Safeguarding parental identity: Dnmt1 maintains imprints during epigenetic reprogramming in early embryogenesis

Genes and Development

Volumn 22, Issue 12, 2008, Pages 1567-1571

  Branco, Miguel R ^a   Oda, Masaaki ^a   Reik, Wolf ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

DNA methylation; Dnmt1; Genomic imprinting; Pre implantation embryos

Indexed keywords

DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B;

DNA METHYLATION; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; GENOME IMPRINTING; MAMMAL; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANIMALS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; GENOMIC IMPRINTING; HUMANS; MODELS, BIOLOGICAL; TIME FACTORS;

MAMMALIA;

EID: 45349103563     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1690508     Document Type: Review

References (41)

1. Bernstein, B.E., Meissner, A., and Lander, E.S. 2007. The mammalian epigenome. Cell 128: 669-681.
2. Bird, A. 2002. DNA methylation patterns and epigenetic memory. Genes & Dev. 16: 6-21.
3. Bostick, M., Kim, J.K., Esteve, P.O., Clark, A., Pradhan, S., and Jacobsen, S.E. 2007. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317: 1760-1764.
4. Bourc'his, D., Xu, G.L., Lin, C.S., Bollman, B., and Bestor, T.H. 2001. Dnmt3L and the establishment of maternal genomic imprints. Science 294: 2536-2539.
5. Burgers, W.A., Fuks, F., and Kouzarides, T. 2002. DNA methyltransferases get connected to chromatin. Trends Genet. 18: 275-277.
6. Carlson, L.L., Page, A.W., and Bestor, T.H. 1992. Properties and localization of DNA methyltransferase in preimplantation mouse embryos: Implications for genomic imprinting. Genes & Dev. 6: 2536-2541.
7. Chen, T. and Li, E. 2004. Structure and function of eukaryotic DNA methyltransferases. Curr. Top. Dev. Biol. 60: 55-89.
8. Chen, T., Ueda, Y., Dodge, J.E., Wang, Z., and Li, E. 2003. Establishment and maintenance of genomic methylation patterns in mouse embryonic stem cells by Dnmt3a and Dnmt3b. Mol. Cell. Biol. 23: 5594-5605.
9. Cirio, M.C., Ratnam, S., Ding, F., Reinhart, B., Navara, C., and Chaillet, J.R. 2008. Preimplantation expression of the somatic form of Dnmt1 suggests a role in the inheritance of genomic imprints. BMC Dev. Biol. 8: 9. doi: 10.1186/1471-213X-8-9.
10. Constancia, M., Kelsey, G., and Reik, W. 2004. Resourceful imprinting. Nature 432: 53-57.
11. Dean, W., Santos, F., Stojkovic, M., Zakhartchenko, V., Walter, J., Wolf, E., and Reik, W. 2001. Conservation of methylation reprogramming in mammalian development: Aberrant reprogramming in cloned embryos. Proc. Natl. Acad. Sci. 98: 13734-13738.
12. Ding, F. and Chaillet, J.R. 2002. In vivo stabilization of the Dnmt1 (cytosine-5)-methyltransferase protein. Proc. Natl. Acad. Sci. 99: 14861-14866.
13. Edwards, C.A. and Ferguson-Smith, A.C. 2007. Mechanisms regulating imprinted genes in clusters. Curr. Opin. Cell Biol. 19: 281-289.
14. Esteve, P.O., Chin, H.G., Smallwood, A., Feehery, G.R., Gangisetty, O., Karpf, A.R., Carey, M.F., and Pradhan, S. 2006. Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes & Dev. 20: 3089-3103.
15. 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. (in press).
16. Gaudet, F., Rideout III, W.M., Meissner, A., Dausman, J., Leonhardt, H., and Jaenisch, R. 2004. Dnmt1 expression in preand postimplantation embryogenesis and the maintenance of IAP silencing. Mol. Cell. Biol. 24: 1640-1648.
17. Hajkova, P., Erhardt, S., Lane, N., Haaf, T., El-Maarri, O., Reik, W., Walter, J., and Surani, M.A. 2002. Epigenetic reprogramming in mouse primordial germ cells. Mech. Dev. 117: 15-23.
18. Hajkova, P., Ancelin, K., Waldmann, T., Lacoste, N., Lange, U.C., Cesari, F., Lee, C., Almouzni, G., Schneider, R., and Surani, M.A. 2008. Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 452: 877-881.
