SON controls mouse early embryonic development by regulating RNA splicing and histone methylation.

IF 3.7 3区 生物学 Q1 DEVELOPMENTAL BIOLOGY Reproduction Pub Date : 2024-11-11 Print Date: 2024-12-01 DOI:10.1530/REP-24-0087
Jiarui Wei, Xianglan An, Cong Fu, Qi Li, Fang Wang, Rong Huang, Haibo Zhu, Ziyi Li, Sheng Zhang
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Abstract

In brief: During zygotic genome activation, thousands of genes are activated, and those pre-mRNAs must be accurately spliced to support the production of functional proteins. This study shows that SON is necessary for proper nuclear speckle organization, pre-mRNA splicing, transcriptome establishment, and histone methylation in mouse preimplantation embryos.

Abstract: Thousands of genes are activated in late two-cell embryos, which means that numerous pre-mRNAs are generated during this time. These pre-mRNAs must be accurately spliced to ensure that the mature mRNAs are translated into functional proteins. However, little is known about the roles of pre-mRNA splicing and the cellular factors modulating pre-mRNA splicing during early embryonic development. Here, we report that downregulation of SON, a large Ser/Arg (SR)-related protein, reduced embryonic development and caused deficient blastomere cleavage. These embryonic developmental defects result from dysregulated nuclear speckle organization and pre-mRNA splicing of a set of cell cycle-related genes. Furthermore, SON downregulation disrupted the transcriptome (2128 upregulated and 1399 downregulated) in four-cell embryos. Increased H3K4me3, H3K9me3, and H3K27me3 levels were detected in four-cell embryos after SON downregulation. Taken together, these results demonstrate that accurate pre-mRNA splicing is essential for early embryonic development and that SON plays important roles in nuclear speckle organization, pre-mRNA splicing, transcriptome establishment, and histone methylation reprogramming during early embryonic development.

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SON 通过调节 RNA 剪接和组蛋白甲基化控制小鼠早期胚胎发育。
在 2 细胞胚胎晚期,数以千计的基因被激活,这意味着在此期间会产生大量前 mRNA。这些前 mRNA 必须准确剪接,以确保成熟的 mRNA 翻译成功能性蛋白质。然而,人们对胚胎早期发育过程中前 mRNA 剪接的作用以及调节前 mRNA 剪接的细胞因素知之甚少。在这里,我们报告了下调 SON(一种大型 Ser/Arg (SR) 相关蛋白)会降低胚胎发育并导致胚泡裂解缺陷。这些胚胎发育缺陷源于核斑点组织和一组细胞周期相关基因的前核糖核酸剪接失调。此外,下调 SON 会破坏 4 细胞胚胎的转录组(2128 个上调和 1399 个下调)。在 SON 下调后的 4 细胞胚胎中检测到 H3K4me3、H3K9me3 和 H3K27me3 水平升高。综上所述,这些结果表明,准确的前核糖核酸剪接对早期胚胎发育至关重要,而 SON 在早期胚胎发育过程中的核斑点组织、前核糖核酸剪接、转录组建立和组蛋白甲基化重编程中发挥着重要作用。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
Reproduction
Reproduction 生物-发育生物学
CiteScore
7.40
自引率
2.60%
发文量
199
审稿时长
4-8 weeks
期刊介绍: Reproduction is the official journal of the Society of Reproduction and Fertility (SRF). It was formed in 2001 when the Society merged its two journals, the Journal of Reproduction and Fertility and Reviews of Reproduction. Reproduction publishes original research articles and topical reviews on the subject of reproductive and developmental biology, and reproductive medicine. The journal will consider publication of high-quality meta-analyses; these should be submitted to the research papers category. The journal considers studies in humans and all animal species, and will publish clinical studies if they advance our understanding of the underlying causes and/or mechanisms of disease. Scientific excellence and broad interest to our readership are the most important criteria during the peer review process. The journal publishes articles that make a clear advance in the field, whether of mechanistic, descriptive or technical focus. Articles that substantiate new or controversial reports are welcomed if they are noteworthy and advance the field. Topics include, but are not limited to, reproductive immunology, reproductive toxicology, stem cells, environmental effects on reproductive potential and health (eg obesity), extracellular vesicles, fertility preservation and epigenetic effects on reproductive and developmental processes.
期刊最新文献
SON controls mouse early embryonic development by regulating RNA splicing and histone methylation. IMPACT OF REAL-LIFE ENVIRONMENTAL EXPOSURES ON REPRODUCTION: Systemic and ovarian impacts of heat stress in the porcine model. Phthalate exposure and reproductive effects in rodents: a model for approaches on the protective role of natural products. YAP1 and WWTR1 are required for murine pregnancy initiation. NSUN2 is critical for mouse oocyte meiosis and early embryonic development.
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