Tet3 and DNA replication mediate demethylation of both the maternal and paternal genomes in mouse zygotes

Cell Stem Cell

Volumn 15, Issue 4, 2014, Pages 459-471

  Shen, Li ^a,b   Inoue, Azusa ^a,b   He, Jin ^a,b   Liu, Yuting ^a,b   Lu, Falong ^a,b   Zhang, Yi ^a,b,c  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; TET3 PROTEIN; UNCLASSIFIED DRUG; 5 METHYLCYTOSINE; DNA BINDING PROTEIN; ONCOPROTEIN; TET3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE G2 PHASE; CONTROLLED STUDY; DEMETHYLATION; DNA METHYLATION; DNA REPLICATION; ENZYME ACTIVE SITE; EXON; GENE ACTIVATION; GENE EXPRESSION; GENOME; MATERNAL GENOME; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PATERNAL GENOME; PRIORITY JOURNAL; PRONUCLEUS; ZYGOTE; ANIMAL; BIOLOGICAL MODEL; EMBRYO DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION; GENE LOCUS; GENETICS; KNOCKOUT MOUSE; MALE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE REPEAT; OXIDATION REDUCTION REACTION;

5-METHYLCYTOSINE; ANIMALS; DNA METHYLATION; DNA REPLICATION; DNA-BINDING PROTEINS; EMBRYONIC DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC LOCI; GENOME; MALE; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PROTO-ONCOGENE PROTEINS; REPETITIVE SEQUENCES, NUCLEIC ACID; ZYGOTE;

EID: 84914818905     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2014.09.002     Document Type: Article

References (38)

