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Chapter 5 - DNA Is Not the Whole Story: Transgenerational Epigenesis and Imprinting

Published online by Cambridge University Press:  15 December 2022

By
Ashwini Balakrishnan  and
J. Richard Chaillet
Edited by
Stéphane Viville  and
Karen D. Sermon
Stéphane Viville
Affiliation:
Laboratoire de Génétique Médicale de Strasbourg and Laboratoire de diagnostic génétique, Strasbourg
Karen D. Sermon
Affiliation:
Reproduction and Genetics Research Group, Vrije Universiteit Brussel
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Summary

There are two types of genomic information accurately inherited or maintained following DNA replication: the entire genomic DNA sequence and epigenetic information in the form of patterns of CpG methylation on a subset of the genome. These DNA methylation patterns are crucially important for mammalian development, primarily because they regulate gene transcription. There are cyclical declines and increases in DNA methylation during gametogenesis and embryogenesis, and the oscillations in methylation occurring across generations must depend on de novo methylation and demethylation processes to rearrange the existing methylation patterns. Within any single reproductive cycle, changes in genomic methylation are the outcome of a linked sequence of active and passive processes that rearrange genomic methylation to generate epigenetic milestones, each with a defined future role. For example, genomic imprints are established during gametogenesis by de novo methylation to generate mature gametes with complete complements of paternal methylation imprints in sperm and maternal methylation imprints in oocytes. The establishment of a collective set of imprints within a sperm and an oocyte is an epigenetic milestone, whose purpose after sperm–oocyte fusion is to ensure monoallelic expression of imprinted genes during fetal development. We postulate that another essential epigenetic milestone is found in the blastocyst-stage embryo; this milestone is achieved at the generation, through the poorly understood process of epigenetic reprogramming, of pluripotent embryo stem cells, whose role is to contribute to the development of the conceptus. Primordial germ cells (PGCs), largely devoid of genomic methylation and poised to differentiate into gametes with sex-specific imprints, and adult stem cells, poised to differentiate into organs, would be other possible epigenetic milestones. The developmental locations of three fundamental milestones (gametes, blastocyst, and PGCs), and the epigenetic processes by which they are crafted, are depicted in Figure 5.1.

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Textbook of Human Reproductive Genetics , pp. 68 - 82
Publisher: Cambridge University Press
Print publication year: 2023

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References

Reinhart, B, Chaillet, JR. Genomic imprinting: cis-acting sequences and regional control. Int Rev Cytol 2005;243:173–213.CrossRefGoogle ScholarPubMed
Cattanach, BM, Kirk, M. Differential activity of maternally and paternally derived chromosome regions in mice. Nature 1985;315:496–8.Google Scholar
MouseBook: www.mousebook.org/catalog.php?catalog=imprintingGoogle Scholar
Chaillet, JR, Vogt, TF, Beier, DR, et al. Parental-specific methylation of an imprinted transgene is established during gametogenesis and progressively changes during embryogenesis. Cell 1991;66:77–83.Google Scholar
Hajkova, P, Erhardt, S, Lane, N, et al. Epigenetic reprogramming in mouse primordial germ cells. Mech Dev 2002;117:15–23.CrossRefGoogle ScholarPubMed
Kaneda, M, Okano, M, Hata, K, et al. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting. Nature 2004;429:900–3.CrossRefGoogle Scholar
Kato, Y, Kaneda, M, Hata, K, et al. 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 2007;16:2272–80.Google Scholar
Hata, K, Okano, M, Lei, H, et al. Dnmt3L cooperates with the Dnmt3 family of de novo DNA methyltransferases to establish maternal imprints in mice. Development 2002;129:1983–93.CrossRefGoogle ScholarPubMed
La Salle, S, Mertineit, C, Taketo, T, et al. Windows for sex-specific methylation marked by DNA methyltransferase expression profiles in mouse germ cells. Dev Biol 2004;268:403–15.Google Scholar
Kono, T, Obata, Y, Yoshimzu, T, et al. Epigenetic modifications during oocyte growth correlates with extended parthenogenetic development in the mouse. Nat Genet 1996;13:91–4.Google Scholar
Li, JYY, Lees-Murdock, DJ, Xu, GLL, et al. Timing of establishment of paternal methylation imprints in the mouse. Genomics 2004;84:952–60.Google Scholar
Lucifero, D, Mann, MR, Bartolomei, MS, et al. Gene-specific timing and epigenetic memory in oocyte imprinting. Hum Mol Genet 2004;13:839–49.CrossRefGoogle ScholarPubMed
Bourc’his, D, Xu, GL, Lin, CS, et al. Dnmt3L and the establishment of maternal genomic imprints. Science 2001;294:2536–9.Google Scholar
Bourc’his, D, Bestor, TH. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 2004;431:96–9.Google Scholar
Jia, D, Jurkowska, RZ, Zhang, X, et al. Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation. Nature 2007;449:248–51.Google Scholar
Ooi, SK, Qiu, C, Bernstein, E, et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 2007;448:714–17.Google Scholar
Cirio, MC, Ratnam, S, Ding, F, et al. Preimplantation expression of the somatic form of Dnmt1 suggests a role in the inheritance of genomic imprints. BMC Dev Biol 2008;25:8–9.Google Scholar
Howell, CY, Bestor, TH, Ding, F, et al. Genomic imprinting disrupted by a maternal effect mutation in the Dnmt1 gene. Cell 2001;104:829–38.Google Scholar
Reinhart, B, Paoloni-Giacobino, A, Chaillet, JR. Specific differentially methylated domain sequences direct the maintenance of methylation at imprinted genes. Mol Cell Biol 2006;26:8347–56.Google Scholar
Borowczyk, E, Mohan, KN, D’Aiuto, L, et al. Identification of a region of the DNMT1 methyltransferase that regulates the maintenance of genomic imprints. Proc Natl Acad Sci USA 2009;106(20):806–11.Google Scholar
Ideraabdullah, FY, Vigneau, S, Bartolomei, MS. Genomic imprinting mechanisms in mammals. Mutat Res 2008;647:77–85.Google Scholar
Singh, P, Cho, J, Tsai, SY, et al. Coordinated allele-specific histone acetylation at the differentially methylated regions of imprinted genes. Nucleic Acids Res 2010;38:7974–90.CrossRefGoogle ScholarPubMed
Sapountzi, V, Logan, IR, Robson, CN. Cellular functions of TIP60. Int J Biochem Cell Biol 2006;38:1496–509.Google Scholar
Mohan, NK, Ding, F, Chaillet, JR. Distinct roles of DMAP1 in mouse development. Mol Cell Biol 2011;31:1861–9.CrossRefGoogle ScholarPubMed
Paoloni-Giacobino, A, Chaillet, JR. Genomic imprinting and assisted reproduction. Reprod Health 2004;1:6.CrossRefGoogle ScholarPubMed
Tremblay, KD, Duran, KL, Bartolomei, MS. A 5′ 2-kilobase-pair region of the imprinted mouse H19 gene exhibits exclusive paternal methylation throughout development. Mol Cell Biol 1997;17:4322–9.Google Scholar
Saitou, M, Kagiwada, S, Kurimoto, K. Epigenetic reprogramming in mouse pre-implantation development and primordial germ cells. Development 2012;139:15–31.CrossRefGoogle ScholarPubMed
Lee, J, Inoue, K, Ono, R, et al. Erasing genomic imprinting memory in mouse clone embryos produced from Day 11.5 primordial germ cells. Development 2002;129:1807–17.Google Scholar

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