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Germ-cell specific eIF4E1b regulates maternal mRNA translation to ensure zygotic genome activation [Ribo-seq]

ABSTRACT: Translation of maternal mRNAs is detected before transcription of zygotic genes and is essential for mammalian embryo development. How certain maternal mRNAs are selected for translation instead of degradation and how this burst of translation affects zygotic genome activation remains unknown. Using gene-edited mice, we document that the oocyte-specific eukaryotic translation initiation factor 4E family member 1b (eIF4E1b) is the regulator of maternal mRNA expression that ensures subsequent reprogramming of the zygotic genome. In oocytes, eIF4E1b binds to transcripts encoding translation machinery proteins, chromatin remodelers and reprogramming factors to promote their translation in zygotes and protect them from degradation. The protein products are thought to establish an open chromatin landscape in one-cell zygotes to enable transcription of genes required for cleavage stage development. Our results define a program for rapid resetting of the zygotic epigenome that is regulated by maternal mRNA expression and provides new insights into the mammalian maternal-to-zygotic transition.

ORGANISM(S): Mus musculus

PROVIDER: GSE230019 | GEO | 2023/06/08

REPOSITORIES: GEO

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Germ cell-specific eIF4E1b regulates maternal mRNA translation to ensure zygotic genome activation

Project description:Translation of maternal mRNAs is detected before transcription of zygotic genes and is essential for mammalian embryo development. How certain maternal mRNAs are selected for translation instead of degradation and how this burst of translation affects zygotic genome activation remain unknown. Using gene-edited mice, we document that the oocyte-specific eukaryotic translation initiation factor 4E family member 1b (eIF4E1b) is the regulator of maternal mRNA expression that ensures subsequent reprogramming of the zygotic genome. In oocytes, eIF4E1b binds to transcripts encoding translation machinery proteins, chromatin remodelers, and reprogramming factors to promote their translation in zygotes and protect them from degradation. The protein products are thought to establish an open chromatin landscape in one-cell zygotes to enable transcription of genes required for cleavage stage development. Our results define a program for rapid resetting of the zygotic epigenome that is regulated by maternal mRNA expression and provide new insights into the mammalian maternal-to-zygotic transition. This SuperSeries is composed of the SubSeries listed below.

2023-06-07 | GSE180218 | GEO

Germ-cell specific eIF4E1b regulates maternal mRNA translation to ensure zygotic genome activation [NOMe-seq]

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2023-06-08 | GSE200685 | GEO

Germ-cell specific eIF4E1b regulates maternal mRNA translation to ensure zygotic genome activation [RNA-seq]

Project description:Translation of maternal mRNAs is detected before transcription of zygotic genes and is essential for mammalian embryo development. How certain maternal mRNAs are selected for translation instead of degradation and how this burst of translation affects zygotic genome activation remains unknown. Using gene-edited mice, we document that the oocyte-specific eukaryotic translation initiation factor 4E family member 1b (eIF4E1b) is the regulator of maternal mRNA expression that ensures subsequent reprogramming of the zygotic genome. In oocytes, eIF4E1b binds to transcripts encoding translation machinery proteins, chromatin remodelers and reprogramming factors to promote their translation in zygotes and protect them from degradation. The protein products are thought to establish an open chromatin landscape in one-cell zygotes to enable transcription of genes required for cleavage stage development. Our results define a program for rapid resetting of the zygotic epigenome that is regulated by maternal mRNA expression and provides new insights into the mammalian maternal-to-zygotic transition.

2023-06-08 | GSE180206 | GEO

Germ-cell specific eIF4E1b regulates maternal mRNA translation to ensure zygotic genome activation [RIP-seq]

Project description:Translation of maternal mRNAs is detected before transcription of zygotic genes and is essential for mammalian embryo development. How certain maternal mRNAs are selected for translation instead of degradation and how this burst of translation affects zygotic genome activation remains unknown. Using gene-edited mice, we document that the oocyte-specific eukaryotic translation initiation factor 4E family member 1b (eIF4E1b) is the regulator of maternal mRNA expression that ensures subsequent reprogramming of the zygotic genome. In oocytes, eIF4E1b binds to transcripts encoding translation machinery proteins, chromatin remodelers and reprogramming factors to promote their translation in zygotes and protect them from degradation. The protein products are thought to establish an open chromatin landscape in one-cell zygotes to enable transcription of genes required for cleavage stage development. Our results define a program for rapid resetting of the zygotic epigenome that is regulated by maternal mRNA expression and provides new insights into the mammalian maternal-to-zygotic transition.

2023-06-08 | GSE180217 | GEO

Protein expression profiling in eggs and embryos from control and Eif4e1b knockout female mice.

Project description:We have identified eukaryotic translation initiation factor 4E family member 1B (Eif4e1b) as a regulator of maternal RNA translation, whose maternal deletion leads to 2-cell arrest phenotype in mouse embryos. eIF4E1b protein binds mRNA selectively in oocytes and controls their translation in early embryos. We aim to profile the global changes in protein expression in metaphase II (MII) eggs and zygotes collected from control or Eif4e1b knockout female mice. An encapsulated proteomic-sample processing protocol is used to perform this low-input mass spectrometry to quantify proteomic changes (Kulak et al. 2014/PMID 24497582).

