Maternally Inherited npm2 mRNA Is Crucial for Egg Developmental Competence in Zebrafish

Type Article
Date 2014-08
Language English
Author(s) Bouleau Aurelien1, 2, Desvignes Thomas1, 2, Traverso Juan Martin1, Nguyen Thaovi1, Chesnel Franck3, Fauvel Christian2, Bobe Julien1
Affiliation(s) 1 : INRA, LPGP Sex Differentiat & Oogenesis Grp UR1037, F-35042 Rennes, France.
2 : IFREMER, LALR, Palavas Les Flots, France.
3 : Univ Rennes 1, CNRS UMR6290, Rennes, France.
Source Biology Of Reproduction (0006-3363) (Soc Study Reproduction), 2014-08 , Vol. 91 , N. 2 , P. 1-9
DOI 10.1095/biolreprod.114.119925
WOS© Times Cited 18
Keyword(s) egg quality, fish, maternal effect gene, maternal-to-zygotic transition, nucleoplasmin, oocyte developmental competence, teleost, zygotic genome activation
Abstract 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.
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