Bouleau Aurélien, Desvignes Thomas, Traverso Juan Martin, Nguyen Thaovi, Chesnel Franck, Fauvel Christian, Bobe Julien
INRA, LPGP UR1037 Sex differentiation and oogenesis group, Campus de Beaulieu, Rennes, France IFREMER, LALR, Palavas-Les-Flots, France.
INRA, LPGP UR1037 Sex differentiation and oogenesis group, Campus de Beaulieu, Rennes, France.
Biol Reprod. 2014 Aug;91(2):43. doi: 10.1095/biolreprod.114.119925. Epub 2014 Jul 9.
The molecular mechanisms underlying and determining egg developmental competence remain poorly understood in vertebrates. Nucleoplasmin (Npm2) is one of the few known maternal effect genes in mammals, but this maternal effect has never been demonstrated in nonmammalian species. A link between developmental competence and the abundance of npm2 maternal mRNA in the egg was previously established using a teleost fish model for egg quality. The importance of maternal npm2 mRNA for egg developmental competence remains unknown in any vertebrate species. In the present study, we aimed to characterize the contribution of npm2 maternal mRNA to early developmental success in zebrafish using a knockdown strategy. We report here the oocyte-specific expression of npm2 and maternal inheritance of npm2 mRNA in zebrafish eggs. The knockdown of the protein translated from this maternal mRNA results in developmental arrest before the onset of epiboly and subsequent embryonic death, a phenotype also observed in embryos lacking zygotic transcription. Npm2 knockdown also results in impaired transcription of the first-wave zygotic genes. Our results show that npm2 is also a maternal effect gene in a nonmammalian vertebrate species and that maternally inherited npm2 mRNA is crucial for egg developmental competence. We also show that de novo protein synthesis from npm2 maternal mRNA is critical for developmental success beyond the blastula stage and required for zygotic genome activation. Finally, our results suggest that npm2 maternal mRNA is an important molecular factor of egg quality in fish and possibly in all vertebrates.
在脊椎动物中，卵子发育能力的潜在分子机制以及决定因素仍未得到充分理解。核质蛋白（Npm2）是哺乳动物中少数已知的母源效应基因之一，但这种母源效应从未在非哺乳动物物种中得到证实。先前使用硬骨鱼卵质量模型建立了发育能力与卵子中npm2母源mRNA丰度之间的联系。在任何脊椎动物物种中，母源npm2 mRNA对卵子发育能力的重要性仍然未知。在本研究中，我们旨在使用敲低策略来表征npm2母源mRNA对斑马鱼早期发育成功的贡献。我们在此报告了npm2在斑马鱼卵母细胞中的特异性表达以及npm2 mRNA的母系遗传。从这种母源mRNA翻译而来的蛋白质的敲低导致在胚盘形成开始之前发育停滞并随后胚胎死亡，这种表型也在缺乏合子转录的胚胎中观察到。Npm2敲低还导致第一波合子基因的转录受损。我们的结果表明，npm2在非哺乳动物脊椎动物物种中也是一个母源效应基因，并且母系遗传的npm2 mRNA对于卵子发育能力至关重要。我们还表明，npm2母源mRNA的从头蛋白质合成对于囊胚期之后的发育成功至关重要，并且是合子基因组激活所必需的。最后，我们的结果表明，npm2母源mRNA是鱼类以及可能所有脊椎动物中卵子质量的重要分子因素。
