Supplementation of spermidine enhances the quality of postovulatory aged porcine oocytes.

IF 8.2 2区生物学 Q1 CELL BIOLOGY Cell Communication and Signaling Pub Date : 2024-10-15 DOI:10.1186/s12964-024-01881-7

Jie Bai, Yu Zhang, Na Li, Zhaokang Cui, Hanwen Zhang, Yiting Liu, Yilong Miao, Shaochen Sun, Bo Xiong

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Abstract

Background: Spermidine (SPD) is an intermediate compound in the polyamine metabolism which takes critical part in a variety of cellular processes. In particular, it has been reported to exert anti-aging effects, suppress the age-related diseases, and extend lifespan across species. However, whether it has the favorable influence on the quality of postovulatory aged oocytes remains elusive.

Methods: Immunostaining and fluorescence intensity measurement were used to evaluate the effects of postovulatory aging and SPD supplementation on the oocyte fragmentation, spindle/chromosome structure, actin polymerization, dynamics of cortical granules (CGs) and ovastacin, mitochondrial distribution and function, as well as autophagy levels. In addition, in vitro sperm binding assay and in vitro fertilization (IVF) experiment were applied to assess the impacts of postovulatory aging and SPD supplementation on the sperm binding ability and fertilization capacity of oocytes.

Results: Here, we showed that supplementation of SPD during postovulatory aging could relieve the deterioration of porcine oocytes. Specifically, we found that postovulatory aging impaired the oocyte quality by damaging the morphological integrity of oocytes, maintenance of spindle/chromosome structure, and dynamics of actin cytoskeleton. Postovulatory aging also weakened the sperm binding ability and fertilization capacity of oocytes by compromising the distribution pattern of CGs and their content ovastacin. Notably, supplementation of SPD attenuated these defects in postovulatory aged porcine oocytes via strengthening mitochondrial function, eliminating excessive reactive oxygen species (ROS), inhibiting apoptosis, and enhancing autophagy levels.

Conclusion: Altogether, our findings demonstrate that SPD supplementation is a feasible approach to ameliorate the quality of postovulatory aged oocytes, which can be potentially applied to the human assisted reproductive technology (ART) and in vitro production of animal embryos.

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补充亚精胺可提高排卵后高龄猪卵母细胞的质量。

背景：精胺（SPD）是多胺代谢的一种中间化合物，在多种细胞过程中发挥着关键作用。特别是，有报道称它具有抗衰老作用，可抑制与年龄有关的疾病，并延长不同物种的寿命。然而，它是否会对排卵后高龄卵母细胞的质量产生有利影响，目前仍无定论：免疫染色法和荧光强度测量法评估了排卵后衰老和补充SPD对卵母细胞破碎、纺锤体/染色体结构、肌动蛋白聚合、皮质颗粒（CGs）和卵黄素动态、线粒体分布和功能以及自噬水平的影响。此外，还应用体外精子结合试验和体外受精（IVF）实验来评估排卵后衰老和补充SPD对卵母细胞精子结合能力和受精能力的影响：结果：我们发现在排卵后衰老过程中补充SPD可以缓解猪卵母细胞的衰退。具体来说，我们发现排卵后衰老会损害卵母细胞的形态完整性、纺锤体/染色体结构的维持以及肌动蛋白细胞骨架的动态，从而影响卵母细胞的质量。排卵后衰老还通过损害CG的分布模式及其含量卵磷脂来削弱卵母细胞的精子结合能力和受精能力。值得注意的是，补充 SPD 可通过增强线粒体功能、消除过多的活性氧（ROS）、抑制细胞凋亡和提高自噬水平来减轻排卵后衰老猪卵母细胞的这些缺陷：总之，我们的研究结果表明，补充 SPD 是改善排卵后高龄卵母细胞质量的一种可行方法，可用于人类辅助生殖技术（ART）和动物胚胎的体外生产。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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来源期刊

Cell Communication and Signaling CELL BIOLOGY-

CiteScore

11.00

自引率

0.00%

发文量

180

期刊介绍： Cell Communication and Signaling (CCS) is a peer-reviewed, open-access scientific journal that focuses on cellular signaling pathways in both normal and pathological conditions. It publishes original research, reviews, and commentaries, welcoming studies that utilize molecular, morphological, biochemical, structural, and cell biology approaches. CCS also encourages interdisciplinary work and innovative models, including in silico, in vitro, and in vivo approaches, to facilitate investigations of cell signaling pathways, networks, and behavior. Starting from January 2019, CCS is proud to announce its affiliation with the International Cell Death Society. The journal now encourages submissions covering all aspects of cell death, including apoptotic and non-apoptotic mechanisms, cell death in model systems, autophagy, clearance of dying cells, and the immunological and pathological consequences of dying cells in the tissue microenvironment.