Feng, J.W. Joo, S.E. Jacobsen, and M. Pellegrini A comparative analysis of DNA methylation across human embryonic stem cell lines Genome Biol. 12 2011 R62
8. T. Chen, Y. Ueda, S. Xie, and E. Li A novel Dnmt3a isoform produced from an alternative promoter localizes to euchromatin and its expression correlates with active de novo methylation J. Biol. Chem. 277 2002 38746 38754 (Pubitemid 35154737)
9. M. Chotalia, S.A. Smallwood, N. Ruf, C. Dawson, D. Lucifero, M. Frontera, K. James, W. Dean, and G. Kelsey Transcription is required for establishment of germline methylation marks at imprinted genes Genes Dev. 23 2009 105 117
10. S. Choufani, J.S. Shapiro, M. Susiarjo, D.T. Butcher, D. Grafodatskaya, Y. Lou, J.C. Ferreira, D. Pinto, S.W. Scherer, and L.G. Shaffer A novel approach identifies new differentially methylated regions (DMRs) associated with imprinted genes Genome Res. 21 2011 465 476
11. S.J. Cokus, S. Feng, X. Zhang, Z. Chen, B. Merriman, C.D. Haudenschild, S. Pradhan, S.F. Nelson, M. Pellegrini, and S.E. Jacobsen Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning Nature 452 2008 215 219 (Pubitemid 351380251)
12. W.N. Cooper, and M. Constância How genome-wide approaches can be used to unravel the remaining secrets of the imprintome Brief Funct Genomics 9 2010 315 328
13. S.T. da Rocha, C.A. Edwards, M. Ito, T. Ogata, and A.C. Ferguson-Smith Genomic imprinting at the mammalian Dlk1-Dio3 domain Trends Genet. 24 2008 306 316
14. O.V. Dyachenko, T.V. Schevchuk, L. Kretzner, Y.I. Buryanov, and S.S. Smith Human non-CG methylation: are human stem cells plant-like? Epigenetics 5 2010 569 572
15. J. Gertz, K.E. Varley, T.E. Reddy, K.M. Bowling, F. Pauli, S.L. Parker, K.S. Kucera, H.F. Willard, and R.M. Myers Analysis of DNA methylation in a three-generation family reveals widespread genetic influence on epigenetic regulation PLoS Genet. 7 2011 e1002228
16. C. Gregg, J. Zhang, B. Weissbourd, S. Luo, G.P. Schroth, D. Haig, and C. Dulac High-resolution analysis of parent-of-origin allelic expression in the mouse brain Science 329 2010 643 648
17. T.R. Haines, D.I. Rodenhiser, and P.J. Ainsworth Allele-specific non-CpG methylation of the Nf1 gene during early mouse development Dev. Biol. 240 2001 585 598 (Pubitemid 34056513)
18. Y. Hayashizaki, H. Shibata, S. Hirotsune, H. Sugino, Y. Okazaki, N. Sasaki, K. Hirose, H. Imoto, H. Okuizumi, and M. Muramatsu Identification of an imprinted U2af binding protein related sequence on mouse chromosome 11 using the RLGS method Nat. Genet. 6 1994 33 40 (Pubitemid 24191910)
19. A. Hellman, and A. Chess Extensive sequence-influenced DNA methylation polymorphism in the human genome Epigenetics Chromatin 3 2010 11
20. H. Hiura, A. Sugawara, H. Ogawa, R.M. John, N. Miyauchi, Y. Miyanari, T. Horiike, Y. Li, N. Yaegashi, and H. Sasaki A tripartite paternally methylated region within the Gpr1-Zdbf2 imprinted domain on mouse chromosome 1 identified by meDIP-on-chip Nucleic Acids Res. 38 2010 4929 4945
21. T. Imamura, A. Kerjean, T. Heams, J.J. Kupiec, C. Thenevin, and A. Pàldi Dynamic CpG and non-CpG methylation of the Peg1/Mest gene in the mouse oocyte and preimplantation embryo J. Biol. Chem. 280 2005 20171 20175 (Pubitemid 41379549)
