Genome-wide identification of novel ovarian-predominant miRNAs: new insights from the medaka (Oryzias latipes)

Bouchareb, Amine; Cam, Aurélie Le; Montfort, Jérôme; Gay, Stéphanie; Tri, Nguyen; Bobe, Julien; Thermes, Violette

doi:10.1038/srep40241

Cited by 19 publications

(13 citation statements)

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“…20 differentially expressed miRs were found in 20(S)-Rg3-treated cells by deep sequencing technique. Among the upregulated miRs, miR-3163, miR-324-5p, miR-664a-5p, miR-486-3p, miR-33a-3p were reported to be tumor suppressors while miR-603 acted as both oncomir and anti-oncomir [26-30], and the roles of miR-4329, miR-519a-5p, miR-6717-5p and miR-1283 were not defined in cancer [31]. Contrarily, the function of most downregulated miRs including miR-7156-5p, miR-1273e, miR-6730-3p, miR-7843-3p, miR-2682-3p, miR-4425 and miR-195-3p were unclear, except that miR-4634 and miR-4532 were reported to be elevated in cancer tissues or serum [32-34].…”

Section: Discussionmentioning

confidence: 99%

Ginsenoside 20(S)-Rg3 Inhibits the Warburg Effect Via Modulating DNMT3A/ MiR-532-3p/HK2 Pathway in Ovarian Cancer Cells

Zhou

Zheng

et al. 2018

Cell Physiol Biochem

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Background/Aims: The Warburg effect is one of the main energy metabolism features supporting cancer cell growth. 20(S)-Rg3 exerts anti-tumor effect on ovarian cancer partly by inhibiting the Warburg effect. microRNAs are important regulators of the Warburg effect. However, the microRNA regulatory network mediating the anti-Warburg effect of 20(S)-Rg3 was largely unknown. Methods: microRNA deep sequencing was performed to identify the 20(S)-Rg3-influenced microRNAs in SKOV3 ovarian cancer cells. miR-532-3p was overexpressed by mimic532-3p transfection in SKOV3 and A2780 cells or inhibited by inhibitor532-3p transfection in 20(S)-Rg3-treated cells to examine the changes in HK2 and PKM2 expression, glucose consumption, lactate production and cell growth. Dual-luciferase reporter assay was conducted to verify the direct binding of miR-532-3p to HK2. The methylation status in the promoter region of pre-miR-532-3p gene was examined by methylation-specific PCR. Expression changes of key molecules controlling DNA methylation including DNMT1, DNMT3A, DNMT3B, and TET1-3 were examined in 20(S)-Rg3-treated cells. DNMT3A was overexpressed in 20(S)-Rg3-treated cells to examine its influence on miR-532-3p level, HK2 and PKM2 expression, glucose consumption and lactate production. Results: Deep sequencing results showed that 11 microRNAs were increased and 9 microRNAs were decreased by 20(S)-Rg3 in SKOV3 cells, which were verified by qPCR. More than 2-fold increase of miR-532-3p was found in 20(S)-Rg3-treated SKOV3 cells. Forced expression of miR-532-3p reduced HK2 and PKM2 expression, glucose consumption and lactate production in SKOV3 and A2780 ovarian cancer cells. Inhibition of miR-532-3p antagonized the suppressive effect of 20(S)-Rg3 on HK2 and PKM2 expression, glucose consumption and lactate production in ovarian cancer cells. Dual-luciferase reporter assay showed that miR-532-3p directly suppressed HK2 rather than PKM2. miR-532-3p level was controlled by the methylation in the promoter region of its host gene. 20(S)-Rg3 inhibited DNMT3A expression while exerted insignificant effect on DNMT1, DNMT3B and TET1-3. 20(S)-Rg3 reversed DNMT3A-mediated methylation in the promoter of the host gene of miR-532-3p, and thus elevated miR-532-3p level followed by suppression of HK2 and PKM2 expression, glucose consumption and lactate production. Conclusions: 20(S)-Rg3 modulated microRNAs to exert the anti-tumor effect in ovarian cancer. 20(S)-Rg3 lessened the DNMT3A-mediated methylation and promoted the suppression of miR-532-3p on HK2 to antagonize the Warburg effect of ovarian cancer cells.

