Possible involvement of insulin-like growth factor 2 mRNA-binding protein 3 in zebrafish oocyte maturation as a novel cyclin B1 mRNA-binding protein that represses the translation in immature oocytes

Abstract

In immature zebrafish oocytes, dormant cyclin B1 mRNAs localize to the animal polar cytoplasm as aggregates. After hormonal stimulation, cyclin B1 mRNAs are dispersed and translationally activated, which are necessary and sufficient for the induction of zebrafish oocyte maturation. Besides cytoplasmic polyadenylation element-binding protein (CPEB) and cis-acting elements in the 3' untranslated region (UTR), Pumilio1 and a cis-acting element in the coding region of cyclin B1 mRNA are important for the subcellular localization and timing of translational activation of the mRNA. However, mechanisms underlying the spatio-temporal control of cyclin B1 mRNA translation during oocyte maturation are not fully understood. We report that insulin-like growth factor 2 mRNA-binding protein 3 (IMP3), which was initially described as a protein bound to Vg1 mRNA localized to the vegetal pole of Xenopus oocytes, binds to the 3' UTR of cyclin B1 mRNA that localizes to the animal pole of zebrafish oocytes. IMP3 and cyclin B1 mRNA co-localize to the animal polar cytoplasm of immature oocytes, but in mature oocytes, IMP3 dissociates from the mRNA despite the fact that its protein content and phosphorylation state are unchanged during oocyte maturation. IMP3 interacts with Pumilio1 and CPEB in an mRNA-dependent manner in immature oocytes but not in mature oocytes. Overexpression of IMP3 and injection of anti-IMP3 antibody delayed the progression of oocyte maturation. On the basis of these results, we propose that IMP3 represses the translation of cyclin B1 mRNA in immature zebrafish oocytes and that its release from the mRNA triggers the translational activation.

Shedding new light on early sex determination in zebrafish

“…Ccnb1 is expressed in 48 organs, including nervous system; oocyte; pectoral fin; trunk mesenchyme; and unfertilized egg, with highest expression level in blastula and third highest expression in the mature ovarian follicle [bgee.org—gene: ccnb1—ENSDARG00000051923— Danio rerio (zebrafish)]. Ccb1 is found in oocytes and needed for oocytes maturation and female sexual development (Kondo et al 1997 , 2001 ; Knoll-Gellida et al 2006 ; Wang et al 2007 ; Nagahama and Yamashita 2008 ; Yasuda et al 2013 ; Kotani et al 2013 ; Takahashi et al 2014 ; Horie and Kotani 2016 ; Dingare et al 2018 ; Takei et al 2018 ; Yi et al 2019 ). Ccnb1 is expressed in early zebrafish development (Yasuda et al 2010 ; Horie and Kotani 2016 ).…”

“…org-gene: ccnb1-ENSDARG00000051923-Danio rerio (zebrafish)]. Ccb1 is found in oocytes and needed for oocytes maturation and female sexual development (Kondo et al 1997(Kondo et al , 2001Knoll-Gellida et al 2006;Wang et al 2007;Nagahama and Yamashita 2008;Yasuda et al 2013;Kotani et al 2013;Takahashi et al 2014;Horie and Kotani 2016;Dingare et al 2018;Takei et al 2018;Yi et al 2019). Ccnb1 is expressed in early zebrafish development (Yasuda et al 2010;Horie and Kotani 2016).…”

Proteomic responses to elevated ocean temperature in ovaries of the ascidian Ciona intestinalis

“…Like CNBP, IGF2BP1 targets mRNAs to stress granules under heat stress ( Stöhr et al, 2006 ). IGF2BP1 also has been shown to have an ovary-specific function in blocking the translation of cyclin B1 mRNA to maintain zebrafish oocytes in an immature state ( Takahashi et al, 2014 ).…”

Pnrc2 regulates 3’UTR-mediated decay of segmentation clock-associated transcripts during zebrafish segmentation

“…Overall, because Her1-Venus reporter protein and endogenous Dlc and Dld proteins are expressed normally despite misexpression of mRNA in pnrc2 -deficient embryos (Fig 7; Fig S4; Table S3), we suggest that Pnrc2-mediated mRNA decay acts in addition to a regulatory layer that controls oscillatory protein expression. Although the her1 transcript does not contain obvious NMD-inducing features such as an uORF and accumulated her1 transcripts in pnrc2 mutants do not appear retained in nuclei (Fig 7F′; Fig S6B″), there are other mechanisms that may function to repress or prevent translation (Mishima et al, 2012; Takeda et al, 2009; Yasuda et al, 2010; Takahashi et al, 2014; Subtelny et al, 2014; Mishima and Tomari, 2016). Alternatively, normal cyclic protein expression in pnrc2 mutants might occur because protein decay machinery compensates for increased cyclic expression.…”