1. Bian, C., and Yu, X. (2014). PGC7 suppresses TET3 for protecting DNA methyl-ation. Nucleic Acids Res. 42, 2893-2905.
2. Goldberg, A.D., Allis, C.D., and Bernstein, E. (2007). Epigenetics: a landscape takes shape. Cell 128, 635-638.
3. Gu, T.P., Guo, F., Yang, H., Wu, H.P., Xu, G.F., Liu, W., Xie, Z.G., Shi, L., He, X., Jin, S.G., et al. (2011). The role of Tet3 DNA dioxygenase in epigenetic reprog-ramming by oocytes. Nature 477, 606-610.
4. Guo, H., Zhu, P., Wu, X., Li, X., Wen, L., and Tang, F. (2013). Single-cell meth-ylome landscapes of mouse embryonic stem cells and early embryos analyzed using reduced representation bisulfite sequencing. Genome Res. 23, 2126-2135.
5. Guo, H., Zhu, P., Yan, L., Li, R., Hu, B., Lian, Y., Yan, J., Ren, X., Lin, S., Li, J., et al. (2014). The DNA methylation landscape of human early embryos. Nature 511, 606-610.
6. Hajkova, P., Jeffries, S.J., Lee, C., Miller, N., Jackson, S.P., and Surani, M.A. (2010). Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 329, 78-82.
7. Hamatani, T., Carter, M.G., Sharov, A.A., and Ko, M.S. (2004). Dynamics of global gene expression changes during mouse preimplantation development. Dev. Cell 6, 117-131.
8. He, Y.F., Li, B.Z., Li, Z., Liu, P., Wang, Y., Tang, Q., Ding, J., Jia, Y., Chen, Z., Li, L., et al. (2011). Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333, 1303-1307.
9. Hirasawa, R., Chiba, H., Kaneda, M., Tajima, S., Li, E., Jaenisch, R., and Sasaki, H. (2008). Maternal and zygotic Dnmt1 are necessary and sufficient for the maintenanceofDNA methylationimprints during preimplantation development. Genes Dev. 22, 1607-1616.
10. Inoue, A., and Zhang, Y. (2011). Replication-dependent loss of 5-hydroxyme-thylcytosine in mouse preimplantation embryos. Science 334, 194.
11. Inoue, A., Shen, L., Dai, Q., He, C., and Zhang, Y. (2011). Generation and replication-dependent dilution of 5fC and 5caC during mouse preimplantation development. Cell Res. 21, 1670-1676.
12. Inoue, A., Matoba, S., and Zhang, Y. (2012). Transcriptional activation of trans-posable elements in mouse zygotes is independent of Tet3-mediated 5-meth-ylcytosine oxidation. Cell Res. 22, 1640-1649.
13. Iqbal, K., Jin, S.G., Pfeifer, G.P., and Szabó, P.E. (2011). Reprogramming of the paternal genome upon fertilization involves genome-wide oxidationof 5-meth-ylcytosine. Proc. Natl. Acad. Sci. USA 108, 3642-3647.
14. Ito, S., D'Alessio, A.C., Taranova, O.V., Hong, K., Sowers, L.C., and Zhang, Y. (2010). Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466, 1129-1133.
15. Ito, S., Shen, L., Dai, Q., Wu, S.C., Collins, L.B., Swenberg, J.A., He, C., and Zhang, Y. (2011). Tet proteins can convert 5-methylcytosine to 5-formylcyto-sine and 5-carboxylcytosine. Science 333, 1300-1303.
16. Jaenisch, R., and Bird, A. (2003). Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33 (Suppl), 245-254.
17. Kang, E., Wu, G., Ma, H., Li, Y., Tippner-Hedges, R., Tachibana, M., Sparman, M., Wolf, D.P., Schöler, H.R., and Mitalipov, S. (2014). Nuclear reprogram-ming by interphase cytoplasm of two-cell mouse embryos. Nature 509, 101-104.
18. Kohli, R.M., and Zhang, Y. (2013). TET enzymes, TDG and the dynamics of DNA demethylation. Nature 502, 472-479.
19. Kurihara, Y., Kawamura, Y., Uchijima, Y., Amamo, T., Kobayashi, H., Asano, T., and Kurihara, H. (2008). Maintenance of genomic methylation patterns during preimplantation development requires the somatic form of DNA methyltrans-ferase 1. Dev. Biol. 313, 335-346.
20. Maiti, A., and Drohat, A.C. (2011). Thymine DNA glycosylase can rapidly excise 5-formylcytosine and 5-carboxylcytosine: potential implications for active demethylation of CpG sites. J. Biol. Chem. 286, 35334-35338.
21. Mayer, W., Niveleau, A., Walter, J., Fundele, R., and Haaf, T. (2000). Demethylation of the zygotic paternal genome. Nature 403, 501-502.
22. 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.
23. Nakamura, T., Liu, Y.J., Nakashima, H., Umehara, H., Inoue, K., Matoba, S., Tachibana, M., Ogura, A., Shinkai, Y., and Nakano, T. (2012). PGC7 binds his-tone H3K9me2 to protect against conversion of 5mC to 5hmC in early embryos. Nature 486, 415-419.
24. Oswald, J., Engemann, S., Lane, N., Mayer, W., Olek, A., Fundele, R., Dean, W., Reik, W., and Walter, J. (2000). Active demethylation of the paternal genome in the mouse zygote. Curr. Biol. 10, 475-478.
25. Peaston, A.E., Evsikov, A.V., Graber, J.H., de Vries, W.N., Holbrook, A.E., Solter, D., and Knowles, B.B. (2004). Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. Dev. Cell 7, 597-606.
26. Plongthongkum, N., Diep, D.H., and Zhang, K. (2014). Advances in the profiling of DNA modifications: cytosine methylation and beyond. Nat. Rev. Genet. 15, 647-661.
27. Santos, F., Peat, J., Burgess, H., Rada, C., Reik, W., and Dean, W. (2013). Active demethylation in mouse zygotes involves cytosine deamination and base excision repair. Epigenetics Chromatin 6, 39.
28. Sasaki, H., and Matsui, Y. (2008). Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat. Rev. Genet. 9, 129-140.
29. Schultz, R.M. (2002). The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum. Reprod. Update 8, 323-331.
30. Seisenberger, S., Peat, J.R., and Reik, W. (2013). Conceptual links between DNA methylation reprogramming in the early embryo and primordial germ cells. Curr. Opin. Cell Biol. 25, 281-288.
31. Smallwood, S.A., Tomizawa, S., Krueger, F., Ruf, N., Carli, N., Segonds-Pichon, A., Sato, S., Hata, K., Andrews, S.R., and Kelsey, G. (2011). Dynamic CpG island methylation landscape in oocytes and preimplantation embryos. Nat. Genet. 43, 811-814.
32. Smith, Z.D., Chan, M.M., Mikkelsen, T.S., Gu, H., Gnirke, A., Regev, A., and Meissner, A. (2012). A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484, 339-344.
33. Smith, Z.D., Chan, M.M., Humm, K.C., Karnik, R., Mekhoubad, S., Regev, A., Eggan, K., and Meissner, A. (2014). DNA methylation dynamics of the human preimplantation embryo. Nature 511, 611-615.
34. Tahiliani, M., Koh, K.P., Shen, Y., Pastor, W.A., Bandukwala, H., Brudno, Y., Agarwal, S., Iyer, L.M., Liu, D.R., Aravind, L., and Rao, A. (2009). Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930-935.
35. Wang, L., Zhang, J., Duan, J., Gao, X., Zhu, W., Lu, X., Yang, L., Zhang, J., Li, G., Ci, W., et al. (2014). Programming and inheritance of parental DNA methyl-omes in mammals. Cell 157, 979-991.
36. Weyrich, A.(2012). Preparation of genomic DNA from mammalian sperm. Curr. Protoc. Mol. Biol. Chapter 2, 1-3, 13.
37. Wossidlo, M., Nakamura, T., Lepikhov, K., Marques, C.J., Zakhartchenko, V., Boiani, M., Arand, J., Nakano, T., Reik, W., and Walter, J. (2011). 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat Commun 2, 241.
38. Wu, H., and Zhang, Y.(2014). Reversing DNA methylation: mechanisms, geno-mics, and biological functions. Cell 156, 45-68.