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Section: Discussionmentioning

confidence: 99%

Ginsenoside 20(S)-Rg3 Inhibits the Warburg Effect Via Modulating DNMT3A/ MiR-532-3p/HK2 Pathway in Ovarian Cancer Cells

Zhou

Zheng

et al. 2018

Cell Physiol Biochem

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“…MZT is a key step that is needed firstly for clearance of maternal components, and secondly to activate zygotic gene expression and to allow subsequent embryonic development. Among the maternally-inherited transcripts that play important roles during early development, some were demonstrated to regulate zygotic program activation such as nanog , pou5f1 , soxb1 and microRNAs in zebrafish ( Danio rerio ) [ 3 , 4 ]. Henceforth, all gene and protein nomenclature written in this manuscript will be based on that of zebrafish regardless of species for simplification purposes.…”

Section: Introductionmentioning

confidence: 99%

Double maternal-effect: duplicated nucleoplasmin 2 genes, npm2a and npm2b, with essential but distinct functions are shared by fish and tetrapods

et al. 2018

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BackgroundNucleoplasmin 2 (npm2) is an essential maternal-effect gene that mediates early embryonic events through its function as a histone chaperone that remodels chromatin. Recently, two npm2 (npm2a and npm2b) genes have been annotated in zebrafish. Thus, we examined the evolution of npm2a and npm2b in a variety of vertebrates, their potential phylogenetic relationships, and their biological functions using knockout models via the CRISPR/cas9 system.ResultsWe demonstrated that the two npm2 duplicates exist in a wide range of vertebrates, including sharks, ray-finned fish, amphibians, and sauropsids, while npm2a was lost in coelacanth and mammals, as well as some specific teleost lineages. Using phylogeny and synteny analyses, we traced their origins to the early stages of vertebrate evolution. Our findings suggested that npm2a and npm2b resulted from an ancient local gene duplication, and their functions diverged although key protein domains were conserved. We then investigated their functions by examining their tissue distribution in a wide variety of species and found that they shared ovarian-specific expression, a key feature of maternal-effect genes. We also demonstrated that both npm2a and npm2b are maternally-inherited transcripts in vertebrates, and that they play essential, but distinct, roles in early embryogenesis using zebrafish knockout models. Both npm2a and npm2b function early during oogenesis and may play a role in cortical granule function that impact egg activation and fertilization, while npm2b is also involved in early embryogenesis.ConclusionThese novel findings will broaden our knowledge on the evolutionary history of maternal-effect genes and underlying mechanisms that contribute to vertebrate reproductive success. In addition, our results demonstrate the existence of a newly described maternal-effect gene, npm2a, that contributes to egg competence, an area that still requires further comprehension.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1281-3) contains supplementary material, which is available to authorized users.

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“…Those factors were shown to participate in the regulation of “first wave” zygotic genes and among them, mir-430, a conserved microRNA that has been shown to be involved in clearance of maternal mRNAs in zebrafish [4][5], as well as mir-427, its orthologue in Xenopus [6]. microRNAs may also have maternal effects by functioning in a similar manner to protein-coding genes, and recent revelations showed that there is a subset of microRNAs that are predominantly expressed in the fish ovary and may function in oogenesis and early embryogenesis [7]. Another gene, nucleoplasmin 2 ( npm2 ), belongs to the family of nucleoplasmins/nucleophosmins that is maternally-inherited at both protein and mRNA levels, whereby both play important roles in early development [8].…”

