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Differential Demethylation of Paternal and Maternal Genomes in the Preimplantation Mouse Embryo: Implications for Mammalian Development

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Book cover Chromosomes Today

Abstract

Higher eukaryotes are endowed with a diploid somatic genome. At fertilization the paternal and maternal genomes are combined, forming the new diploid organism. Nuclear transfer experiments in the 1980s (McGrath and Solter, 1984; Surani et al., 1986) demonstrated for the first time the functional non-equivalence of the two parental genomes in mammals. In contrast to many lower vertebrates, mammalian uniparental embryos cannot develop beyond mid-gestation. Androgenetic embryos, with two paternal genomes, are usually very stage-retarded but often have well developed mural trophoblast and yolk sac. Gynogenetic embryos, with two maternal genomes, can develop relatively normally to mid-term but are small and have very restricted trophoblast and yolk sac. In both cases there is no normal placental development. Because of opposing patterns of gene expression from maternal and paternal alleles of imprinted genes (Fundele and Surani, 1994; Tilghman, 1999), normal mammalian development requires the participation of both a maternal and a paternal genome. Genomic imprinting is thought to be a by-product of the unique fetal-maternal relationship in mammals to control the different parental interests on embryo development. Consistent with the parental conflict hypothesis (Moore and Haig, 1991), many paternally expressed genes enhance fetal growth, whereas maternally expressed genes inhibit growth.

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References

  • Adenot PG, Mercier Y, Renard J-P, Thompson EM (1997). Differential H4 acetylation of paternal and maternal chromatin precedes DNA replication and differential transcriptional activity in pronuclei of 1-cell mouse embryos. Development 124: 4, 615–4, 625.

    Google Scholar 

  • Aoki F, Worrad DM, Schultz RM (1997). Regulation of transcriptional activity during the first and second cell cycles in the preimplantation mouse embryo. Dev Biol 181: 296–307.

    Article  PubMed  CAS  Google Scholar 

  • Balhorn R (1982). A model for the structure of chromatin in mammalian sperm. J Cell Biol 93: 298–305.

    Article  PubMed  CAS  Google Scholar 

  • Barton SC, Surani MA (1993). Manipulations of genetic constitution by nuclear transplantation. Meth Enzymol 225: 732–744.

    Article  PubMed  CAS  Google Scholar 

  • Bouniol-Baly C, Nguyen E, Besombes D, Debey P (1997). Dynamic organization of DNA replication in one-cell mouse embryos: relationship to transcriptional activation. Exp Cell Res 236: 201–211.

    Article  PubMed  CAS  Google Scholar 

  • Brannan CI, Bartolomei MS (1999). Mechanisms of genomic imprinting. Curr Opin Genet Dev 9: 164–170.

    Article  PubMed  CAS  Google Scholar 

  • Cardoso MC, Leonhardt H (1999). DNA methyltransferase is actively retained in the cytoplasm during early development. J Cell Biol 147: 25–32.

    Article  PubMed  CAS  Google Scholar 

  • Constancia M, Pickard P, Kelsey G, Reik W (1998). Imprinting mechanisms. Genome Res 8: 881–900.

    PubMed  CAS  Google Scholar 

  • El-Maarri O, Buiting K, Peery EG, Kroisel PM, Balaban B, Wagner K, Urman B, Heyd J, Lich C ,Brannan CI, Walter J, Horsthemke B (2001). Maternal methylation imprints on human chromosome 15 are established during or after fertilization. Nature Genet 27: 341–344.

    Article  PubMed  CAS  Google Scholar 

  • Fundele R, Surani MA (1994). Experimental embryological analysis of genetic imprinting in mouse development. Dev Genet 15: 515–522.

    Article  PubMed  CAS  Google Scholar 

  • Haaf T (2001). The battle of the sexes after fertilization: behaviour of paternal and maternal chromosomes in the early mammalian embryo. Chrom Res 9: 263–271.

    Article  PubMed  CAS  Google Scholar 

  • Howlett SK, Reik W (1991). Methylation levels of maternal and paternal genomes during preimplantation development. Development 113: 119–127.

    PubMed  CAS  Google Scholar 

  • Hsieh CL (2000). Dynamics of DNA methylation pattern. Curr Opin Genet Dev 10: 224–228. Jenuwein T, Allis CD (2001). Translating the histone code. Science 293: 1,074–1, 080.

    Google Scholar 

  • Kang Y-K, Koo D-B, Park J-S, Choi Y-H, Chung A-S, Lee K-K, Han Y-M (2001). Aberrant methylation of donor genome in cloned bovine embryos. Nat Genet 28: 173–177.