22. D. Jia, R.Z. Jurkowska, X. Zhang, A. Jeltsch, and X. Cheng Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation Nature 449 2007 248 251 (Pubitemid 47402375)
23. T.M. Keane, L. Goodstadt, P. Danecek, M.A. White, K. Wong, B. Yalcin, A. Heger, A. Agam, G. Slater, and M. Goodson Mouse genomic variation and its effect on phenotypes and gene regulation Nature 477 2011 289 294
24. G. Kelsey, D. Bodle, H.J. Miller, C.V. Beechey, C. Coombes, J. Peters, and C.M. Williamson Identification of imprinted loci by methylation-sensitive representational difference analysis: application to mouse distal chromosome 2 Genomics 62 1999 129 138 (Pubitemid 30053926)
25. K. Kerkel, A. Spadola, E. Yuan, J. Kosek, L. Jiang, E. Hod, K. Li, V.V. Murty, N. Schupf, and E. Vilain Genomic surveys by methylation-sensitive SNP analysis identify sequence-dependent allele-specific DNA methylation Nat. Genet. 40 2008 904 908
26. S. Kriaucionis, and N. Heintz The nuclear DNA base 5- hydroxymethylcytosine is present in Purkinje neurons and the brain Science 324 2009 929 930
27. M. Lalande Parental imprinting and human disease Annu. Rev. Genet. 30 1996 173 195 (Pubitemid 27014467)
28. E. Li, T.H. Bestor, and R. Jaenisch Targeted mutation of the DNA methyltransferase gene results in embryonic lethality Cell 69 1992 915 926
29. R. Lister, R.C. O'Malley, J. Tonti-Filippini, B.D. Gregory, C.C. Berry, A.H. Millar, and J.R. Ecker Highly integrated single-base resolution maps of the epigenome in Arabidopsis Cell 133 2008 523 536
30. R. Lister, M. Pelizzola, R.H. Dowen, R.D. Hawkins, G. Hon, J. Tonti-Filippini, J.R. Nery, L. Lee, Z. Ye, and Q.M. Ngo Human DNA methylomes at base resolution show widespread epigenomic differences Nature 462 2009 315 322
31. R. Lister, M. Pelizzola, Y.S. Kida, R.D. Hawkins, J.R. Nery, G. Hon, J. Antosiewicz-Bourget, R. O'Malley, R. Castanon, and S. Klugman Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells Nature 471 2011 68 73
32. A. Meissner, T.S. Mikkelsen, H. Gu, M. Wernig, J. Hanna, A. Sivachenko, X. Zhang, B.E. Bernstein, C. Nusbaum, and D.B. Jaffe Genome-scale DNA methylation maps of pluripotent and differentiated cells Nature 454 2008 766 770
33. R.D. Nicholls, and J.L. Knepper Genome organization, function, and imprinting in Prader-Willi and Angelman syndromes Annu. Rev. Genomics Hum. Genet. 2 2001 153 175 (Pubitemid 35265004)
34. M. Okano, D.W. Bell, D.A. Haber, and E. Li DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development Cell 99 1999 247 257 (Pubitemid 29519904)
35. S.K. Ooi, C. Qiu, E. Bernstein, K. Li, D. Jia, Z. Yang, H. Erdjument-Bromage, P. Tempst, S.P. Lin, and C.D. Allis DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA Nature 448 2007 714 717 (Pubitemid 47236857)
36. J. Peters, S.F. Wroe, C.A. Wells, H.J. Miller, D. Bodle, C.V. Beechey, C.M. Williamson, and G. Kelsey A cluster of oppositely imprinted transcripts at the Gnas locus in the distal imprinting region of mouse chromosome 2 Proc. Natl. Acad. Sci. USA 96 1999 3830 3835 (Pubitemid 29168996)
37. C. Plass, H. Shibata, I. Kalcheva, L. Mullins, N. Kotelevtseva, J. Mullins, R. Kato, H. Sasaki, S. Hirotsune, and Y. Okazaki Identification of Grf1 on mouse chromosome 9 as an imprinted gene by RLGS-M Nat. Genet. 14 1996 106 109 (Pubitemid 26301557)
