Mouse Oocyte Methylomes at Base Resolution Reveal Genome-Wide Accumulation of Non-CpG Methylation and Role of DNA Methyltransferases

PLoS Genetics

Volumn 9, Issue 4, 2013, Pages

  Shirane, Kenjiro ^a,b   Toh, Hidehiro ^a   Kobayashi, Hisato ^c   Miura, Fumihito ^d   Chiba, Hatsune ^a,e   Ito, Takashi ^d   Kono, Tomohiro ^c   Sasaki, Hiroyuki ^a,b  

^a KYUSHU UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DNA; CYTOSINE; DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; DNA METHYLTRANSFERASE 3L; GUANINE; METHYLCYTOSINE; UNCLASSIFIED DRUG; DNA;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; CELL DIVISION; CELL GROWTH; CONTROLLED STUDY; DNA METHYLATION; ENZYME ACTIVITY; FEMALE; GENE STRUCTURE; GENOME; MAMMAL; MOUSE; MUTANT; NONHUMAN; OOCYTE; PROTEIN PROTEIN INTERACTION; ANIMAL; CPG ISLAND; GENETICS; METABOLISM; OOCYTE DEVELOPMENT;

MAMMALIA;

ANIMALS; CPG ISLANDS; DNA; DNA METHYLATION; GENOME; MICE; OOCYTES; OOGENESIS;

EID: 84876820776     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003439     Document Type: Article

References (51)

