Abstract
The ovarian follicle encloses oocytes in a microenvironment throughout their growth and acquisition of competence. Evidence suggests a dynamic interplay among follicular cells and oocytes, since they are constantly exchanging “messages”. We dissected bovine ovarian follicles and recovered follicular cells (FCs—granulosa and cumulus cells) and cumulus-oocyte complexes (COCs) to investigate whether the PI3K-Akt signaling pathway impacted oocyte quality. Following follicle rupture, COCs were individually selected for in vitro cultures to track the follicular cells based on oocyte competence to reach the blastocyst stage after parthenogenetic activation. Levels of PI3K-Akt signaling pathway components in FCs correlated with oocyte competence. This pathway is upregulated in FCs from follicles with high-quality oocytes that are able to reach the blastocyst stage, as indicated by decreased levels of PTEN and increased levels of the PTEN regulators bta-miR-494 and bta-miR-20a. Using PI3K-Akt responsive genes, we showed decreased FOXO3a levels and BAX levels in lower quality groups, indicating changes in cell cycle progression, oxidative response and apoptosis. Based on these results, the measurement of levels of PI3K-Akt pathway components in FCs from ovarian follicles carrying oocytes with distinct developmental competences is a useful tool to identify putative molecular pathways involved in the acquisition of oocyte competence.
Highlights
The success of in vitro production of bovine embryos is closely associated with oocyte quality [1, 2]
The relative abundance of the PTEN mRNA was significantly reduced (p < 0.05) in follicular cells (FCs) that originated from follicles containing oocytes capable of generating blastocysts in vitro compared to FCs that originated from follicles containing oocytes that did not reach this stage (Fig 1A)
We dissected ovarian follicles, stored FCs, and individually activated oocytes to evaluate their developmental competences and determine whether components of the PI3K-Akt pathway serve as predictors of oocyte quality
Summary
The success of in vitro production of bovine embryos is closely associated with oocyte quality [1, 2]. The oocyte’s competence to reach the blastocyst stage is progressively acquired during follicle growth [3], and is the result of interactions between external factors and the follicular microenvironment [4]. The PI3K-Akt pathway is related to oocyte competence oocyte, theca, granulosa, and cumulus cells, along with a basement membrane and follicular fluid. Each one of these cell types plays an active role in oocyte differentiation and regulation [5]. A reliable method for measuring oocyte competence prior to phenotype analysis following fertilization is not available
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