rRNA Genes Are Not Fully Activated in Mouse Somatic Cell Nuclear Transfer Embryos

Zheng, Zhong; Jia, Jialin; Bou, Gerelchimeg; Hu, Li-Li; Wang, Zhendong; Shen, Xiaopei; Shan, Zhiyan; Shen, Jingling; Z, Liu; Lei, Lei

doi:10.1074/jbc.m112.355099

Cited by 23 publications

(26 citation statements)

References 54 publications

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“…Lastly, we have verified that the synthesis of rRNAs is not affected in spermatid-derived embryos. Indeed, in mouse, defect in rRNA synthesis has been proposed to explain the developmental defect of nuclear transfer embryos (Suzuki et al 2007;Zheng et al 2012) and could explain the difference in the bulk of RNA synthesis observed between sperm-and spermatid-derived embryos (Bui et al 2011). We observed that newly synthesized 18S and 28S rRNAs are equally well produced in sperm-and spermatid-derived embryos (Supplemental Fig.…”

Section: Developmentally Important Genes Are Misregulated In Spermatimentioning

confidence: 52%

“…Several hypotheses were proposed to explain the nature of this programming, including the idea that sperm is programmed for efficient replication after fertilization (Lemaitre et al 2005) or for supporting proper embryonic transcription (Suzuki et al 2007;Hammoud et al 2009;Zheng et al 2012). The latter hypothesis was proposed following the observation that promoters of developmentally important genes escape global replacement of histones by protamines in mature sperm.…”

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confidence: 99%

“…The latter hypothesis was proposed following the observation that promoters of developmentally important genes escape global replacement of histones by protamines in mature sperm. In fact, these promoters retain post-translationally modified histones, suggesting that epigenetic marks on sperm chromatin may be transmitted to the embryo at fertilization and could subsequently pattern transcription of embryonic genes (Suzuki et al 2007;Hammoud et al 2009;Brykczynska et al 2010;Wu et al 2011;Paradowska et al 2012;Zheng et al 2012;Ihara et al 2014;Siklenka et al 2015). However, the validity of this hypothesis was recently questioned (Carone et al 2014;Samans et al 2014).…”

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confidence: 99%

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Sperm is epigenetically programmed to regulate gene transcription in embryos

et al. 2016

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For a long time, it has been assumed that the only role of sperm at fertilization is to introduce the male genome into the egg. Recently, ideas have emerged that the epigenetic state of the sperm nucleus could influence transcription in the embryo. However, conflicting reports have challenged the existence of epigenetic marks on sperm genes, and there are no functional tests supporting the role of sperm epigenetic marking on embryonic gene expression. Here, we show that sperm is epigenetically programmed to regulate embryonic gene expression. By comparing the development of sperm- and spermatid-derived frog embryos, we show that the programming of sperm for successful development relates to its ability to regulate transcription of a set of developmentally important genes. During spermatid maturation into sperm, these genes lose H3K4me2/3 and retain H3K27me3 marks. Experimental removal of these epigenetic marks at fertilization de-regulates gene expression in the resulting embryos in a paternal chromatin-dependent manner. This demonstrates that epigenetic instructions delivered by the sperm at fertilization are required for correct regulation of gene expression in the future embryos. The epigenetic mechanisms of developmental programming revealed here are likely to relate to the mechanisms involved in transgenerational transmission of acquired traits. Understanding how parental experience can influence development of the progeny has broad potential for improving human health.

