Melatonin protects porcine oocytes from gossypol-induced meiosis defects via regulation of SIRT1-mediated mitophagy

IF 3.9 3区医学 Q2 FOOD SCIENCE & TECHNOLOGY

Food and Chemical Toxicology Pub Date : 2024-11-20 DOI:10.1016/j.fct.2024.115122

Xiaoli Su , Yijing He , Heran Li, Tianhang Yu, Qinfeng Sun, Miaoyu Chen, Biao Zhang, Weihan Wang, Shiqiang Ju, Qiao Li

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Abstract

Cottonseed meal (CSM) is an ideal source of protein feed ingredients. However, the gossypol contained in it has toxic effects on animals, limiting its use in livestock production. The underlying mechanisms remain largely unknown. This study aimed to investigate the adverse effects of gossypol exposure and assess whether melatonin, a natural antioxidant, could alleviate oocyte damage induced by gossypol. Porcine cumulus oocyte complexes (COCs) were treated with gossypol alone or co-treated with melatonin for 44 h during in vitro maturation. The results demonstrated that gossypol exposure induced oxidative stress and mitochondrial dysfunction, leading to oocyte maturation failure. Conversely, melatonin co-treatment mitigated these detrimental effects, by promoting oocyte mitophagy, as evidenced by the upregulation of PINK1, Parkin, and LC3 expressions, along with the downregulation of P62. Further investigation revealed that gossypol treatment significantly decreased SIRT1 protein expression, while melatonin co-treatment markedly increased it. Using the SIRT1 inhibitor Ex527 confirmed that melatonin enhances mitophagy through SIRT1, improving mitochondrial function and rescuing oocyte maturation. This study revealed the potential harm of gossypol on mammalian reproductive health, provided experimental reference for the protective effect of melatonin, and provided theoretical basis for the effective prevention and treatment of reproductive damage caused by gossypol.

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褪黑素通过调节 SIRT1 介导的有丝分裂来保护猪卵母细胞免受棉酚诱导的减数分裂缺陷的影响。

棉籽粕（CSM）是蛋白质饲料原料的理想来源。然而，棉籽粕中含有的棉酚会对动物产生毒性作用，从而限制了棉籽粕在畜牧业生产中的使用。其潜在机制在很大程度上仍然未知。本研究旨在调查棉酚暴露的不良影响，并评估天然抗氧化剂褪黑素是否能减轻棉酚对卵母细胞的损伤。在猪卵母细胞体外成熟过程中，用棉酚单独或与褪黑素联合处理猪精原卵母细胞复合体（COCs）44小时。结果表明，棉酚暴露会诱发氧化应激和线粒体功能障碍，导致卵母细胞成熟失败。相反，褪黑素联合处理可通过促进卵母细胞的有丝分裂来减轻这些不利影响，这体现在 PINK1、Parkin 和 LC3 表达的上调以及 P62 的下调。进一步研究发现，棉酚处理会显著降低 SIRT1 蛋白表达，而褪黑素联合处理则会显著提高 SIRT1 蛋白表达。使用 SIRT1 抑制剂 Ex527 证实，褪黑素可通过 SIRT1 增强有丝分裂，改善线粒体功能并挽救卵母细胞成熟。该研究揭示了棉酚对哺乳动物生殖健康的潜在危害，为褪黑素的保护作用提供了实验参考，为有效预防和治疗棉酚对生殖健康的损害提供了理论依据。

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来源期刊

Food and Chemical Toxicology 工程技术-毒理学

CiteScore

10.90

自引率

4.70%

发文量

651

审稿时长

31 days

期刊介绍： Food and Chemical Toxicology (FCT), an internationally renowned journal, that publishes original research articles and reviews on toxic effects, in animals and humans, of natural or synthetic chemicals occurring in the human environment with particular emphasis on food, drugs, and chemicals, including agricultural and industrial safety, and consumer product safety. Areas such as safety evaluation of novel foods and ingredients, biotechnologically-derived products, and nanomaterials are included in the scope of the journal. FCT also encourages submission of papers on inter-relationships between nutrition and toxicology and on in vitro techniques, particularly those fostering the 3 Rs. The principal aim of the journal is to publish high impact, scholarly work and to serve as a multidisciplinary forum for research in toxicology. Papers submitted will be judged on the basis of scientific originality and contribution to the field, quality and subject matter. Studies should address at least one of the following: -Adverse physiological/biochemical, or pathological changes induced by specific defined substances -New techniques for assessing potential toxicity, including molecular biology -Mechanisms underlying toxic phenomena -Toxicological examinations of specific chemicals or consumer products, both those showing adverse effects and those demonstrating safety, that meet current standards of scientific acceptability. Authors must clearly and briefly identify what novel toxic effect (s) or toxic mechanism (s) of the chemical are being reported and what their significance is in the abstract. Furthermore, sufficient doses should be included in order to provide information on NOAEL/LOAEL values.