    Article  PubMed  CAS  Google Scholar 

  • Li E, Bestor TH, Jaenisch R (1992). Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69: 915–926.

    Article  PubMed  CAS  Google Scholar 

  • Mayer W, Smith A, Fundele R, Haaf T (2000a). Spatial separation of parental genomes in preimplantation mouse embryos. J Cell Biol 148: 629–634.

    Article  PubMed  CAS  Google Scholar 

  • Mayer W, Niveleau A, Walter J, Fundele R, Haaf T (2000b). Active demethylation of the zygotic paternal genome. Nature 403: 501–502.

    Article  PubMed  CAS  Google Scholar 

  • McGrath J, Solter D (1984). Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37: 179–183.

    Article  PubMed  CAS  Google Scholar 

  • Monk M, Boubelik M, Lehnert S (1987). Temporal and regional changes in DNA methylation in the embryonic, extraembryonic and germ cell lineages during mouse embryo development. Development 99: 371–382.

    PubMed  CAS  Google Scholar 

  • Moore T, Haig D (1991). Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet 7: 45–49.

    PubMed  CAS  Google Scholar 

  • Ng HH, Bird A (1999). DNA methylation and chromatin modification. Curr Opin Genet Dev 9: 158–163.

    Article  PubMed  CAS  Google Scholar 

  • Nonchev S, Tsanev R (1990). Protamine-hi stone replacement and DNA replication in the male pronucleus. Mol Reprod Dev 25: 72–76.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Olek A, Walter J (1998). The pre-implantation ontogeny of the H19 methylation imprint. Nat Genet 17: 275–276.

    Article  Google Scholar 

  • Oswald J, Engemann S, Lane N, Mayer W, Olek A, Fundele R, Dean W, Reik W, Walter J (2000). Active demethylation of the paternal genome in the mouse zygote. Curr Biol 10: 475–478.

    Article  PubMed  CAS  Google Scholar 

  • Perreault SD (1992). Chromatin remodeling in mammalian zygotes. Mut Res 296: 43–55. Razin A, Shemer R (1995). DNA methylation in early development. Hum Mol Genet 4:1, 751–1, 755.

    Google Scholar 

  • Reik W, Walter J (1998). Imprinting mechanisms in mammals. Curr Opin Genet Dev 8: 154–164.

    Article  PubMed  CAS  Google Scholar 

  • Reik W, Walter J (2001). Evolution of imprinting mechanisms: the battle of the sexes begins in the zygote. Nat Genet 27: 255–256.

    Article  PubMed  CAS  Google Scholar 

  • Rodman TC, Pruslin FH, Hoffmann HP, Allfrey VG (1981). Turnover of basic chromosomal proteins in fertilized eggs: a cytoimmunochemical study of events in vivo. J Cell Biol 90: 351–361.

    Article  CAS  Google Scholar 

  • Rougier D, Bourc’his D, Gomes DM, Niveleau A, Plachot M, Pàldi A, Viegas-Péquignot E (1998). Chromosome methylation patterns during mammalian development. Genes Dev 12:2, 108–2, 113.

    Google Scholar 

  • Sanford JP, Clark HJ, Chapman VM, Rossant J (1987). Differences in DNA methylation during oogenesis and spermatogenesis and their persistence during early embryogenesis in the mouse. Genes Dev 1: 1, 039–1, 046.

    Google Scholar 

  • Surani MAH, Barton SC, Norris ML (1986). Nuclear transplantation in the mouse: heritable differences between parental genomes after activation of the embryonic genome. Cell 45: 127–136.

    Article  PubMed  CAS  Google Scholar 

  • Tilghman SM (1999). The sins of the fathers and mothers: genomic imprinting in mammalian development. Cell 96: 185–193.

    Article  PubMed  CAS  Google Scholar 

  • Yoder JA, Walsh CP, Bestor TH (1997). Cytosine methylation and the ecology of intragenomic parasites. Trends Genet 13: 335–340.

    Article  PubMed  CAS  Google Scholar 

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© 2004 Springer Science+Business Media Dordrecht

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Haaf, T., Shi, W., Fundele, R., Arney, K.L., Surani, M.A., Barton, S.C. (2004). Differential Demethylation of Paternal and Maternal Genomes in the Preimplantation Mouse Embryo: Implications for Mammalian Development. In: Schmid, M., Nanda, I. (eds) Chromosomes Today. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-1033-6_19

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  • DOI: https://doi.org/10.1007/978-94-017-1033-6_19

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-90-481-5855-3

  • Online ISBN: 978-94-017-1033-6

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