Prostaglandins in teleost ovulation: A review of the roles with a view to comparison with prostaglandins in mammalian ovulation

Takahashi, Takayuki; Hagiwara, Akane; Ogiwara, Katsueki

doi:10.1016/j.mce.2017.09.019

Cited by 58 publications

(47 citation statements)

References 171 publications

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“…Based on the present observations together with our previous findings [6,13], we propose a schematic model for the role of Ccni/Cdk9 in the pathway leading to mmp15 /Mmp15 expression after the LH surge in follicles (Figure 8). In this model, we focus on the events occurring in granulosa cells, because these cells have been documented to play a major role in fish ovulation [24]. Roscovitine’s effects are also shown in this model.…”

Section: Discussionmentioning

confidence: 99%

Nuclear Progestin Receptor Phosphorylation by Cdk9 Is Required for the Expression of Mmp15, a Protease Indispensable for Ovulation in Medaka

Ogiwara

Takahashi

2019

Cells

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Ovulation denotes the discharge of fertilizable oocytes from ovarian follicles. Follicle rupture during ovulation requires extracellular matrix (ECM) degradation at the apex of the follicle. In the teleost medaka, an excellent model for vertebrate ovulation studies, LH-inducible matrix metalloproteinase 15 (Mmp15) plays a critical role during rupture. In this study, we found that follicle ovulation was inhibited not only by roscovitine, the cyclin-dependent protein kinase (CDK) inhibitor, but also by CDK9-inhibitor II, a specific CDK9 inhibitor. Inhibition of follicle ovulation by the inhibitors was accompanied by the suppression of Mmp15 expression in the follicle. In follicles treated with the inhibitors, the formation of the phosphorylated nuclear progestin receptor (Pgr) was inhibited. Roscovitine treatment caused a reduction in the binding of Pgr to the promoter region of mmp15. The expression of Cdk9 and cyclin I (Ccni), and their association in the follicle was demonstrated, suggesting that Cdk9 and Ccni may be involved in the phosphorylation of Pgr in vivo. LH-induced follicular expression of ccni/Ccni was also shown. This study is the first to report the involvement of CDK in ECM degradation during ovulation in a vertebrate species.

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Section: Discussionmentioning

confidence: 99%

Nuclear Progestin Receptor Phosphorylation by Cdk9 Is Required for the Expression of Mmp15, a Protease Indispensable for Ovulation in Medaka

Ogiwara

Takahashi

2019

Cells

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“…There is persuasive evidence that prostaglandins are also critically involved in follicle rupture during ovulation in vertebrates (Sirois et al 2004a,b, Richards 2005, Stouffer et al 2007, Sugimoto et al 2015. The role for prostaglandins in teleost ovulation has been recently reviewed (Takahashi et al 2018). In medaka, Ptger4b, a prostaglandin E 2 receptor isoform of Ptger4, is expressed in the granulosa cells of ovulating follicles and is activated with its ligand prostaglandin E 2 at the time of ovulation (Fujimori et al 2011, 2012, Hagiwara et al 2014.…”

Section: Perspectivementioning

confidence: 99%

Follicle rupture during ovulation with an emphasis on recent progress in fish models

2018

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Ovulation, which is induced by the ovulatory luteinizing hormone (LH) surge, is a dynamic process that results in a discharge of one or more fertilizable oocytes from the ovarian follicle into the ovarian cavity or into the abdominal cavity. Follicle rupture is a core event of the ovulatory process and has been the subject of intensive investigation. Many studies have been performed in various vertebrate animals that focused on proteolysis during ovulation. Despite much effort, the proteases responsible for follicle rupture in ovulation have not yet been identified for mammalian species. However, studies conducted using the teleost medaka have recently provided valuable information about the follicle rupture process. Follicle rupture during medaka ovulation is accomplished by a two-step extracellular matrix (ECM) hydrolysis mechanism involving two distinct protease systems, the urokinase-type plasminogen activator-1 /plasmin and the matrix metalloproteinase system. In the 24-h spawning cycle of the fish, the former protease system is activated first, and the latter subsequently becomes active. Proteolytic activities of these systems are regulated by their intrinsic inhibitors. The endocrine regulation of the rupture was examined by investigating the expression of matrix metalloproteinase 15 (Mmp15), which is the only LH-inducible protease among those involved in the rupture process. At least two transcription factors, classical nuclear progestin receptor and CCAAT/enhancer-binding protein β, play critical roles in the expression of the protease transcript. This review also summarizes studies addressing follicle rupture during ovulation conducted using other teleost models to understand the current status of teleost ovulation studies.

