Atypical GATA protein TRPS1 plays indispensable roles in mouse two-cell embryo

Liu, Yue; Xu, Shunqing; Lian, Xiuli; Su, Yang; Zhong, Yuhuan; Lv, Ruimin; Mo, Kaien; Zhu, Huimin; Wang, Xiaojiang; Xu, Lixuan; Wang, Shie

doi:10.1080/15384101.2019.1577650

Cited by 18 publications

(10 citation statements)

References 70 publications

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“…Nevertheless, the functions and biochemical properties of the MuERVL gene have yet to be fully identified. A recent report also demonstrated that reduced H3K27me3 resulted in the up-regulation of ZGA marker genes in mouse embryos [37]. These results suggested that the H3K27me3 demethylase UTX serves as a novel MuERVL regulator and is essential for preimplantation embryonic development.…”

Section: Discussionmentioning

confidence: 78%

Histone Demethylase UTX is an Essential Factor for Zygotic Genome Activation and Regulates Zscan4 Expression in Mouse Embryos

et al. 2019

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Following fertilization, the zygotic genome is activated through a process termed zygotic genome activation (ZGA), which enables zygotic gene products to replace the maternal products and initiates early embryonic development. During the ZGA period, the embryonic epigenome experiences extensive recodifications. The H3K27me3 demethylase UTX is essential for post-implantation embryonic development. However, it remains unclear whether UTX participates in preimplantation development, especially during the ZGA process. In the present study, we showed that either knockdown or overexpression of UTX led to embryonic development retardation, whereas simultaneous depletion of UTX and overexpression of ZSCAN4D rescued the embryonic development, indicating that UTX positively regulated Zscan4d expression. Using a transgenic mice model, we also found that UTX was required for preimplantation embryonic development. In conclusion, these results indicate that UTX functions as a novel regulator and plays critical roles during ZGA in addition to early embryonic development.

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Section: Discussionmentioning

confidence: 78%

Histone Demethylase UTX is an Essential Factor for Zygotic Genome Activation and Regulates Zscan4 Expression in Mouse Embryos

et al. 2019

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“…MuERV-L is one of the earliest transcribed genes in mouse 1-cell embryos (Kigami et al 2003 ) and promotes the expression of hundreds of neighboring genes (Schoorlemmer et al 2014 ). Other studies showed that the expression of MuERV-L was regulated by some maternal factors such as REX1 (Schoorlemmer et al 2014 ), TRPS1 (Liu et al 2019 ), and DPPA3 (Huang et al 2017 ), contributing to the epigenetic plasticity of mouse embryos. As H3K9me3 is known to be required for silencing ERVs (Elsässer et al 2015 ; Matsui et al 2010 ), Didier Trono’s group demonstrated that SETDB1 regulates the deposition of H3K9me3 and controls the activation of MuERV-L by interacting with KAP1 in ESCs (Rowe et al 2010 ).…”

Section: Discussionmentioning

confidence: 99%

Elevated RIF1 participates in the epigenetic abnormalities of zygotes by regulating histone modifications on MuERV-L in obese mice

Huang

Sun

et al. 2022

Mol Med

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Background Maternal obesity impairs embryonic developmental potential and significantly increases the risks of metabolic disorders in offspring. However, the epigenetic transmission mechanism of maternal metabolic abnormalities is still poorly understood. Methods We established an obesity model in female mice by high-fat diet (HFD) feeding. The effects of the HFD on the developmental potential of oocytes and embryos, the metabolic phenotype, and epigenetic modifications were investigated. The efficacy of metformin administration was assessed. Finally, the regulatory pathway of epigenetic remodeling during zygotic genome activation (ZGA) was explored. Results Maternal HFD consumption significantly impaired glucose tolerance and increased the risk of metabolic disorders in F0 and F1 mice. Maternal HFD consumption also decreased embryonic developmental potential, increased reactive oxygen species (ROS) and γH2AX levels, and reduced the mitochondrial membrane potential (MMP) within oocytes, causing high levels of oxidative stress damage and DNA damage. Starting with this clue, we observed significantly increased RIF1 levels and shortened telomeres in obese mice. Moreover, significant abnormal DNA methylation and histone modification remodeling were observed during ZGA in obese mice, which may be coregulated by RIF1 and the ZGA marker gene MuERV-L. Metformin treatment reduced RIF1 levels, and partially improved ZGA activation status by rescuing epigenetic modification remodeling in oocytes and preimplantation embryos of obese mice. RIF1 knockdown experiments employing Trim-Away methods showed that RIF1 degradation altered the H3K4me3 and H3K9me3 enrichment and then triggered the MuERV-L transcriptional activation. Moreover, ChIP-seq data analysis of RIF1 knockouts also showed that RIF1 mediates the transcriptional regulation of MuERV-L by changing the enrichment of H3K4me3 and H3K9me3 rather than by altered DNA methylation. Conclusion Elevated RIF1 in oocytes caused by maternal obesity may mediate abnormal embryonic epigenetic remodeling and increase metabolic risk in offspring by regulating histone modifications on MuERV-L, which can be partially rescued by metformin treatment.

