A unique regulatory phase of DNA methylation in the early mammalian embryo

Nature

Volumn 484, Issue 7394, 2012, Pages 339-344

  Smith, Zachary D ^a,b,c   Chan, Michelle M ^a,d   Mikkelsen, Tarjei S ^a,b   Gu, Hongcang ^a   Gnirke, Andreas ^a   Regev, Aviv ^a,d   Meissner, Alexander ^a,b,c  

^a BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^b HARVARD STEM CELL INSTITUTE   (United States)

^c HARVARD UNIVERSITY   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANONICAL ANALYSIS; CELL ORGANELLE; DEVELOPMENTAL BIOLOGY; DNA; EMBRYO; FERTILIZATION (REPRODUCTION); GENOME; MAMMAL; METHYLATION; NUMERICAL MODEL; RODENT;

ANIMAL EXPERIMENT; ARTICLE; BLASTOCYST; CELL DENSITY; CELL DIVISION; CONFORMATIONAL TRANSITION; CPG ISLAND; DNA METHYLATION; EMBRYO; EMBRYO DEVELOPMENT; LONG TERMINAL REPEAT; MOUSE; NONHUMAN; OOCYTE CLEAVAGE; PRIORITY JOURNAL; RETROPOSON; SOMATIC CELL; ZYGOTE;

ANIMALS; CPG ISLANDS; DNA METHYLATION; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; FEMALE; FERTILIZATION; GENOME; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MALE; MICE; OOCYTES; SPERMATOZOA; TERMINAL REPEAT SEQUENCES; ZYGOTE;

MAMMALIA;

EID: 84859910536     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature10960     Document Type: Article

References (56)

