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Evolutionary Epigenomic Analyses in Mammalian Early Embryos Reveal Species-specific Innovations and Conserved Principles of Imprinting

Overview
Journal Sci Adv
Specialties Biology
Science
Date 2021 Nov 24
PMID 34818044
Citations 26
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Abstract

While mouse remains the most popular model, the conservation of parental-to-embryonic epigenetic transition across mammals is poorly defined. Through analysis of oocytes and early embryos in human, bovine, porcine, rat, and mouse, we revealed remarkable species-specific innovations as no single animal model fully recapitulates the human epigenetic transition. In rodent oocytes, transcription-dependent DNA methylation allows methylation of maternal imprints but not intergenic paternal imprints. Unexpectedly, prevalent DNA hypermethylation, paralleled by H3K36me2/3, also occurs in nontranscribed regions in porcine and bovine oocytes, except for megabase-long “CpG continents (CGCs)” where imprinting control regions preferentially reside. Broad H3K4me3 and H3K27me3 domains exist in nonhuman oocytes, yet only rodent H3K27me3 survives beyond genome activation. Coincidently, regulatory elements preferentially evade H3K27me3 in rodent oocytes, and failure to do so causes aberrant embryonic gene repression. Hence, the diverse mammalian innovations of parental-to-embryonic transition center on a delicate “to-methylate-or-not” balance in establishing imprints while protecting other regulatory regions.

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References
1.
Moore T, Haig D . Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet. 1991; 7(2):45-9. DOI: 10.1016/0168-9525(91)90230-N. View

2.
Xiang Y, Zhang Y, Xu Q, Zhou C, Liu B, Du Z . Epigenomic analysis of gastrulation identifies a unique chromatin state for primed pluripotency. Nat Genet. 2019; 52(1):95-105. PMC: 7362285. DOI: 10.1038/s41588-019-0545-1. View

3.
Jambhekar A, Dhall A, Shi Y . Roles and regulation of histone methylation in animal development. Nat Rev Mol Cell Biol. 2019; 20(10):625-641. PMC: 6774358. DOI: 10.1038/s41580-019-0151-1. View

4.
Wang L, Zhang J, Duan J, Gao X, Zhu W, Lu X . Programming and inheritance of parental DNA methylomes in mammals. Cell. 2014; 157(4):979-991. PMC: 4096154. DOI: 10.1016/j.cell.2014.04.017. View

5.
Bhattacharya S, Workman J . Regulation of SETD2 stability is important for the fidelity of H3K36me3 deposition. Epigenetics Chromatin. 2020; 13(1):40. PMC: 7542105. DOI: 10.1186/s13072-020-00362-8. View