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“…H3K4me3 regulates the expression of important genes during early embryonic development, such as OCT-4, NANOG, SOX2, and CDX2 [11,12,37,38], and the expression of apoptosis-related genes (Bax, Bak, and Bcl) [39]. Therefore, H3K4me3 exhibits different modification patterns in different stages of embryonic development [11,12,37,38]. Before the activation of the zygotic genome, the H3K4me3 modification from the paternal chromosome will undergo extensive reprogramming.…”

Section: Discussionmentioning

confidence: 99%

New Wenshen Shengjing Decoction Improves Early Embryonic Development by Maintaining Low Levels of H3K4me3 in Sperm

Zhang

Lü

Sun

et al. 2022

BioMed Research International

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Background. New Wenshen Shengjing Decoction (NWSSJD), a traditional Chinese compound medicine, has significant effect on spermatogenesis disorder and can significantly improve sperm quality. Many components in NWSSJD can induce epigenetic modifications of different types of cells. It is not yet known whether they can cause epigenetic modifications in sperm or early embryos. Objective. This study investigated the effect of NWSSJD on mouse early embryonic development and its regulation of H3K4me3 in mouse sperm and early embryos. Methods. Spermatogenesis disorder was induced in male mice with CPA (cyclophosphamide). NWSSJD was administrated for 30 days. Then, the male mice were mated with the female mice with superovulation, and the embryo degeneration rate of each stage was calculated. Immunofluorescence staining was used to detect the expression of H3K4me3 in sperm and embryos at various stages. Western blotting was performed to detect methyltransferase SETD1B expression. The expressions of development-related genes (OCT-4, NANOG, and CDX2) and apoptosis-related genes (BCL-2 and p53) were measured with qRT-PCR. Results. Compared with the CPA group, NWSSJD significantly reduced the H3K4me3 level in sperms, significantly increased the number of normal early embryos (2-cell embryos, 3-4-cell embryos, 8-16-cell embryos, and blastocysts) per mouse, and reduced the degeneration rate of the embryos. The expression levels of H3K4me3 and methyltransferase SETD1B in early embryos were significantly elevated by NWSSJD. Additionally, NWSSJD significantly promoted BCL-2 expression, while reducing p53 expression, thus inhibiting embryonic cell apoptosis. Moreover, the expressions of development-related genes OCT-4 and CDX2 were significantly increased by NWSSJD, but NANOG expression had no significant difference. Conclusion. NWSSJD may promote early embryonic development possibly by maintaining low H3K4me3 levels in sperms and normal H3K4me3 modification in early embryos and by inhibiting embryonic cell apoptosis.

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Atypical GATA protein TRPS1 plays indispensable roles in mouse two-cell embryo

Cited by 18 publications

References 70 publications

Histone Demethylase UTX is an Essential Factor for Zygotic Genome Activation and Regulates Zscan4 Expression in Mouse Embryos

Histone Demethylase UTX is an Essential Factor for Zygotic Genome Activation and Regulates Zscan4 Expression in Mouse Embryos

Elevated RIF1 participates in the epigenetic abnormalities of zygotes by regulating histone modifications on MuERV-L in obese mice

New Wenshen Shengjing Decoction Improves Early Embryonic Development by Maintaining Low Levels of H3K4me3 in Sperm

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