Abstract
Cathecolestrogens are estradiol metabolites produced during folliculogenesis in the mammalian ovary. 2-Hydroxyestradiol (2-OHE2) is one of the most abundant although its role remains unknown. The aim of this study is to investigate whether the presence of 2-OHE2 during the germinal vesicle-to-metaphase II transition affects oocyte meiotic and preimplantation developmental competence. Mouse cumulus-oocyte complexes (COCs), isolated from fully grown antral follicles, were in vitro–matured (IVM) in the presence of 2-OHE2 (0.1, 1, 10 or 100 nM) for 6 or 15 h; then, their meiotic and developmental competence was evaluated using a number of cytological quality markers. With the exception of the highest dose (100 nM), the addition of 2-OHE2 to the IVM medium, did not alter, compared with untreated control, the frequency of oocytes that reached the MII stage. Instead, IVM in the presence of 1 nM 2-OHE2 highly increased the rate of preimplantation development and blastocyst quality. To understand whether this positive effect could be attributed to the events occurring during meiosis resumption, we analysed a number of specific cytological quality markers of the asymmetric division, such as PB-I volume and position, presence and extension of the cortical F-actin cap, meiotic spindle shape and area, and microtubule organisation centre localisation. The results highlighted how the presence of 1 nM 2-OHE2 significantly improved the overall cytological organisation required for a correct asymmetric division. Our results contribute a first step to acknowledge a potential role of this estradiol metabolite during the GV-to-MII transition, contributing to the acquisition of oocytes developmental competence.
Highlights
The acquisition of the oocyte developmental competence occurs inside the ovarian follicle thanks to a continuous crosstalk between the germ cell and the surrounding cumulus and granulosa cells
Compared with the control in vitro–matured cumulus-oocyte complexes (COCs) (IVM) (Table 1), oocytes whose COCs were cultured in the presence of 2-OHE2 (IVM-2-OHE2), spontaneously resumed meiosis and reached metaphase II (MII) without significant differences (p > 0.05), with the exception of those treated with the highest 2-OHE2 concentration (100 nM) in which a decreased MII rate was observed (90.4 ± 1.5%; p = 0.015)
Compared with in vitro maturation (IVM) (28.6 ± 1.6%), 32.4 ± 4.7% (p = 0.283), 49.6 ± 1.2% (p < 0.001), 47.8 ± 4.9% (p < 0.001) and 29.2 ± 1.6% (p = 0.875) of 0.1 nM, 1 nM, 10 nM or 100 nM IVM-2OHE2-treated embryos reached the blastocyst stage, respectively
Summary
The acquisition of the oocyte developmental competence occurs inside the ovarian follicle thanks to a continuous crosstalk between the germ cell and the surrounding cumulus and granulosa cells. The follicle somatic cell components contribute crucial factors required, through several signalling pathways and regulatory loops, to complete oocyte growth and meiotic maturation [1, 2]. The importance to preserve the communication between oocyte and surrounding granulosa cells becomes evident when cumulus-oocyte complexes (COCs) are isolated from fully grown antral follicles and in vitro cultured [3, 4]. The efficiency of COCs in vitro maturation (IVM) varies depending on both strain (i.e., outbred or inbred) [5] and culture conditions [6, 7], the meiotic and developmental competence of metaphase II (MII) oocytes obtained in vitro remains lower compared with that of ovulated MII oocytes [8, 9]
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