2023-06-12 | PXD041583 | Pride

eIF4E1b is a non-canonical eIF4E required for maternal mRNA dormancy

Project description:Maternal mRNAs are essential for protein synthesis during oogenesis and early embryogenesis. To adapt translation to specific needs during development, maternal mRNAs are translationally repressed by shortening the polyA tails. While mRNA deadenylation is associated with decapping and degradation in somatic cells, maternal mRNAs with short polyA tails are stable. Here we report an essential role for the germline-specific paralog of the mRNA cap-binding factor eIF4E, known as eIF4E1b, in the storage and repression of maternal mRNAs with short polyA tails. eIF4E1b binds to the mRNA cap and is targeted to ribonucleoprotein complexes through its direct interaction with eIF4ENIF1/4E-T. In early embryos, eIF4E1b binds to a specific set of translationally repressed mRNAs with short or no polyA tails, such as histone mRNAs, which are translated later on during embryogenesis. Consistent with an important role in maternal mRNA dormancy, mutation of eIF4E1b in zebrafish impairs female germline development. Understanding the mechanism and function of eIF4E1B provides new insights into fundamental post-transcriptional regulatory principles governing early vertebrate development.

2024-04-12 | PXD042434 | Pride

Profiling and functional characterization of maternal mRNA translation in mouse maternal-to-zygotic transition

Project description:Translational regulation plays an important role in gene expression and function. Although the transcriptional dynamics of mouse pre-implantation embryos has been well characterized, the global mRNA translation landscape and the master regulators of zygotic genome activation (ZGA) remain unknown. Here, by developing and applying a low-input ribosome profiling (LiRibo-seq) technique, we profiled the mRNA translation landscape in mouse pre-implantation embryos and revealed the translational dynamics during mouse pre-implantation development. We identified a dramatic translational transition from MII oocytes to zygotes, and demonstrated that active translation of maternal mRNAs is essential for maternal-to-zygotic transition (MZT). We further showed that two maternal factors, Smarcd2 and Cyclin T2, whose translation is activated in zygotes, are required for chromatin reprogramming and ZGA, respectively. Our study thus not only filled in a knowledge gap on translational regulation during mammalian pre-implantation development, but also revealed new insights into the critical function of maternal mRNA translation in MZT.

2021-11-28 | GSE169632 | GEO

Identification of co-factors of eIF4E1b protein in mouse ovary.

Project description:We have identified eukaryotic translation initiation factor 4E family member 1B (Eif4e1b) as a regulator of maternal RNA translation, whose maternal deletion leads to 2-cell arrest phenotype in mouse embryos. eIF4E1b protein binds mRNA selectively in oocytes and controls their translation in early embryos. eIF4E1b expresses specifically in mouse ovary and we have generated a knock-in mouse line in which HA tag is conjugated to the C terminus of eIF4E1b. We aim to identify eIF4E1b co-factors using mass spectrometry after anit-HA immunoprecipitation (IP) using mouse ovaries.

2023-06-12 | PXD041622 | Pride

Selective Translation of Maternal mRNA by eIF4E1B Controls Oocyte to Embryo Transition

Project description:To identify mRNAs loaded onto eIF4E1B and eIF4E, LACE-seq was performed using eIF4E1B and eIF4E immunoprecipitated mRNAs from mouse fully grown oocytes RNA co-precipitated with eIF4E1B and eIF4E differed from the control RNA enriched by the control IgG rabbit serum antibody.

2023-02-21 | GSE213866 | GEO

Reading and writing of mRNA m6A modification orchestrate mouse maternal-to-zygotic transition

Project description:Background: Maternal and zygotic mRNAs play critical roles in maternal-to-zygotic transition (MZT) stage and N6-methyladenosine (m6A) has been proven as an important RNA metabolism regulation system. However, the dynamic profiles of m6A modification during mammalian MZT and its potential functions remain largely unknown. Results: Here we utilized m6A-seq, low-input RNA-seq, LiRibo-seq and low-input proteomic analysis to examine the mRNA regulation dynamics during mouse MZT. We found that m6A could be inherited from maternal origin or de novo added after fertilization. Interestingly, we observed the de novo m6A modification on mRNA during zygotic genome activation (ZGA), especially at major ZGA. Further analysis showed that m6A modification on maternal mRNAs not only correlates with mRNA degradation after fertilization, but also maintains the stability of a small group of mRNAs thereby promoting their translation after fertilization. Using CRISPR-Cas13d mediated RNA editing, we systemically evaluated the functions of ten m6A regulators and identified Ythdc1 and Ythdf2 as key m6A readers for mouse preimplantation development. By combining low-input RNA-seq, RNA immunoprecipitation (RIP) and qRT-PCR, we uncovered and verified that Ythdc1 can associate with a small group of m6A-tagged mRNAs and participate in their mRNA stability regulation. Conclusions: Our integrated multi-omic analysis links m6A modification to the diverse fates of maternal and zygotic mRNAs and establishes a key role of m6A mediated RNA metabolism in mammalian MZT.

2023-03-28 | GSE228201 | GEO

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