19. 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 maintenance of DNA methylation imprints during preimplantation development. Genes & Dev. (this issue), doi: 10.1101/gad.1667008.
20. Howell, C.Y., Bestor, T.H., Ding, F., Latham, K.E., Mertineit, C., Trasler, J.M., and Chaillet, J.R. 2001. Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell 104: 829-838.
21. Jackson, M., Krassowska, A., Gilbert, N., Chevassut, T., Forrester, L., Ansell, J., and Ramsahoye, B. 2004. Severe global DNA hypomethylation blocks differentiation and induces histone hyperacetylation in embryonic stem cells. Mol. Cell. Biol. 24: 8862-8871.
22. Kaneda, M., Okano, M., Hata, K., Sado, T., Tsujimoto, N., Li, E., and Sasaki, H. 2004. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 429: 900-903.
23. Kato, Y., Kaneda, M., Hata, K., Kumaki, K., Hisano, M., Kohara, Y., Okano, M., Li, E., Nozaki, M., and Sasaki, H. 2007. Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse. Hum. Mol. Genet. 16: 2272-2280.
24. Ko, Y.G., Nishino, K., Hattori, N., Arai, Y., Tanaka, S., and Shiota, K. 2005. Stage-by-stage change in DNA methylation status of Dnmt1 locus during mouse early development. J. Biol. Chem. 280: 9627-9634.
25. 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 methyltransferase 1. Dev. Biol. 313: 335-346.
26. Lane, N., Dean, W., Erhardt, S., Hajkova, P., Surani, A., Walter, J., and Reik, W. 2003. Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35: 88-93.
27. Lee, J., Inoue, K., Ono, R., Ogonuki, N., Kohda, T., Kaneko-Ishino, T., Ogura, A., and Ishino, F. 2002. Erasing genomic imprinting memory in mouse clone embryos produced from day 11.5 primordial germ cells. Development 129: 1807-1817.
28. Li, E., Beard, C., and Jaenisch, R. 1993. Role for DNA methylation in genomic imprinting. Nature 366: 362-365.
29. Li, J.Y., Pu, M.T., Hirasawa, R., Li, B.Z., Huang, Y.N., Zeng, R., Jing, N.H., Chen, T., Li, E., Sasaki, H., et al. 2007. Synergistic function of DNA methyltransferases Dnmt3a and Dnmt3b in the methylation of Oct4 and Nanog. Mol. Cell. Biol. 27: 8748-8759.
30. Myant, K. and Stancheva, I. 2008. LSH cooperates with DNA methyltransferases to repress transcription. Mol. Cell. Biol. 28: 215-226.
31. 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.
32. Oda, M., Yamagiwa, A., Yamamoto, S., Nakayama, T., Tsumura, A., Sasaki, H., Nakao, K., Li, E., and Okano, M. 2006. DNA methylation regulates long-range gene silencing of an X-linked homeobox gene cluster in a lineage-specific manner. Genes & Dev. 20: 3382-3394.
33. Okano, M., Bell, D.W., Haber, D.A., and Li, E. 1999. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99: 247-257.
34. 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.
35. Ratnam, S., Mertineit, C., Ding, F., Howell, C.Y., Clarke, H.J., Bestor, T.H., Chaillet, J.R., and Trasler, J.M. 2002. Dynamics of Dnmt1 methyltransferase expression and intracellular localization during oogenesis and preimplantation development. Dev. Biol. 245: 304-314.
36. Reik, W. 2007. Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447: 425-432.
37. Robertson, K.D. 2002. DNA methylation and chromatin - Unraveling the tangled web. Oncogene 21: 5361-5379.
38. Santos, F., Hendrich, B., Reik, W., and Dean, W. 2002. Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev. Biol. 241: 172-182.
39. 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.
40. Vassena, R., Dee Schramm, R., and Latham, K.E. 2005. Species-dependent expression patterns of DNA methyltransferase genes in mammalian oocytes and preimplantation embryos. Mol. Reprod. Dev. 72: 430-436.
41. Watanabe, D., Suetake, I., Tada, T., and Tajima, S. 2002. Stage-and cell-specific expression of Dnmt3a and Dnmt3b during embryogenesis. Mech. Dev. 118: 187-190.