Abstract
Melatonin, a nighttime-secreted antioxidant hormone produced by the pineal gland, and AKT, a serine/threonine-specific protein kinase, have been identified as regulators for several cellular processes essential for reproduction. The current study aimed to investigate the potential interplay between melatonin and AKT in bovine oocytes in the context of embryo development. Results showed that the inclusion of SH6, a specific AKT inhibitor, during in vitro maturation (IVM) significantly reduced oocyte maturation, cumulus cell expansion, cleavage, and blastocyst development that were rescued upon addition of melatonin. Oocytes treated with SH6 in the presence of melatonin showed lower levels of reactive oxygen species (ROS) and blastocysts developed exhibited low apoptosis while the mitochondrial profile was significantly improved compared to the SH6-treated group. The RT-qPCR results showed up-regulation of the mRNA of maturation-, mitochondrial-, and cumulus expansion-related genes including GDF-9, BMP-15, MARF1, ATPase, ATP5F1E, POLG2, HAS2, TNFAIP6, and PTGS2 and down-regulation of Bcl-2 associated X apoptosis regulator (BAX), caspase 3, and p21 involved in apoptosis and cell cycle arrest in melatonin-SH6 co-treated group compared to SH6 sole treatment. The immunofluorescence showed high levels of caspase 3 and caspase 9, and low AKT phosphorylation in the SH6-treated group compared to the control and melatonin-SH6 co-treatment. Taken together, our results showed the importance of both melatonin and AKT for overall embryonic developmental processes and, for the first time, we report that melatonin could neutralize the deleterious consequences of AKT inhibition, suggesting a potential role in regulation of AKT signaling in bovine oocytes.
Highlights
Mammalian oocytes are naturally arrested in their follicles in a quiescent state known as the first meiotic prophase stage, the so-called germinal vesicle (GV) stage, whereas oocyte meiotic maturation refers to the process of transfer from the GV stage to metaphase II (MII) stage
It has been shown that melatonin protects oocytes and the developing embryos from the oxidative stress and nuclear fragmentation [45,46,47]
One possible mechanism is related to the direct function of melatonin as a potent antioxidant via scavenging the reactive oxygen species (ROS) and mitigating the pressure of oxidative stress in oocytes and developing embryos
Summary
Mammalian oocytes are naturally arrested in their follicles in a quiescent state known as the first meiotic prophase stage, the so-called germinal vesicle (GV) stage, whereas oocyte meiotic maturation refers to the process of transfer from the GV stage to metaphase II (MII) stage. The environment surrounding the oocytes, where the maturation and growth occur, plays an important role in the subsequent developmental processes including chromosomal condensation, cumulus cell expansion and progression from the first meiosis metaphase I (MI) to the second meiosis MII stage followed by arrest at MII stage until fertilization [1,2]. It has been reported that supplementation with certain hormones and antioxidants during IVM affects the developmental competence of bovine embryos via modulation of the PI3K/AKT signaling pathway [17,38,39,40]. The effect of melatonin supplementation on AKT signaling and developmental competence of SH6-treated oocytes was investigated. EEffffeecctt ooff mmeellaattoonniinn ttrreeaattmmeenntt dduurriinngg IIVVMM oonn tthhee ddeevveellooppmmeenntt ooff SSHH66--ttrreeaatteedd ooooccyytteess..
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