Abstract
Aging processes accelerate dramatically in oocytes that have reached the metaphase-II (M-II) stage. The present work aimed to study the patterns and intracellular pathways of actions of prolactin (PRL) and growth hormone (GH) on age-associated changes in bovine M-II oocytes aging in vitro. To this end, we analyzed spontaneous parthenogenetic activation (cytogenetic assay), apoptosis (TUNEL assay), and the developmental capacity (IVF/IVC) of in vitro-matured oocytes after prolonged culturing. Both PRL and GH reduced the activation rate of aging cumulus-enclosed oocytes (CEOs) and denuded oocytes (DOs), and their respective hormone receptors were revealed in the ova. The inhibitor of Src-family tyrosine kinases PP2 eliminated the effects of PRL and GH on meiotic arrest in DOs, whereas the MEK inhibitor U0126 only abolished the PRL effect. Furthermore, PRL was able to maintain the apoptosis resistance and developmental competence of aging CEOs. The protein kinase C inhibitor calphostin C suppressed both the actions of PRL. Thus, PRL and GH can directly support meiotic arrest in aging M-II oocytes by activating MAP kinases and/or Src-family kinases. The effect of PRL in maintaining the developmental capacity of aging oocytes is cumulus-dependent and related to the pro-survival action of the protein kinase C-mediated signal pathway.
Highlights
The developmental competence of mammalian oocytes depends on their quality
We have previously shown that the frequency of spontaneous parthenogenetic activation (SPA) reaches a maximum after 36 h of prolonged culturing of bovine cumulus-enclosed oocytes (CEOs), whereas it continues to increase between 36 h and 48 h in the case of denuded oocytes (DOs) [24]
The present research aimed to clarify the effects of two related hormones, PRL and growth hormone (GH), on SPA, apoptosis, and the developmental capacity of matured bovine oocytes during aging in vitro
Summary
The developmental competence of mammalian oocytes depends on their quality. Once the oocyte reaches the metaphase-II (M-II) stage, both in vivo and in vitro, it undergoes a time-dependent process of deterioration named postovulatory oocyte aging [1,2]. Postovulatory aging triggers different morphological and functional changes in oocytes, primarily spontaneous parthenogenetic activation (SPA), apoptosis, and abnormal transformations of organelles [2,3]. As a consequence, when fertilization or the artificial activation of the matured ovum fail to occur at the appropriate time, its quality is compromised, leading to impaired embryo development and offspring health [2,4,5]. The spontaneous activation and apoptosis associated with ovum aging are believed to be contributing to the decline in the population of some threatened mammalian species [8]
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