1. Bird, A. DNA methylation patterns and epigenetic memory. Genes Dev. 16, 6-21 (2002). (Pubitemid 34049633)
2. Jaenisch, R. & Bird, A. Epigenetic regulation of gene expression: how the genome integrates intrinsic andenvironmental signals.NatureGenet.33(Suppl.) , 245-254 (2003). (Pubitemid 36278835)
3. Suzuki, M. M. & Bird, A. DNA methylation landscapes: provocative insights from epigenomics. Nature Rev. Genet. 9, 465-476 (2008). (Pubitemid 351693975)
4. Meissner, A. et al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454, 766-770 (2008).
5. Weber, M. et al.Chromosome-wide and promoter-specific analyses identify sites of differential DNA methylation in normal and transformed human cells. Nature Genet. 37, 853-862 (2005). (Pubitemid 41077111)
6. Weber, M. et al. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome. Nature Genet. 39, 457-466 (2007). (Pubitemid 46514772)
7. Ji, H. et al. Comprehensive methylome map of lineage commitment from haematopoietic progenitors. Nature 467, 338-342 (2010).
8. Wossidlo, M. et al. 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nature Commun. 2, 241 (2011).
9. Gu, T. P. et al. The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 477, 606-610 (2011).
10. Inoue, A. & Zhang, Y. Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science 334, 194 (2011).
11. Reik, W., Dean, W. & Walter, J. Epigenetic reprogramming in mammalian development. Science 293, 1089-1093 (2001). (Pubitemid 32758081)
12. Kafri, T. et al. Developmental pattern of gene-specific DNA methylation in the mouse embryo and germ line. Genes Dev. 6, 705-714 (1992).
13. Borgel, J. et al. Targets and dynamics of promoter DNA methylation during early mouse development. Nature Genet. 42, 1093-1100 (2010).
14. Meissner, A. Epigenetic modifications in pluripotent and differentiated cells. Nature Biotechnol. 28, 1079-1088 (2010).
15. Razin, A. & Shemer, R. DNA methylation in early development. Hum. Mol. Genet. 4, 1751-1755 (1995).
16. Monk, M., Boubelik, M. & Lehnert, S. Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. Development 99, 371-382 (1987). (Pubitemid 17048855)
17. Rougier, N. et al. Chromosome methylation patterns during mammalian preimplantation development. Genes Dev. 12, 2108-2113 (1998). (Pubitemid 28348034)
18. Mayer, W., Niveleau, A., Walter, J., Fundele, R. & Haaf, T. Demethylation of the zygotic paternal genome. Nature 403, 501-502 (2000). (Pubitemid 30082186)
19. Lane, N. et al. Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35, 88-93 (2003). (Pubitemid 36330631)
20. Oswald, J. et al. Active demethylation of the paternal genome in themouse zygote. Curr. Biol. 10, 475-478 (2000). (Pubitemid 30247337)
21. Santos, F., Hendrich, B., Reik, W. & Dean, W. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev. Biol. 241, 172-182 (2002). (Pubitemid 34066770)
22. Kim, S. H. et al. Differential DNA methylation reprogramming of various repetitive sequences in mouse preimplantation embryos. Biochem. Biophys. Res. Commun. 324, 58-63 (2004).
23. Bock, C. et al.Quantitative comparison of genome- wideDNAmethylationmapping technologies. Nature Biotechnol. 28, 1106-1114 (2010).
24. Harris, R. A. et al. Comparison of sequencing-based methods to profile DNA methylation and identification of monoallelic epigenetic modifications. Nature Biotechnol. 28, 1097-1105 (2010).
25. Smallwood, S. A. et al. Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nature Genet. 43, 811-814 (2011).
26. Davis, T. & Vaisvila, R. High sensitivity 5-hydroxymethylcytosine detection in Balb/C brain tissue. J. Vis. Exp. 48 (2011).
27. Ficz, G. et al. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 473, 398-402 (2011).
28. Szulwach, K. E. et al. Integrating 5-hydroxymethylcytosine into the epigenomic landscape of human embryonic stem cells. PLoS Genet. 7, e1002154 (2011).
29. Williams, K. et al. TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 473, 343-348 (2011).
30. Wu, H. et al. Genome-wide analysis of 5-hydroxymethylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells. Genes Dev. 25, 679-684 (2011).
31. Xu, Y. et al. Genome-wide regulation of 5hmC, 5mC, and gene expression by Tet1 hydroxylase in mouse embryonic stem cells. Mol. Cell 42, 451-464 (2011).
32. Branco, M. R., Ficz, G.&Reik, W.Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nature Rev. Genet. 13, 7-13 (2011).
33. Santos, F., Hendrich, B., Reik, W. & Dean, W. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev. Biol. 241, 172-182 (2002). (Pubitemid 34066770)
34. Hajkova, P. et al. Genome-wide reprogramming in the mouse germline entails the base excision repair pathway. Science 329, 78-82 (2010).
35. Wossidlo, M. et al. Dynamic link of DNA demethylation, DNA strand breaks and repair in mouse zygotes. EMBO J. 29, 1877-1888 (2010).
36. Popp, C. et al. Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency. Nature 463, 1101-1105 (2010).
37. Mouse Genome Sequencing Consortium. Initial sequencing and comparative analysis of the mouse genome. Nature 420, 520-562 (2002).
38. Ichiyanagi, K. et al. Locus-and domain-dependent control of DNA methylation at mouse B1retrotransposons duringmale germcell development. GenomeRes. 21, 2058-2066 (2011).
39. Goodier, J. L., Ostertag, E. M., Du, K. & Kazazian, H. H. Jr. A novel active L1 retrotransposon subfamily in the mouse. Genome Res. 11, 1677-1685 (2001). (Pubitemid 33040494)
40. Edwards, C. A. & Ferguson-Smith, A. Mechanisms regulating imprinted genes in clusters. Curr. Opin. Cell Biol. 19, 281-289 (2007). (Pubitemid 46899514)
41. Bestor, T. H. The DNA methyltransferases of mammals. Hum. Mol. Genet. 9, 2395-2402 (2000).
42. Hirasawa, R. et al. Maternal and zygoticDnmt1 are necessary and sufficient for the maintenance of DNA methylation imprints during preimplantation development. Genes Dev. 22, 1607-1616 (2008). (Pubitemid 351846841)
43. Lucifero, D. et al. Coordinate regulation of DNA methyltransferase expression during oogenesis. BMC Dev. Biol. 7, 36 (2007).
44. Ramsahoye, B. H. et al. Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. Proc. Natl Acad. Sci. USA 97, 5237-5242 (2000). (Pubitemid 30313702)
45. Ziller, M. J. et al. Genomic distribution and inter-sample variation of non-CpG methylation across human cell types. PLoS Genet. 7, e1002389 (2011).
46. Haines, T., Rodenhiser, D. & Ainsworth, P. Allele-specific non-CpG methylation of the Nf1 gene during early mouse development. Dev. Biol. 240, 585-598 (2001). (Pubitemid 34056513)
47. Tomizawa, S. et al. Dynamic stage-specific changes in imprinted differentially methylated regions duringearlymammalian development and prevalence of non-CpG methylation in oocytes. Development 138, 811-820 (2011).
48. Beraldi, R., Pittoggi, C., Sciamanna, I.,Mattei, E.& Spadafora, C. Expression of LINE-1 retroposons is essential for murine preimplantation development. Mol. Reprod. Dev. 73, 279-287 (2006).
49. Kigami, D., Minami, N., Takayama, H. & Imai, H. MuERV-L is one of the earliest transcribed genes in mouse one-cell embryos. Biol. Reprod. 68, 651-654 (2003). (Pubitemid 36139333)
50. Okada, Y., Yamagata, K., Hong, K.,Wakayama, T.&Zhang, Y. A role for the elongator complex in zygotic paternal genomedemethylation.Nature463, 554-558(2010).
51. Nagy, A.Manipulating the MouseEmbryo: a Laboratory Manual 3rd edn (Cold Spring Harbor Laboratory Press, 2003).
52. Smith, Z. D., Gu, H., Bock, C., Gnirke, A. & Meissner, A. High-throughput bisulfite sequencing in mammalian genomes. Methods 48, 226-232 (2009).
53. Gu, H. et al. Preparation of reduced representation bisulfite sequencing libraries for genome-scale DNAmethylation profiling. Nature Protocols 6, 468-481 (2011).
54. Gu, H. et al. Genome-scale DNAmethylationmapping of clinical samples at singlenucleotide resolution. Nature Methods 7, 133-136 (2010).
55. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289-300 (1995).
56. Blake, J. A., Bult, C. J., Kadin, J. A., Richardson, J. E.&Eppig, J. T. TheMouse Genome Database (MGD): premier model organism resource for mammalian genomics and genetics. Nucleic Acids Res. 39, D842-D848 (2011).