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Section: Developmentally Important Genes Are Misregulated In Spermatimentioning

confidence: 52%

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confidence: 99%

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confidence: 99%

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Sperm is epigenetically programmed to regulate gene transcription in embryos

et al. 2016

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“…ICSI was carried out with a piezo-driven unit using a previously described method (Tesarik et al, 2002;Zheng et al, 2012), except that our experiment was performed at room temperature in HEPES-CZB medium containing 5 g/ml cytochalasin B (Sigma). Whole spermatozoon were injected into oocytes.…”

Section: Mouse Oocyte Collection Ivf Icsi and Embryo Culturementioning

confidence: 99%

Autophagy and ubiquitin-mediated proteolysis may not be involved in the degradation of spermatozoon mitochondria in mouse and porcine early embryos

Jin

Zheng

et al. 2014

Zygote

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The mitochondrial genome is maternally inherited in animals, despite the fact that paternal mitochondria enter oocytes during fertilization. Autophagy and ubiquitin-mediated degradation are responsible for the elimination of paternal mitochondria in Caenorhabditis elegans; however, the involvement of these two processes in the degradation of paternal mitochondria in mammals is not well understood. We investigated the localization patterns of light chain 3 (LC3) and ubiquitin in mouse and porcine embryos during preimplantation development. We found that LC3 and ubiquitin localized to the spermatozoon midpiece at 3 h post-fertilization, and that both proteins were colocalized with paternal mitochondria and removed upon fertilization during the 4-cell stage in mouse and the zygote stage in porcine embryos. Sporadic paternal mitochondria were present beyond the morula stage in the mouse, and paternal mitochondria were restricted to one blastomere of 4-cell embryos. An autophagy inhibitor, 3-methyladenine (3-MA), did not affect the distribution of paternal mitochondria compared with the positive control, while an autophagy inducer, rapamycin, accelerated the removal of paternal mitochondria compared with the control. After the intracytoplasmic injection of intact spermatozoon into mouse oocytes, LC3 and ubiquitin localized to the spermatozoon midpiece, but remnants of undegraded paternal mitochondria were retained until the blastocyst stage. Our results show that paternal mitochondria colocalize with autophagy receptors and ubiquitin and are removed after in vitro fertilization, but some remnants of sperm mitochondrial sheath may persist up to morula stage after intracytoplasmic spermatozoon injection (ICSI).

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“…Microarray analysis of 2-cell mouse embryos has revealed that more than 2000 mRNAs are misregulated in NT embryos compared to fertilised embryos [152]. Transcription by RNA polymerase I is also disturbed in cloned embryos around this stage [139, 153]. This early abnormal gene expression can be rescued by treatment with histone deacetylase inhibitors [135, 139], suggesting that abnormal gene expression in early embryos is at least partially due to the somatic epigenome, which is not adequate to support the embryonic gene expression program.…”

Section: Abnormalities In Cloned Embryos In Relation To Somatic Cell mentioning

confidence: 99%

Nuclear reprogramming of sperm and somatic nuclei in eggs and oocytes

Teperek

Miyamoto

2013

Reprod Medicine & Biology

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Eggs and oocytes have a prominent ability to reprogram sperm nuclei for ensuring embryonic development. The reprogramming activity that eggs/oocytes intrinsically have towards sperm is utilised to reprogram somatic nuclei injected into eggs/oocytes in nuclear transfer (NT) embryos. NT embryos of various species can give rise to cloned animals, demonstrating that eggs/oocytes can confer totipotency even to somatic nuclei. However, many studies indicate that reprogramming of somatic nuclei is not as efficient as that of sperm nuclei. In this review, we explain how and why sperm and somatic nuclei are differentially reprogrammed in eggs/oocytes. Recent studies have shown that sperm chromatin is epigenetically modified to be adequate for early embryonic development, while somatic nuclei do not have such modifications. Moreover, epigenetic memories encoded in sperm chromatin are transgenerationally inherited, implying unique roles of sperm. We also discuss whether somatic nuclei can be artificially modified to acquire sperm-like chromatin states in order to increase the efficiency of nuclear reprogramming.

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rRNA Genes Are Not Fully Activated in Mouse Somatic Cell Nuclear Transfer Embryos

Cited by 23 publications

References 54 publications

Sperm is epigenetically programmed to regulate gene transcription in embryos

Sperm is epigenetically programmed to regulate gene transcription in embryos

Autophagy and ubiquitin-mediated proteolysis may not be involved in the degradation of spermatozoon mitochondria in mouse and porcine early embryos

Nuclear reprogramming of sperm and somatic nuclei in eggs and oocytes

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