Ustiloxin A impairs oocyte quality by disrupting organelles function

IF 7.6 2区环境科学与生态学 Q1 ENVIRONMENTAL SCIENCES

Environmental Pollution Pub Date : 2025-01-20 DOI:10.1016/j.envpol.2025.125733

Jun Han, Gang Wang, Xin Liu, You Zhou, Junqiang Hu, Yuzhuo Wu, Weikang Wang, Jianrong Shi, Jianhong Xu

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Abstract

Oocyte quality is pivotal for fertilization and early embryonic development. Ustiloxin A (UA), is an emerging mycotoxin that has been frequently detected in rice and paddy. Because UA has been reported to be phytotoxic and cytotoxic, it poses a potential hazard to human and animal health. However, the effects of UA on oocyte maturation remain unknown. Here, we investigated the effects of acute UA exposure on mouse oocyte maturation. First, UA exposure inhibited oocyte maturation in a concentration-dependent manner and induced meiotic arrest by disrupting spindle assembly and reducing actin density. Moreover, mitochondrial function was substantially disrupted in oocytes upon UA exposure. Aberrant mitochondrial distribution, substantial downregulation of mitochondrial dynamics-associated genes Mfn1, Mfn2 and Fis1, decreased membrane potential and TOM20 expression were observed in UA-exposed oocytes; these effects further led to oxidative stress and DNA damage. Furthermore, UA induced ER and Golgi dysfunction and triggered ER stress by increasing GRP78 expression, which ultimately resulted in autophagy and early apoptosis in oocytes. Therefore, these results demonstrate that UA impairs oocyte quality by disrupting organelles function, providing new insight into the influence of UA on female reproduction in mammals.

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Ustiloxin A通过破坏细胞器功能来损害卵母细胞的质量

卵母细胞质量对受精和早期胚胎发育至关重要。Ustiloxin A （UA）是一种在水稻和水稻中经常检测到的新型真菌毒素。由于UA已被报道具有植物毒性和细胞毒性，它对人类和动物健康构成潜在危害。然而，UA对卵母细胞成熟的影响尚不清楚。在这里，我们研究了急性UA暴露对小鼠卵母细胞成熟的影响。首先，UA暴露以浓度依赖的方式抑制卵母细胞成熟，并通过破坏纺锤体组装和降低肌动蛋白密度诱导减数分裂停滞。此外，暴露于UA后，卵母细胞的线粒体功能被严重破坏。暴露于ua的卵母细胞线粒体分布异常，线粒体动力学相关基因Mfn1、Mfn2和Fis1显著下调，膜电位和TOM20表达降低；这些影响进一步导致氧化应激和DNA损伤。此外，UA通过增加GRP78表达诱导内质网和高尔基体功能障碍，引发内质网应激，最终导致卵母细胞自噬和早期凋亡。因此，这些结果表明，UA通过破坏细胞器功能来损害卵母细胞质量，为UA对哺乳动物雌性生殖的影响提供了新的见解。

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

Environmental Pollution 环境科学-环境科学

CiteScore

16.00

自引率

6.70%

发文量

2082

审稿时长

2.9 months

期刊介绍： Environmental Pollution is an international peer-reviewed journal that publishes high-quality research papers and review articles covering all aspects of environmental pollution and its impacts on ecosystems and human health. Subject areas include, but are not limited to: • Sources and occurrences of pollutants that are clearly defined and measured in environmental compartments, food and food-related items, and human bodies; • Interlinks between contaminant exposure and biological, ecological, and human health effects, including those of climate change; • Contaminants of emerging concerns (including but not limited to antibiotic resistant microorganisms or genes, microplastics/nanoplastics, electronic wastes, light, and noise) and/or their biological, ecological, or human health effects; • Laboratory and field studies on the remediation/mitigation of environmental pollution via new techniques and with clear links to biological, ecological, or human health effects; • Modeling of pollution processes, patterns, or trends that is of clear environmental and/or human health interest; • New techniques that measure and examine environmental occurrences, transport, behavior, and effects of pollutants within the environment or the laboratory, provided that they can be clearly used to address problems within regional or global environmental compartments.