Minor zygotic gene activation is essential for mouse preimplantation development

Abe, Ken‐ichiro; Funaya, Satoshi; Tsukioka, Dai; Kawamura, Machika; Suzuki, Yutaka; Suzuki, Masataka; Schultz, Richard M.; Aoki, Fugaku

doi:10.1073/pnas.1804309115

Cited by 155 publications

(141 citation statements)

References 54 publications

(62 reference statements)

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“…By comparing the overlapped genes under different development stages, it was suggested that ZGA initiates during one-cell stage, bursts during 2-cell stage and hit the peak during 4-cell stage (Figure 2E). This conclusion is consistent with Abe et al (2018). They concluded that ZGA in mouse initiates at the mid-one-cell stage (minor ZGA) and is dramatically activated after 2-cell stage (major ZGA).…”

Section: Analysis Of Degs In Consecutive Developmental Stages Of Preisupporting

confidence: 79%

“…ZGA is essential for replacing the degraded maternal transcripts with zygotic transcripts (Yan et al, 2013). In mouse embryos, major ZGA process reportedly occurs at the 2-cell and 4-cell stages (Abe et al, 2018). The greatest DEGs number between 2-cell and zygote compared with other consecutive stages during preimplantation development was detected ( Figure 1E).…”

Section: Analysis Of Degs In Consecutive Developmental Stages Of Preimentioning

confidence: 93%

“…During ZGA process of mouse embryos development, lots of zygotic genes are activated and maternal genes have not been degraded thoroughly. Given that 2-cell stage is major start of ZGA in mouse (Abe et al, 2018), the fact that the maximum number of protein-coding genes was observed in the 2-cell stage is reasonable.…”

Section: The Global Outlook Of Degs and Das During Preimplantation Dementioning

confidence: 96%

“…If minor ZGA was inhibited transiently, most of embryos were arrested at the 2-cell stage. Thus, minor ZGA is crucial for the maternal-to-zygotic transition (Abe et al, 2018).…”

Section: Analysis Of Degs In Consecutive Developmental Stages Of Preimentioning

confidence: 99%

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Dynamic Alternative Splicing During Mouse Preimplantation Embryo Development

Xing

Yang

Liu

et al. 2020

Front. Bioeng. Biotechnol.

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The mechanism of alternative pre-mRNA splicing (AS) during preimplantation development is largely unknown. In order to capture the dynamic changes of AS occurring during embryogenesis, we carried out bioinformatics analysis based on scRNA-seq data over the time-course preimplantation development in mouse. We detected numerous previously-unreported differentially expressed genes at specific developmental stages and investigated the nature of AS at both minor and major zygotic genome activation (ZGA). The AS and differential AS atlas over preimplantation development were established. The differentially alternatively spliced genes (DASGs) are likely to be key splicing factors (SFs) during preimplantation development. We also demonstrated that there is a regulatory cascade of AS events in which some key SFs are regulated by differentially AS of their own gene transcripts. Moreover, 212 isoform switches (ISs) during preimplantation development were detected, which may be critical for decoding the mechanism of early embryogenesis. Importantly, we uncovered that zygotic AS activation (ZASA) is in conformity with ZGA and revealed that AS is coupled with transcription during preimplantation development. Our results may provide a deeper insight into the regulation of early embryogenesis.

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Section: Analysis Of Degs In Consecutive Developmental Stages Of Preisupporting

confidence: 79%

Section: Analysis Of Degs In Consecutive Developmental Stages Of Preimentioning

confidence: 93%

Section: The Global Outlook Of Degs and Das During Preimplantation Dementioning

confidence: 96%

“…If minor ZGA was inhibited transiently, most of embryos were arrested at the 2-cell stage. Thus, minor ZGA is crucial for the maternal-to-zygotic transition (Abe et al, 2018).…”

Section: Analysis Of Degs In Consecutive Developmental Stages Of Preimentioning

confidence: 99%

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Dynamic Alternative Splicing During Mouse Preimplantation Embryo Development

Xing

Yang

Liu

et al. 2020

Front. Bioeng. Biotechnol.

