Maternal RNF114-mediated target substrate degradation regulates zygotic genome activation in mouse embryos

Zhou, Shuai; Guo, Yueshuai; Sun, Haifeng; Liu, Lu; Yao, Liping; Liu, Chao; He, Yuanlin; Cao, Shanren; Zhou, Cheng; Li, Mingrui; Cao, Yumeng; Wang, Congjing; Lu, Qiao; Li, Wei; Guo, Xuejiang; Huo, Ran

doi:10.1242/dev.199426

Cited by 11 publications

(9 citation statements)

References 68 publications

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“…These developmental stages correspond to the minor and major EGA phases in porcine embryos, which suggests these genes may be involved in the regulation of OET in pigs. In support of this are findings from previous studies in other species, for example, RNF114 participates in the regulation of EGA in mouse embryos by ubiquitinating the TGF-beta activated kinase 1 and MAP3K7-binding protein 1 (TAB1) [ 20 ], and the CBX5 [ 33 ], targeting them to degradation. TAB1 degradation activates the NF-kB pathway, which promotes maternal mRNA clearance in mouse embryos [ 20 ], while CBX5 degradation allows gene transcription through its interaction with dimethylated (H3K9me2) and trimethylated (H3K9me3) histone H3 lysine 9, which represses gene transcription [ 20 , 33 ].…”

Section: Discussionsupporting

confidence: 79%

“…In support of this are findings from previous studies in other species, for example, RNF114 participates in the regulation of EGA in mouse embryos by ubiquitinating the TGF-beta activated kinase 1 and MAP3K7-binding protein 1 (TAB1) [ 20 ], and the CBX5 [ 33 ], targeting them to degradation. TAB1 degradation activates the NF-kB pathway, which promotes maternal mRNA clearance in mouse embryos [ 20 ], while CBX5 degradation allows gene transcription through its interaction with dimethylated (H3K9me2) and trimethylated (H3K9me3) histone H3 lysine 9, which represses gene transcription [ 20 , 33 ]. On the other hand, DCAF13 was shown to negatively regulate the histone lysine methyltransferase SUV39H1, which leads to a decrease of H3K9me3 in mouse embryos [ 34 ].…”

Section: Discussionsupporting

confidence: 79%

See 1 more Smart Citation

DNA Damage Induction Alters the Expression of Ubiquitin and SUMO Regulators in Preimplantation Stage Pig Embryos

Silva

Glanzner

Currin

et al. 2022

IJMS

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DNA damage in early-stage embryos impacts development and is a risk factor for segregation of altered genomes. DNA damage response (DDR) encompasses a sophisticated network of proteins involved in sensing, signaling, and repairing damage. DDR is regulated by reversible post-translational modifications including acetylation, methylation, phosphorylation, ubiquitylation, and SUMOylation. While important regulators of these processes have been characterized in somatic cells, their roles in early-stage embryos remain broadly unknown. The objective of this study was to explore how ubiquitylation and SUMOylation are involved in the regulation of early development in porcine embryos by assessing the mRNA profile of genes encoding ubiquitination (UBs), deubiquitination (DUBs), SUMOylation (SUMOs) or deSUMOylation (deSUMOs) enzymes in oocyte and embryos at different stages of development, and to evaluate if the induction of DNA damage at different stages of embryo development would alter the mRNA abundance of these genes. Pig embryos were produced by in vitro fertilization and DNA damage was induced by ultraviolet (UV) light exposure for 10 s on days 2, 4 or 7 of development. The relative mRNA abundance of most UBs, DUBs, SUMOs, and deSUMOs was higher in oocytes and early-stage embryos than in blastocysts. Transcript levels for UBs (RNF20, RNF40, RNF114, RNF169, CUL5, DCAF2, DECAF13, and DDB1), DUBs (USP16), and SUMOs (CBX4, UBA2 and UBC9), were upregulated in early-stage embryos (D2 and/or D4) compared to oocytes and blastocysts. In response to UV-induced DNA damage, transcript levels of several UBs, DUBs, SUMOs, and deSUMOs decreased in D2 and D4 embryos, but increased in blastocysts. These findings revealed that transcript levels of genes encoding for important UBs, DUBs, SUMOs, and deSUMOs are regulated during early embryo development and are modulated in response to induced DNA damage. This study has also identified candidate genes controlling post-translational modifications that may have relevant roles in the regulation of normal embryo development, repair of damaged DNA, and preservation of genome stability in the pig embryo.