38. B.H. Ramsahoye, D. Biniszkiewicz, F. Lyko, V. Clark, A.P. Bird, and R. Jaenisch Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a Proc. Natl. Acad. Sci. USA 97 2000 5237 5242 (Pubitemid 30313702)
39. W. Reik, and J. Walter Genomic imprinting: parental influence on the genome Nat. Rev. Genet. 2 2001 21 32 (Pubitemid 33674766)
40. W. Reik, W. Dean, and J. Walter Epigenetic reprogramming in mammalian development Science 293 2001 1089 1093 (Pubitemid 32758081)
41. H. Royo, and J. Cavaillé Non-coding RNAs in imprinted gene clusters Biol. Cell 100 2008 149 166 (Pubitemid 351372674)
42. L.C. Schalkwyk, E.L. Meaburn, R. Smith, E.L. Dempster, A.R. Jeffries, M.N. Davies, R. Plomin, and J. Mill Allelic skewing of DNA methylation is widespread across the genome Am. J. Hum. Genet. 86 2010 196 212
43. E. Schilling, C. El Chartouni, and M. Rehli Allele-specific DNA methylation in mouse strains is mainly determined by cis-acting sequences Genome Res. 19 2009 2028 2035
44. R. Schulz, K. Woodfine, T.R. Menheniott, D. Bourc'his, T. Bestor, and R.J. Oakey WAMIDEX: a web atlas of murine genomic imprinting and differential expression Epigenetics 3 2008 89 96
45. R. Shoemaker, J. Deng, W. Wang, and K. Zhang Allele-specific methylation is prevalent and is contributed by CpG-SNPs in the human genome Genome Res. 20 2010 883 889
46. P. Singh, X. Wu, D.H. Lee, A.X. Li, T.A. Rauch, G.P. Pfeifer, J.R. Mann, and P.E. Szabó Chromosome-wide analysis of parental allele-specific chromatin and DNA methylation Mol. Cell. Biol. 31 2011 1757 1770
47. R.J. Smith, W. Dean, G. Konfortova, and G. Kelsey Identification of novel imprinted genes in a genome-wide screen for maternal methylation Genome Res. 13 2003 558 569 (Pubitemid 36511915)
48. 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
49. M.A. Surani, R. Kothary, N.D. Allen, P.B. Singh, R. Fundele, A.C. Ferguson-Smith, and S.C. Barton Genome imprinting and development in the mouse Dev. Suppl. 1990 1990 89 98
50. S. Takada, M. Paulsen, M. Tevendale, C.E. Tsai, G. Kelsey, B.M. Cattanach, and A.C. Ferguson-Smith Epigenetic analysis of the Dlk1-Gtl2 imprinted domain on mouse chromosome 12: implications for imprinting control from comparison with Igf2-H19 Hum. Mol. Genet. 11 2002 77 86 (Pubitemid 34100770)
51. J.P. Thomson, P.J. Skene, J. Selfridge, T. Clouaire, J. Guy, S. Webb, A.R. Kerr, A. Deaton, R. Andrews, and K.D. James CpG islands influence chromatin structure via the CpG-binding protein Cfp1 Nature 464 2010 1082 1086
52. S. Tierling, S. Dalbert, S. Schoppenhorst, C.E. Tsai, S. Oliger, A.C. Ferguson-Smith, M. Paulsen, and J. Walter High-resolution map and imprinting analysis of the Gtl2-Dnchc1 domain on mouse chromosome 12 Genomics 87 2006 225 235 (Pubitemid 43117443)
53. S. Tomizawa, H. Kobayashi, T. Watanabe, S. Andrews, K. Hata, G. Kelsey, and H. Sasaki Dynamic stage-specific changes in imprinted differentially methylated regions during early mammalian development and prevalence of non-CpG methylation in oocytes Development 138 2011 811 820
54. B. Tycko Allele-specific DNA methylation: beyond imprinting Hum. Mol. Genet. 19 R2 2010 R210 R220