Section: Introductionmentioning

confidence: 99%

Double maternal effect: duplicated nucleoplasmin 2 genes,npm2aandnpm2b, are shared by fish and tetrapods, and have distinct and essential roles in early embryogenesis

Cheung

Pasquier

Bouleau

et al. 2017

Preprint

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(2017). Double maternal effect: duplicated nucleoplasmin 2 genes, npm2a and npm2b, are shared by fish and tetrapods, and have distinct and essential roles in early embryogenesis. BioRxiv, 1-39.DOI : 10. . CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/104760 doi: bioRxiv preprint first posted online May. 22, 2017; Version preprint Comment citer ce document : Cheung, C., Pasquier, J., Bouleau, A., Nguyen, T. T. V., Chesnel, F., Guiguen, Y., Bobe, J. (2017). Double maternal effect: duplicated nucleoplasmin 2 genes, npm2a and npm2b, are shared by fish and tetrapods, and have distinct and essential roles in early embryogenesis. BioRxiv, 1-39. DOI : 10.1101/1047602 Abstract 1 4Nucleoplasmin 2 (npm2) is an essential maternal-effect gene that mediates early embryonic 1 5 events through its function as a histone chaperone that remodels chromatin. Here we report 1 6 the existence of two npm2 (npm2a and npm2b) genes in zebrafish. We examined the 1 7evolution of npm2a and npm2b in a variety of vertebrates, their potential phylogenetic 1 8relationships, and their biological functions using knockout models via the CRISPR/cas91 9system. We demonstrated that the two npm2 duplicates exist in a wide range of vertebrates, 2 0including sharks, ray-finned fish, amphibians, and sauropsids, while npm2a was lost in 1Coelacanth and mammals, as well as some specific teleost lineages. Using phylogeny and 2 2 synteny analyses, we traced their origins to the early stages of vertebrate evolution. Our 2 3findings suggested that npm2a and npm2b resulted from an ancient local gene duplication, 4and their functions diverged although key protein domains were conserved. We then 2 5investigated their functions by examining their tissue distribution in a wide variety of species 2 6and found that they shared ovarian-specific expression, a key feature of maternal-effect 2 7genes. We also showed that both npm2a and npm2b are maternally-inherited transcripts in 2 8vertebrates. Moreover, we used zebrafish knockouts to demonstrate that npm2a and npm2b 2 9play essential, but distinct, roles in early embryogenesis. npm2a functions very early during 3 0 embryogenesis, at or immediately after fertilization, while npm2b is involved in processes 3 1 leading up to or during zygotic genome activation. These novel findings will broaden our 3 2 knowledge on the evolutionary diversity of maternal-effect genes and underlying mechanisms 3 3 that contribute to vertebrate reproductive success. . CC-BY-NC-ND 4.0 International license peer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/104760 doi: bioRxiv preprint first posted online May. 22, 2017; Version preprint Comment citer ce document : Cheung, C., Pasquier, J., Bouleau, A., Nguyen, T. T. V., Chesnel, F., Guiguen, Y., Bobe, J. (2017). Double maternal effect: duplicated nucleop...

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Genome-wide identification of novel ovarian-predominant miRNAs: new insights from the medaka (Oryzias latipes)

Cited by 19 publications

References 64 publications

Ginsenoside 20(S)-Rg3 Inhibits the Warburg Effect Via Modulating DNMT3A/ MiR-532-3p/HK2 Pathway in Ovarian Cancer Cells

Ginsenoside 20(S)-Rg3 Inhibits the Warburg Effect Via Modulating DNMT3A/ MiR-532-3p/HK2 Pathway in Ovarian Cancer Cells

Double maternal-effect: duplicated nucleoplasmin 2 genes, npm2a and npm2b, with essential but distinct functions are shared by fish and tetrapods

Double maternal effect: duplicated nucleoplasmin 2 genes,npm2aandnpm2b, are shared by fish and tetrapods, and have distinct and essential roles in early embryogenesis

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