Evidence of melatonin synthesis in the cumulus oocyte complexes and its role in enhancing oocyte maturation in vitro in cattle

Abstract

Melatonin is a multifunctional molecule that mediates several circadian and seasonal reproductive processes. The exact role of melatonin in modulating reproduction, however, is not fully understood-especially its effects on the ovarian follicles and oocytes. This study was conducted to investigate the expressions of the ASMT and melatonin-receptor MTNR1A and MTNR1B genes in bovine oocytes and their cumulus cells, as well as the effects of melatonin on oocyte nuclear and cytoplasmic maturation in vitro. Cumulus-oocyte complexes (COCs) from abattoir ovaries were cultured in TCM-199 supplemented with melatonin at concentrations of 0, 10, 50, and 100 ng/ml. The expression of ASMT, MTNR1A, and MTNR1B genes was evaluated by RT-PCR. Moreover, the effects of melatonin on cumulus cell expansion, nuclear maturation, mitochondrial characteristics and COCs steroidogenesis were investigated. Furthermore, the level of reactive oxygen species (ROS) was evaluated in denuded oocytes. Our study revealed that ASMT and MTNR1A genes were expressed in COCs, while the MTNR1B gene was expressed only in oocytes. Additionally, melatonin supplementation at 10 and 50 ng/ml to in vitro maturation medium significantly enhanced oocyte nuclear maturation, cumulus cell expansion and altered the mitochondrial distribution patterns, but had no effects on oocyte mitochondrial activity and COCs steroidogenesis. Melatonin-treated oocytes had a significantly lower level of ROS than controls. The presence of melatonin receptors in COCs and its promoting effects on oocyte nuclear and cytoplasmic events, indicate the potentially important roles of this hormone in regulating bovine oocyte maturation. Moreover, the presence of ASMT transcript in COCs suggests the possible involvement of these cells in melatonin biosynthesis.

Melatonin modulates the expression of BCL-xl and improve the development of vitrified embryos obtained by IVF in mice

“…Previous studies have shown the expression of melatonin MT1 receptors in oocytes, cumulus cells and bovine blastocysts [50,51]. Studies on other species have shown the presence of MT1 receptor transcripts in porcine cumulus cells and granulosa cells but not in oocytes [22].…”

“…However, in some cells, melatonin causes stimulation of cAMP, and this stimulatory effect is independent of G proteins [53]. Activation of MT1 receptor stimulates phosphoinositide turnover and inhibits the guanylate cyclase enzyme and can induce PKC activation by Ca2+ waves, in parallel with the inhibition of the cAMP pathways [22,50,51]. Cellular signaling of melatonin receptors needs further investigations to understand the melatonin role in preimplantation development.…”

Melatonin receptor (MTNR1A and MTNR2B) expression during the breeding season in the yak (Bos grunniens)

“…Reactive oxygen species (ROS) and apoptosis are involved with a number of reproductive events, including folliculogenesis, follicular atresia, ovulation, oocyte maturation, and corpus luteum (CL) formation (Tamura et al, 2009). The ROS produced within the follicles, especially during the ovulation process, were scavenged by melatonin and reduced oxidative stress may be involved with oocyte maturation and embryo development (El-Raey et al, 2011;Tamura et al, 2012). We suggest that melatonin was involved with the growth and maturation of ovarian follicles and it also participated in the growth of oocytes.…”

“…Melatonin has an important role in the maturation of oocytes where the melatonin receptor 1A (MTNR1A) genes are expressed in the cumulus-oocytes complex, whereas the MTNR1B gene is expressed only in the oocytes. Melatonin can enhance the maturation of oocytes in vitro (Berlinguer et al, 2009;Kang et al, 2009;El-Raey et al, 2011). There was a positive correlation between MTNR1A allele polymorphisms and reproduction in the Sarda sheep breed (Carcangiu et al, 2009(Carcangiu et al, , 2011.…”

Melatonin in human reproduction

“…Мелатонин был обнаружен в текаклетках и клет-ках гранулезы, где экспрессируются его рецепторы МТ1 и МТ2 [15,16]. Эти рецепторы могут участво-вать в регуляции секреции эстрогена и прогестерона фолликулярными клетками гранулезы.…”