Epigenetic reprogramming during the maternal‐to‐zygotic transition

Abstract

After fertilization, sperm and oocyte fused and gave rise to a zygote which is the beginning of a new life. Then the embryonic development is monitored and regulated precisely from the transition of oocyte to the embryo at the early stage of embryogenesis, and this process is termed maternal‐to‐zygotic transition (MZT). MZT involves two major events that are maternal components degradation and zygotic genome activation. The epigenetic reprogramming plays crucial roles in regulating the process of MZT and supervising the normal development of early development of embryos. In recent years, benefited from the rapid development of low‐input epigenome profiling technologies, new epigenetic modifications are found to be reprogrammed dramatically and may play different roles during MZT whose dysregulation will cause an abnormal development of embryos even abortion at various stages. In this review, we summarized and discussed the important novel findings on epigenetic reprogramming and the underlying molecular mechanisms regulating MZT in mammalian embryos. Our work provided comprehensive and detailed references for the in deep understanding of epigenetic regulatory network in this key biological process and also shed light on the critical roles for epigenetic reprogramming on embryonic failure during artificial reproductive technology and nature fertilization.

High estrogen during ovarian stimulation induced loss of maternal imprinted methylation that is essential for placental development via overexpression of TET2 in mouse oocytes

“…Prior research indicates that in the zygote, the paternal genome undergoes active demethylation, whereas the maternal genome is subject to passive demethylation through DNA replication during the cleavage stage. Active demethylation of the male pronucleus in mouse zygotes is mediated by Tet3 [ 37 – 39 ]. This could explain why an increase in TET2 levels in the oocyte-sperm (OS) zygote does not influence DNA methylation within the male pronucleus.…”

A maternal-effectPadi6variant causes nuclear and cytoplasmic abnormalities in oocytes, as well as failure of epigenetic reprogramming and zygotic genome activation in embryos

“…After fertilization, the zygotic genome is inert, and mRNAs derived from the oocyte are translated to direct embryo development up to the two-cell stage ( Chen et al 2023 ). Oocyte transcripts are progressively decayed through either maternal (Mat-decay) and zygotic (Z-decay) pathways ( Jiang and Fan 2022 ; Chen et al 2023 ).…”

“…After fertilization, the zygotic genome is inert, and mRNAs derived from the oocyte are translated to direct embryo development up to the two-cell stage ( Chen et al 2023 ). Oocyte transcripts are progressively decayed through either maternal (Mat-decay) and zygotic (Z-decay) pathways ( Jiang and Fan 2022 ; Chen et al 2023 ). In particular, the Z-decay pathway involves the polyA-binding proteins PABPC1 and PABPN1, both of which were found to be down-regulated at the transcriptional level in Padi6 MatP620A/+ embryos, suggesting that the up-regulation of Mat-decay genes is a consequence of the ZGA failure or developmental delay of the mutant embryos.…”

A maternal-effectPadi6variant results in abnormal nuclear localization of DNMT1 and failure of epigenetic reprogramming and zygotic genome activation in mouse embryos

“…After fertilization, the zygotic genome is inert and mRNAs derived from the oocyte are translated to direct embryo development up to the 2-cell stage (Chen et al 2023). Oocyte transcripts are progressively decayed through either maternal (M-decay) and zygotic (Z-decay) pathways (Jiang and Fan 2022; Chen et al 2023).…”

“…After fertilization, the zygotic genome is inert and mRNAs derived from the oocyte are translated to direct embryo development up to the 2-cell stage (Chen et al 2023). Oocyte transcripts are progressively decayed through either maternal (M-decay) and zygotic (Z-decay) pathways (Jiang and Fan 2022; Chen et al 2023). In particular, the Z-decay pathway involves the polyA-binding proteins PABPC1 and PABPN1, both of which were found down-regulated at the transcriptional level in Padi6 MatP620A/+ embryos, suggesting that the up-regulation of Mat-decay genes is a consequence of the ZGA failure.…”