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Mitochondria of Porcine Oocytes Synthesize Melatonin, Which Improves Their In Vitro Maturation and Embryonic Development

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Date 2024 Jul 27
PMID 39061883
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Abstract

The in vitro maturation efficiency of porcine oocytes is relatively low, and this limits the production of in vitro porcine embryos. Since melatonin is involved in mammalian reproductive physiology, in this study, we have explored whether endogenously produced melatonin can help in porcine oocyte in vitro maturation. We have found, for the first time in the literature, that mitochondria are the major sites for melatonin biosynthesis in porcine oocytes. This mitochondrially originated melatonin reduces ROS production and increases the activity of the mitochondrial respiratory electron transport chain, mitochondrial biogenesis, mitochondrial membrane potential, and ATP production. Therefore, melatonin improves the quality of oocytes and their in vitro maturation. In contrast, the reduced melatonin level caused by siRNA to knockdown (siAANAT) is associated with the abnormal distribution of mitochondria, decreasing the ATP level of porcine oocytes and inhibiting their in vitro maturation. These abnormalities can be rescued by melatonin supplementation. In addition, we found that siAANAT switches the mitochondrial oxidative phosphorylation to glycolysis, a Warburg effect. This metabolic alteration can also be corrected by melatonin supplementation. All these activities of melatonin appear to be mediated by its membrane receptors since the non-selective melatonin receptor antagonist Luzindole can blunt the effects of melatonin. Taken together, the mitochondria of porcine oocytes can synthesize melatonin and improve the quality of oocyte maturation. These results provide an insight from a novel aspect to study oocyte maturation under in vitro conditions.

References
1.
Zeng H, Ren Z, Yeung W, Shu Y, Xu Y, Zhuang G . Low mitochondrial DNA and ATP contents contribute to the absence of birefringent spindle imaged with PolScope in in vitro matured human oocytes. Hum Reprod. 2007; 22(6):1681-6. DOI: 10.1093/humrep/dem070. View

2.
Yuan Y, Spate L, Redel B, Tian Y, Zhou J, Prather R . Quadrupling efficiency in production of genetically modified pigs through improved oocyte maturation. Proc Natl Acad Sci U S A. 2017; 114(29):E5796-E5804. PMC: 5530680. DOI: 10.1073/pnas.1703998114. View

3.
Dumollard R, Campbell K, Halet G, Carroll J, Swann K . Regulation of cytosolic and mitochondrial ATP levels in mouse eggs and zygotes. Dev Biol. 2008; 316(2):431-40. DOI: 10.1016/j.ydbio.2008.02.004. View

4.
Kala M, Vaseem Shaikh M, Nivsarkar M . Equilibrium between anti-oxidants and reactive oxygen species: a requisite for oocyte development and maturation. Reprod Med Biol. 2017; 16(1):28-35. PMC: 5715868. DOI: 10.1002/rmb2.12013. View

5.
Graveleau C, Paust H, Mukhopadhyay A . Presence of a 5-HT7 receptor positively coupled to adenylate cyclase activation in human granulosa-lutein cells. J Clin Endocrinol Metab. 2000; 85(3):1277-86. DOI: 10.1210/jcem.85.3.6448. View