miR-92a-3p controls cell cycle progression in zebrafish

Abstract

Biological functions of micro RNAs (miRNAs) in the early stages of vertebrate development remain largely unknown. In zebrafish, miRNA miR-92a-3p is abundant in the germ cells throughout gonadal development, as well as in ovulated oocytes. Previously, we demonstrated that inhibition of miR-92a-3p in mature ovaries resulted in developmental arrest at the 1-cell stage upon fertilization of the affected oocytes. This suggested functions of miR-92a-3p in early development. In the present study, we identified wee2, an oocyte-specific protein tyrosine kinase, as a target of maternal miR-92a-3p during the early stages of zebrafish embryogenesis. Spatiotemporal co-presence of both miR-92a-3p and wee2 during early embryo development was confirmed by absolute quantification and in situ hybridization. Targeted knockdown of miR-92a-3p in embryos resulted in retarded embryonic development over the first 24 hours. Target validation assays demonstrated that miR-92a-3p interacted with the predicted wee2 3’UTR binding site, which was strongly suppressed by endogenous miR-92a-3p. Our results suggest that miR-92a-3p regulates the abundance of wee2, a cyclin-dependent kinase 1 inhibitor, thus having important role in regulation of the cell cycle during cleavage stages in zebrafish.Summary statementIn zebrafish, maternal miR-92a-3p was demonstrated to suppress translation of wee2, a cyclin-dependent kinase 1 inhibitor which regulates cell cycle progression during the early stages of embryogenesis.

Deciphering sex-specific miRNAs as heat-recorders in zebrafish

“…1 C) that showed those miRNAs that were constitutively differentially expressed between both sexes.

Figure 1 The number of miRNAs that were significantly expressed (average normalized reads > 100) of two AB strains (current data and Desvignes et al 18 ) and zf45Tg hybrid zebrafish (Presslauer et al 47 ). ( A ) In ovaries, and ( B ) testes.

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“…Another miRNA that was upregulated by heat treatment was dre-miR-92a, which has been found as the most abundant miRNA in zebrafish gonads 17 . This miRNA was responsible for cell cycle progression during the early stage of embryo development and metamorphosis in both Japanese flounder ( Paralichthys olivaceus ) 46 and in zebrafish 47 .…”

Identification of sex differentiation-related microRNA and long non-coding RNA in Takifugu rubripes gonads

“…A recent study has demonstrated that during the early stages of embryogenesis of D. rerio , maternal miR-92a-3p can suppress the cyclin dependent kinase 1 inhibitor (Wee 1 homolog 2), which regulates cell cycle progression. A significantly higher rate of embryonic developmental arrest at the one-cell embryo stage was observed due to the inhibition of maternal miR-92a-3p expression 38 . let-7 is one of the miRNAs family initially identified in Caenorhabditis elegans as a key developmental switch and plays a crucial role in controlling the transition from larva to adult 39 .…”

Role of sex‐biased miRNAs in teleosts – a review

“…miR‐92a‐3p is a maternal transcript housed in unfertilized eggs that acts as a suppressor of wee2 , a cyclin‐dependent kinase 1 inhibitor, consequently promoting the progression of cell cycle during early embryogenesis in zebrafish (Presslauer et al . 2019). While high expression of miR‐430‐3p and miR‐22a‐3p was unique in ovary, testicular abundance of miR‐125c‐5p and miR‐462‐5p was noted (Presslauer et al .…”