Abstract
In the present study, we investigated the potential role of glucose and pyruvate in the cytoplasmic maturation of porcine oocytes by investigating the effect of glucose and/or pyruvate supplementation, in the presence or absence of 10% porcine follicular fluid (PFF), on meiotic maturation and subsequent embryo development. In the absence of 10% PFF, without exogenous addition of glucose and pyruvate, the medium seemed unable to support maturation. In the presence of 10% PFF, the addition of 5.6 mM glucose and/or 2 mM pyruvate during in vitro maturation of cumulus enclosed oocytes increased MII oocyte and blastocyst rates. In contrast, oocytes denuded of cumulus cells were not able to take full advantage of the glucose in the medium, as only pyruvate was able to increase the MII rate and the subsequent early embryo developmental ability. Treatment of cumulus enclosed oocytes undergoing maturation with 200 μM dehydroepiandrosterone (DHEA), a pentose phosphate pathway inhibitor, or 2 μM iodoacetate (IA), a glycolysis inhibitor, significantly reduced GHS, intra-oocyte ATP, maternal gene expression, and MPF activity levels. DHEA was also able to increase ROS and reduce the levels of NADPH. Moreover, blastocysts of the DHEA- or IA-treated groups presented higher apoptosis rates and markedly lower cell proliferation cell rates than those of the non-treated group. In conclusion, our results suggest that oocytes maturing in the presence of 10% PFF can make full use of energy sources through glucose metabolism only when they are accompanied by cumulus cells, and that pentose phosphate pathway (PPP) and glycolysis promote porcine oocyte cytoplasmic maturation by supplying energy, regulating maternal gene expression, and controlling MPF activity.
Highlights
In a variety of mammals, glucose metabolism and pyruvate play an important role in oocyte maturation and subsequent early embryonic development [1,2,3]
COCs maturated in the presence of 10% porcine follicular fluid (PFF), with or without glucose and/or pyruvate supplementation, were able to reach oocyte nuclear maturation and embryo development
The presence of 5.6 mM glucose and/or 2 mM pyruvate significantly increased MII-stage oocyte and embryo rates, suggesting that energy metabolism is critical to oocyte maturation and subsequent embryo development
Summary
In a variety of mammals, glucose metabolism and pyruvate play an important role in oocyte maturation and subsequent early embryonic development [1,2,3]. In an in vitro oocyte culture system, a decrease in glucose concentration was shown to significantly inhibit meiotic divisions, subcapsular maturation, and subsequent embryonic development in bubaline and PLOS ONE | DOI:10.1371/journal.pone.0168329. The addition of a sufficient amount of glucose to the IVM medium significantly enhances IVM and subsequent developmental capacity of bovine and porcine oocytes [6,7,8]. PPP and/or glycolysis appear to play a key role in the resumption of meiosis in mouse oocytes [1, 10]. High concentrations of glucose in the IVM medium can inhibit oocyte maturation [9]
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