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Section: Discussionsupporting

confidence: 79%

Section: Discussionsupporting

confidence: 79%

DNA Damage Induction Alters the Expression of Ubiquitin and SUMO Regulators in Preimplantation Stage Pig Embryos

Silva

Glanzner

Currin

et al. 2022

IJMS

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“…Given that a hallmark feature of a competent oocyte is chromatin condensation, the surprisingly highly selective translation of these genes in oocytes (both GV and MII) and the likely role of the translated proteins in maintaining the repressive heterochromatic state suggest that, in combination, these genes may have important function in the epigenetic control of bovine oocyte competence. Degradation of transcripts including SUV39H1 and TAB1 (Figure 4C) also have shown their essential roles in the maternal to zygotic transition (26, 27) and bovine preimplantation development (28–30), respectively. On the other hand, the top ranked up-regulated polysome-occupied transcripts across developmental stages is RAB17 (Figure 4C), which belongs to a subfamily of small GTPases, plays an important role in the regulation of membrane trafficking (31).…”

Section: Resultsmentioning

confidence: 90%

High-resolution Ribosome Profiling Reveals Translational Selectivity for Transcripts in Bovine Preimplantation Embryo Development

Jiang¹,

Zhu²,

Tong

et al. 2022

Preprint

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High resolution ribosome fractionation and low-input ribosome profiling of bovine oocytes and preimplantation embryos has enabled us to define the translational landscapes of early embryo development at an unprecedented level. We analyzed the transcriptome, polysome- and non-polysome-bound RNA profiles of bovine oocytes (GV and MII stage) and early embryos at 2-, 8-cell, morula, and blastocyst stage, and revealed four modes of translational selectivity: i. selective translation of non-abundant mRNAs, ii. active, but modest translation of a selection of highly expressed mRNAs, iii. translationally suppressed abundant to moderately abundant mRNAs, and iv. mRNAs associated specifically with monosomes. A strong translational selection of low abundance mRNAs encoding protein components involved in metabolic pathways and lysosome was found throughout bovine oocyte and preimplantation development. In particular, genes encoding components involved in mitochondrial function were prioritized for translation. Notably, transcripts encoding proteins regulating chromatin modifications selectively translated in oocytes. We found that the translational dynamics largely reflects transcriptional profiles in oocytes and 2-cell embryos, but observed marked shift in translational control in 8-cell embryos associated with the main phase of embryonic genome activation. Subsequently, transcription and translation become better synchronized in morulae and blastocysts. Together, these data reveal a unique spatiotemporal translational regulation that accompanies bovine preimplantation development.

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“…Recently, another E3 ligase RNF114 is also reported to be highly expressed in oocytes and early embryos 179 . The knockout of Rnf114 results in abnormal protein metabolism in oocytes, and most maternal KO embryos fail to develop beyond the 2‐cell stage with major ZGA defects 179,180 . In line with this, the knockdown of some RNF114 substrates, Tab1 or Cbx5 , can partially rescue the abnormal development of maternal Rnf114 KO embryos 179,180 .…”

Section: Non‐histone Protein Post‐translational Modifications In Mztmentioning

confidence: 85%

Epigenetic reprogramming during the maternal‐to‐zygotic transition

Chen

Wang

Guo

et al. 2023

MedComm

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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.

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Maternal RNF114-mediated target substrate degradation regulates zygotic genome activation in mouse embryos

Cited by 11 publications

References 68 publications

DNA Damage Induction Alters the Expression of Ubiquitin and SUMO Regulators in Preimplantation Stage Pig Embryos

DNA Damage Induction Alters the Expression of Ubiquitin and SUMO Regulators in Preimplantation Stage Pig Embryos

High-resolution Ribosome Profiling Reveals Translational Selectivity for Transcripts in Bovine Preimplantation Embryo Development

Epigenetic reprogramming during the maternal‐to‐zygotic transition

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