1. Sasaki H, Matsui Y, (2008) Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet 9: 129-140.
2. Law JA, Jacobsen SE, (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11: 204-220.
3. Laird PW, (2010) Principles and challenges of genome-wide DNA methylation analysis. Nat Rev Genet 11: 191-203.
4. Krueger F, Kreck B, Franke A, Andrews SR, (2012) DNA methylome analysis using short bisulfite sequencing data. Nat Methods 9: 145-151.
5. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, et al. (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462: 315-322.
6. Laurent L, Wong E, Li G, Huynh T, Tsirigos A, et al. (2010) Dynamic changes in the human methylome during differentiation. Genome Res 20: 320-331.
7. Lister R, Pelizzola M, Kida YS, Hawkins RD, Nery JR, et al. (2011) Hotspots of aberrant epigenomic reprogramming in human induced pluripotent stem cells. Nature 471: 68-73.
8. 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.
9. 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.
10. Tomizawa S, Kobayashi H, Watanabe T, Andrews S, Hata K, et al. (2011) Dynamic stage-specific changes in imprinted differentially methylated regions during early mammalian development and prevalence of non-CpG methylation in oocytes. Development 138: 811-820.
11. Kobayashi H, Sakurai T, Imai M, Takahashi N, Fukuda A, et al. (2012) Contribution of intragenic DNA methylation in mouse gametic DNA methylomes to establish oocyte-specific heritable marks. PLoS Genet 8: e1002440 doi:10.1371/journal.pgen.1002440.
12. Chédin F, (2011) The DNMT3 family of mammalian de novo DNA methyltransferases. Prog Mol Biol Transl Sci 101: 255-285.
13. Liao HF, Tai KY, Chen WS, Cheng LC, Ho HN, et al. (2012) Functions of DNA methyltransferase 3-like in germ cells and beyond. Biol Cell 104: 571-587.
14. Smallwood SA, Tomizawa S, Krueger F, Ruf N, Carli N, et al. (2011) Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat Genet 43: 811-814.
15. Miura F, Enomoto Y, Dairiki R, Ito T, (2012) Amplification-free whole-genome bisulfite sequencing by post-bisulfite adaptor tagging. Nucleic Acids Res 40: e136.
16. Kaneda M, Hirasawa R, Chiba H, Okano M, Li E, et al. (2010) Genetic evidence for Dnmt3a-dependent imprinting during oocyte growth obtained by conditional knockout with Zp3-Cre and complete exclusion of Dnmt3b by chimera formation. Genes Cells 15: 169-179.
17. Arand J, Spieler D, Karius T, Branco MR, Meilinger D, et al. (2012) In vivo control of CpG and non-CpG DNA methylation by DNA methyltransferases. PLoS Genet 8: e1002750 doi:10.1371/journal.pgen.1002750.
18. Hiura H, Obata Y, Komiyama J, Shirai M, Kono T, (2006) Oocyte growth-dependent progression of maternal imprinting in mice. Genes Cells 11: 353-361.
19. Lane N, Dean W, Erhardt S, Hajkova P, Surani A, et al. (2003) Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35: 88-93.
20. Popp C, Dean W, Feng S, Cokus SJ, Andrews S, et al. (2010) Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463: 1101-1105.
21. Seisenberger S, Andrews S, Krueger F, Arand J, Walter J, et al. (2012) The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol Cell 48: 849-862.
22. Hackett JA, Sengupta R, Zylicz JJ, Murakami K, Lee C, et al. (2013) Germline demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science 339: 448-452.
23. Okamura K, Hagiwara-Takeuchi Y, Li T, Vu TH, Hirai M, et al. (2000) Comparative genome analysis of the mouse imprinted gene impact and its nonimprinted human homolog IMPACT: toward the structural basis for species-specific imprinting. Genome Res 10: 1878-1889.
24. Ono R, Shiura H, Aburatani H, Kohda T, Kaneko-Ishino T, et al. (2003) Identification of a large novel imprinted gene cluster on mouse proximal chromosome 6. Genome Res 13: 1696-1705.
25. Jia D, Jurkowska RZ, Zhang X, Jeltsch A, Cheng X, (2007) Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 449: 248-251.
26. Lucifero D, La Salle S, Bourc'his D, Martel J, Bestor TH, et al. (2007) Coordinate regulation of DNA methyltransferase expression during oogenesis. BMC Dev Biol 7: 36.
27. Haines TR, Rodenhiser DI, Ainsworth PJ, (2001) Allele-specific non-CpG methylation of the Nf1 gene during early mouse development. Dev Biol 240: 585-598.
28. Imamura T, Kerjean A, Heams T, Kupiec JJ, Thenevin C, et al. (2005) Dynamic CpG and non-CpG methylation of the Peg1/Mest gene in the mouse oocyte and preimplantation embryo. J Biol Chem 280: 20171-20175.
29. Chen PY, Feng S, Joo JW, Jacobsen SE, Pellegrini M, (2011) A comparative analysis of DNA methylation across human embryonic stem cell lines. Genome Biol 12: R62.
30. Ziller MJ, Müller F, Liao J, Zhang Y, Gu H, et al. (2011) Genomic distribution and inter-sample variation of non-CpG methylation across human cell types. PLoS Genet 7: e1002389 doi:10.1371/journal.pgen.1002389.
31. Wienholz BL, Kareta MS, Moarefi AH, Gordon CA, Ginno PA, et al. (2010) DNMT3L modulates significant and distinct flanking sequence preference for DNA methylation by DNMT3A and DNMT3B in vivo. PLoS Genet 6: e1001106 doi:10.1371/journal.pgen.1001106.
32. Ramsahoye BH, Biniszkiewicz D, Lyko F, Clark V, Bird AP, et al. (2000) Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. Proc Natl Acad Sci U S A 97: 5237-5242.
33. Hirasawa R, Chiba H, Kaneda M, Tajima S, Li E, et al. (2008) Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. Genes Dev 22: 1607-1616.
34. Bostick M, Kim JK, Estève PO, Clark A, Pradhan S, et al. (2007) UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317: 1760-1764.
35. Sharif J, Muto M, Takebayashi S, Suetake I, Iwamatsu A, et al. (2007) The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450: 908-912.
36. Wang S, Kou Z, Jing Z, Zhang Y, Guo X, et al. (2010) Proteome of mouse oocytes at different developmental stages. Proc Natl Acad Sci U S A 107: 17639-17644.
37. Aoki A, Suetake I, Miyagawa J, Fujio T, Chijiwa T, et al. (2001) Enzymatic properties of de novo-type mouse DNA (cytosine-5) methyltransferases. Nucleic Acids Res 29: 3506-3512.
38. Gowher H, Jeltsch A, (2002) Molecular enzymology of the catalytic domains of the Dnmt3a and Dnmt3b DNA methyltransferases. J Biol Chem 277: 20409-20414.
39. White J, Dalton S, (2005) Cell cycle control of embryonic stem cells. Stem Cell Rev 1: 131-138.
40. Smith ZD, Chan MM, Mikkelsen TS, Gu H, Gnirke A, et al. (2012) A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484: 339-344.
41. Ichiyanagi T, Ichiyanagi K, Miyake M, Sasaki H, (2013) Accumulation and loss of asymmetric non-CpG methylation during male germ-cell development. Nucleic Acids Res 41: 738-745.
42. Branco MR, Ficz G, Reik W, (2011) Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat Rev Genet 13: 7-13.
43. Song CX, Yi C, He C, (2012) Mapping recently identified nucleotide variants in the genome and transcriptome. Nat Biotechnol 30: 1107-1116.
44. Hata K, Okano M, Lei H, Li E, (2002) Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 129: 1983-1993.
45. Li E, Bestor TH, Jaenisch R, (1992) Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69: 915-926.
46. Okano M, Bell DW, Haber DA, Li E, (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99: 247-257.
47. Kaneda M, Okano M, Hata K, Sado T, Tsujimoto N, et al. (2004) Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429: 900-903.
48. Bourc'his D, Xu GL, Lin CS, Bollman B, Bestor TH, (2001) Dnmt3L and the establishment of maternal genomic imprints. Science 294: 2536-2539.
49. Krueger F, Andrews SR, (2011) Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 27: 1571-1572.
50. Dreszer TR, Karolchik D, Zweig AS, Hinrichs AS, Raney BJ, et al. (2012) The UCSC Genome Browser database: extensions and updates 2011. Nucleic Acids Res 40: D918-923.
51. Crooks GE, Hon G, Chandonia JM, Brenner SE, (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190.