55. X. Wang, Q. Sun, S.D. McGrath, E.R. Mardis, P.D. Soloway, and A.G. Clark Transcriptome-wide identification of novel imprinted genes in neonatal mouse brain PLoS ONE 3 2008 e3839
56. B.L. Wienholz, M.S. Kareta, A.H. Moarefi, C.A. Gordon, P.A. Ginno, and F. Chédin DNMT3L modulates significant and distinct flanking sequence preference for DNA methylation by DNMT3A and DNMT3B in vivo PLoS Genet. 6 2010 e1001106
57. L.S. Wilkinson, W. Davies, and A.R. Isles Genomic imprinting effects on brain development and function Nat. Rev. Neurosci. 8 2007 832 843 (Pubitemid 350006217)
58. Y. Zhang, C. Rohde, R. Reinhardt, C. Voelcker-Rehage, and A. Jeltsch Non-imprinted allele-specific DNA methylation on human autosomes Genome Biol. 10 2009 R138
59. Y. Zheng, D. Cohen-Karni, D. Xu, H.G. Chin, G. Wilson, S. Pradhan, and R.J. Roberts A unique family of Mrr-like modification-dependent restriction endonucleases Nucleic Acids Res. 38 2010 5527 5534
60. M.J. Ziller, F. Muller, J. Liao, Y. Zhang, H. Gu, C. Bock, P. Boyle, C.B. Epstein, B.E. Bernstein, and T. Lengauer Genomic distribution and inter-sample variation of non-CpG methylation across human cell types PLoS Genet. 7 2011 e1002389
61. Bressler, J., Tsai, T.F., Wu, M.Y., Tsai, S.F., Ramirez, M.A., Armstrong, D., and Beaudet, A.L. (2001). The SNRPN promoter is not required for genomic imprinting of the Prader-Willi/Angelman domain in mice. Nat. Genet. 28, 232-240. (Pubitemid 32626025)
62. Ciccone, D.N., Su, H., Hevi, S., Gay, F., Lei, H., Bajko, J., Xu, G., Li, E., and Chen, T. (2009). KDM1B is a histone H3K4 demethylase required to establish maternal genomic imprints. Nature 461, 415-418.
63. Cohen-Karni, D., Xu, D., Apone, L., Fomenkov, A., Sun, Z., Davis, P.J., Kinney, S.R., Yamada-Mabuchi, M., Xu, S.Y., Davis, T., et al. (2011). The MspJI family of modification-dependent restriction endonucleases for epigenetic studies. Proc. Natl. Acad. Sci. USA 108, 11040-11045.
64. Crooks, G.E., Hon, G., Chandonia, J.M., and Brenner, S.E. (2004). WebLogo: a sequence logo generator. Genome Res. 14, 1188-1190. (Pubitemid 38811555)
65. Gregg, C., Zhang, J., Weissbourd, B., Luo, S., Schroth, G.P., Haig, D., and Dulac, C. (2010). High-resolution analysis of parent-of-origin allelic expression in the mouse brain. Science 329, 643-648.
66. Hawkins, R.D., Hon, G.C., Lee, L.K., Ngo, Q., Lister, R., Pelizzola, M., Edsall, L.E., Kuan, S., Luu, Y., Klugman, S., et al. (2010). Distinct epigenomic landscapes of pluripotent and lineage-committed human cells. Cell Stem Cell 6, 479-491.
67. Hiura, H., Sugawara, A., Ogawa, H., John, R.M., Miyauchi, N., Miyanari, Y., Horiike, T., Li, Y., Yaegashi, N., Sasaki, H., et al. (2010). A tripartite paternally methylated region within the Gpr1-Zdbf2 imprinted domain on mouse chromosome 1 identified by meDIP-on-chip. Nucleic Acids Res. 38, 4929-4945.
68. Jia, D., Jurkowska, R.Z., Zhang, X., Jeltsch, A., and Cheng, X. (2007). Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449, 248-251. (Pubitemid 47402375)
69. Kanduri, C. (2011). Kcnq1ot1: A chromatin regulatory RNA. Semin. Cell Dev. Biol. 22, 343-350.
70. Kantor, B., Shemer, R., and Razin, A. (2006). The Prader-Willi/Angelman imprinted domain and its control center. Cytogenet. Genome Res. 113, 300-305.