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“…Past studies investigated the effects of oocyte cryopreservation on whole oocyte transcriptomes [34] [35,36] or selected genes [37][38][39][40] and reported significantly altered mRNA levels. Since the MII oocytes are transcriptionally silent [41,42] and major embryonic genome activation occurs at the two-cell stage and four-to eight-cell stage in the mouse [43,44] and human [45], respectively, the published studies do not address how oocytes cryopreservation affect gene expression after embryonic genome activation (EGA) as a way of assessing long-term effects of oocyte cryopreservation.…”

mentioning

confidence: 99%

Probing lasting cryoinjuries to oocyte-embryo transcriptome

Eroglu¹,

Szurek²,

Schall³

et al. 2020

PLoS ONE

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Clinical applications of oocytes cryopreservation include preservation of future fertility of young cancer patients, substitution of embryo freezing to avoid associated legal and ethical issues, and delaying childbearing years. While the outcome of oocyte cryopreservation has recently been improved, currently used vitrification method still suffer from increased biosafety risk and handling issues while slow freezing techniques yield overall low success. Understanding better the mechanism of cryopreservation-induced injuries may lead to development of more reliable and safe methods for oocyte cryopreservation. Using the mouse model, a microarray study was conducted on oocyte cryopreservation to identify cryoinjuries to transcriptionally active genome. To this end, metaphase II (MII) oocytes were subjected to standard slow freezing, and then analyzed at the four-cell stage after embryonic genome activation. Non-frozen four-cell embryos served as controls. Differentially expressed genes were identified and validated using RT-PCR. Embryos produced from the cryopreserved oocytes displayed 200 upregulated and 105 downregulated genes, associated with the regulation of mitochondrial function, protein ubiquitination and maintenance, cellular response to stress and oxidative states, fatty acid and lipid regulation/metabolism, and cell cycle maintenance. These findings reveal previously unrecognized effects of standard slow oocyte freezing on embryonic gene expression, which can be used to guide improvement of oocyte cryopreservation methods.Editor: Joël R. Drevet, chemical toxicity of cryoprotective agents (CPA) [5], osmotic stress [6], disruption of cytoskeleton and spindle microtubules [7,8], premature exocytosis of cortical granules and zona hardening [9, 10], parthenogenetic activation [11][12][13], and polyploidy [7,14,15]. Through intensive efforts to mitigate these cryoinjuries, increasingly encouraging results have been reported with human oocytes after both slow-freezing [16][17][18][19][20][21] and vitrification [22][23][24][25]. A vitrification approach requiring minimum sample volume (less than 1 μl), low permeating CPA concentrations (~30%), and extremely fast cooling/warming rates yielded clinically acceptable results [26][27][28] and is currently the preferred approach for human oocyte cryopreservation. However, the minimal sample volume, low CPA concentrations, and direct contact with LN 2 required to achieve extremely fast cooling/warming rates make this approach prone to devitrification, handling and reproducibility issues, and biosafety risk for contaminating cryopreserved samples with different pathogens [29][30][31][32]. In contrast, slow-freezing methods are usually not associated with a biosafety risk; however, clinical success rates obtained with slowly frozen human oocytes remain lower than those obtained with the vitrification method [19,21,25]. Understanding better the mechanism of cryopreservation-induced injuries may help overcome the shortcomings of the current approaches, and thereby lead to ...

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H3K4 Methylation Promotes Expression of Mitochondrial Dynamics Regulators to Ensure Oocyte Quality in Mice

et al. 2023

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Significantly decreased H3K4 methylation in oocytes from aged mice indicates the important roles of H3K4 methylation in female reproduction. However, how H3K4 methylation regulates oocyte development remains largely unexplored. In this study, it is demonstrated that oocyte‐specific expression of dominant negative mutant H3.3‐K4M led to a decrease of the level of H3K4 methylation in mouse oocytes, resulting in reduced transcriptional activity and increased DNA methylation in oocytes, disturbed oocyte developmental potency, and fertility of female mice. The impaired expression of genes regulating mitochondrial functions in H3.3‐K4M oocytes, accompanied by mitochondrial abnormalities, is further noticed. Moreover, early embryos from H3.3‐K4M oocytes show developmental arrest and reduced zygotic genome activation. Collectively, these results show that H3K4 methylation in oocytes is critical to orchestrating gene expression profile, driving the oocyte developmental program, and ensuring oocyte quality. This study also improves understanding of how histone modifications regulate organelle dynamics in oocytes.

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Minor zygotic gene activation is essential for mouse preimplantation development

Cited by 155 publications

References 54 publications

Dynamic Alternative Splicing During Mouse Preimplantation Embryo Development

Dynamic Alternative Splicing During Mouse Preimplantation Embryo Development

Probing lasting cryoinjuries to oocyte-embryo transcriptome

H3K4 Methylation Promotes Expression of Mitochondrial Dynamics Regulators to Ensure Oocyte Quality in Mice

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