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“…Culture of COCs in medium containing granulosa secreted factors has been suggested to increase the proximity of in vitro culture to in vivo condition and improve the efficiency of in vitro oocyte maturation, especially in COCs derived from small follicles (2 to � 4mm) with lower developmental competence compared to follicles of � 4 to 6mm or of greater size [29,30]. Our goal is to select ovine as a model for human IVM in future studies.…”

Section: Introductionmentioning

confidence: 99%

Granulosa secreted factors improve the developmental competence of cumulus oocyte complexes from small antral follicles in sheep

et al. 2020

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Oocyte in vitro maturation can be improved by mimicking the intra-follicular environment. Oocyte, cumulus cells, granulosa cells, and circulating factors act as meiotic regulators in follicles and maintain oocyte in the meiotic phase until oocyte becomes competent and ready to be ovulated. In a randomized experimental design, an ovine model was used to optimize the standard in vitro maturation media by Granulosa secreted factors. At first, the development capacity of oocyte derived from medium (>4 to 6 mm) and small (2 to �4 mm) size follicles was determined. Differential gene expression of granulosa secreted factors and their receptors were compared between the cumulus cells of the two groups. Then, the best time and concentration for arresting oocytes at the germinal vesicle stage by natriuretic peptide type C (CNP) were determined by nuclear staining in both groups. Oocyte quality was further confirmed by calcein uptake and gene expression. The developmental competence of cumulus oocyte complexes derived from small size follicles that were cultured in the presence of CNP in combination with amphiregulin (AREG) and prostaglandin E2 (PGE2) for 24 h was determined. Finally, embryo quality was specified by assessing expressions of NANOG, SOX2, CDX2, OCT4, and TET1. The cumulus oocyte complexes derived from small size follicles had a lower capacity to form blastocyst in comparison with cumulus oocyte complexes derived from medium size follicles. Prostaglandin E receptor 2 and prostaglandin-endoperoxide synthase 2 had significantly lower expression in cumulus cells derived from small size follicles in comparison with cumulus cells derived from medium size follicles. Natriuretic peptide type C increased the percentage of cumulus oocyte complexes arresting at the germinal vesicle stage in both oocytes derived from medium and small follicles. Gap junction communication was also improved in the presence of natriuretic peptide type C. In oocytes derived from small size follicles; best blastocyst rates were achieved by sequential exposure of cumulus oocyte complexes in [TCM+CNP (6 h), then cultured in TCM+AREG+PGE2 (18h)] and [TCM+CNP (6 h), then cultured in conventional IVM supple-ments+AREG+PGE2 (18h)]. Increased SOX2 expression was observed in [TCM+CNP (6 h), then cultured in TCM+AREG+PGE2 (18h)], while decreased OCT4 expression was

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Prostaglandins in teleost ovulation: A review of the roles with a view to comparison with prostaglandins in mammalian ovulation

Cited by 58 publications

References 171 publications

Nuclear Progestin Receptor Phosphorylation by Cdk9 Is Required for the Expression of Mmp15, a Protease Indispensable for Ovulation in Medaka

Nuclear Progestin Receptor Phosphorylation by Cdk9 Is Required for the Expression of Mmp15, a Protease Indispensable for Ovulation in Medaka

Follicle rupture during ovulation with an emphasis on recent progress in fish models

Granulosa secreted factors improve the developmental competence of cumulus oocyte complexes from small antral follicles in sheep

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