71. Kikyo, N., Williamson, C.M., John, R.M., Barton, S.C., Beechey, C.V., Ball, S.T., Cattanach, B.M., Surani, M.A., and Peters, J. (1997). Genetic and functional analysis of neuronatin in mice with maternal or paternal duplication of distal Chr 2. Dev. Biol. 190, 66-77. (Pubitemid 27444738)
72. Kin, T., Yamada, K., Terai, G., Okida, H., Yoshinari, Y., Ono, Y., Kojima, A., Kimura, Y., Komori, T., and Asai, K. (2007). fRNAdb: a platform for mining/annotating functional RNA candidates from non-coding RNA sequences. Nucleic Acids Res. 35 (Database issue), D145-D148. (Pubitemid 46056187)
73. Kobayashi, H., Suda, C., Abe, T., Kohara, Y., Ikemura, T., and Sasaki, H. (2006). Bisulfite sequencing and dinucleotide content analysis of 15 imprinted mouse differentially methylated regions (DMRs): paternally methylated DMRs contain less CpGs than maternally methylated DMRs. Cytogenet. Genome Res. 113, 130-137.
74. Landers, M., Bancescu, D.L., Le Meur, E., Rougeulle, C., Glatt-Deeley, H., Brannan, C., Muscatelli, F., and Lalande, M. (2004). Regulation of the large (approximately 1000 kb) imprinted murine Ube3a antisense transcript by alternative exons upstream of Snurf/Snrpn. Nucleic Acids Res. 32, 3480-3492. (Pubitemid 39117465)
75. Li, B.Z., Huang, Z., Cui, Q.Y., Song, X.H., Du, L., Jeltsch, A., Chen, P., Li, G., Li, E., and Xu, G.L. (2011). Histone tails regulate DNA methylation by allosterically activating de novo methyltransferase. Cell Res. 21, 1172-1181.
76. Lister, R., Pelizzola, M., Kida, Y.S., Hawkins, R.D., Nery, J.R., Hon, G., Antosiewicz-Bourget, J., O'Malley, R., Castanon, R., Klugman, S., et al. (2011). Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 471, 68-73.
77. Nakamura, T., Arai, Y., Umehara, H., Masuhara, M., Kimura, T., Taniguchi, H., Sekimoto, T., Ikawa, M., Yoneda, Y., Okabe, M., et al. (2007). PGC7/Stella protects against DNA demethylation in early embryogenesis. Nat. Cell Biol. 9, 64-71. (Pubitemid 46024198)
78. 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. (Pubitemid 47236857)
79. Schulz, R., Woodfine, K., Menheniott, T.R., Bourc'his, D., Bestor, T., and Oakey, R.J. (2008). WAMIDEX: a web atlas of murine genomic imprinting and differential expression. Epigenetics 3, 89-96.
80. Stöger, R., Kubicka, P., Liu, C.G., Kafri, T., Razin, A., Cedar, H., and Barlow, D.P. (1993). Maternal-specific methylation of the imprinted mouse Igf2r locus identifies the expressed locus as carrying the imprinting signal. Cell 73, 61-71. (Pubitemid 23115449)
81. 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.
82. Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M.J., Salzberg, S.L., Wold, B.J., and Pachter, L. (2010). Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515.
83. Wood, A.J., Schulz, R., Woodfine, K., Koltowska, K., Beechey, C.V., Peters, J., Bourc'his, D., and Oakey, R.J. (2008). Regulation of alternative polyadenylation by genomic imprinting. Genes Dev. 22, 1141-1146. (Pubitemid 351656573)
84. Zheng, Y., Cohen-Karni, D., Xu, D., Chin, H.G., Wilson, G., Pradhan, S., and Roberts, R.J. (2010). A unique family of Mrr-like modification-dependent restriction endonucleases. Nucleic Acids Res. 38, 5527-5534.