1-Nitropyrene exposure induces mitochondria dysfunction and impairs oocyte maturation in mice

Oocyte quality is essential for a successful pregnancy. 1-Nitropyrene (1-NP) is a widely distributed pollutant in the environment and is well-known for its mutagenicity and carcinogenicity. However, whether 1-NP has toxic effects on mammalian oocyte quality remains unknown. In the present study, we...

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Main Authors: Xiaoxia Yu, Fei Meng, Ju Huang, Weidong Li, Jiaming Zhang, Shen Yin, Liangran Zhang, Shunxin Wang
Format: Article
Language:English
Published: Elsevier 2022-09-01
Series:Ecotoxicology and Environmental Safety
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0147651322007618
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author Xiaoxia Yu
Fei Meng
Ju Huang
Weidong Li
Jiaming Zhang
Shen Yin
Liangran Zhang
Shunxin Wang
author_facet Xiaoxia Yu
Fei Meng
Ju Huang
Weidong Li
Jiaming Zhang
Shen Yin
Liangran Zhang
Shunxin Wang
author_sort Xiaoxia Yu
collection DOAJ
description Oocyte quality is essential for a successful pregnancy. 1-Nitropyrene (1-NP) is a widely distributed pollutant in the environment and is well-known for its mutagenicity and carcinogenicity. However, whether 1-NP has toxic effects on mammalian oocyte quality remains unknown. In the present study, we focused on the effect of 1-NP on oocyte maturation using mouse oocytes as an in vitro model. Our study showed that 1-NP exposure disrupted the meiotic spindle assembly and caused chromosome misalignment, further impaired first polar body extrusion, and significantly decreased the fertilization capability in mouse oocytes. Further investigation showed that the mitochondrial membrane potential (MMP) and ATP levels were decreased, and the expression of genes encoding components of the mitochondrial respiratory chain was inhibited in 1-NP exposed oocytes. Meanwhile, 1-NP exposure increased the levels of reactive oxygen species (ROS), inhibited the expression of genes encoding antioxidant enzymes, and increased the frequency of early apoptotic oocytes. Overall, our data suggest that 1-NP exposure disrupts mitochondrial function and intracellular redox balance, ultimately impairing oocyte maturation. These findings reveal the adverse effect of 1-NP exposure on oocyte quality.
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spelling doaj.art-7afa4262eb0148108fdaef3faeb1f0312022-12-22T03:44:45ZengElsevierEcotoxicology and Environmental Safety0147-65132022-09-012421139211-Nitropyrene exposure induces mitochondria dysfunction and impairs oocyte maturation in miceXiaoxia Yu0Fei Meng1Ju Huang2Weidong Li3Jiaming Zhang4Shen Yin5Liangran Zhang6Shunxin Wang7Center for Reproductive Medicine, Cheeloo College of Medicine, Shandong University, China; National Research Center for Assisted Reproductive Technology and Reproductive Genetics, Shandong University, Jinan, Shandong 250012, China; Key Laboratory of Reproductive Endocrinology of Ministry of Education, Jinan, Shandong 250001, China; Shandong Provincial Clinical Research Center for Reproductive Health, Jinan, Shandong 250012, ChinaCenter for Reproductive Medicine, Cheeloo College of Medicine, Shandong University, China; National Research Center for Assisted Reproductive Technology and Reproductive Genetics, Shandong University, Jinan, Shandong 250012, China; Key Laboratory of Reproductive Endocrinology of Ministry of Education, Jinan, Shandong 250001, China; Shandong Provincial Clinical Research Center for Reproductive Health, Jinan, Shandong 250012, ChinaCenter for Reproductive Medicine, Cheeloo College of Medicine, Shandong University, China; National Research Center for Assisted Reproductive Technology and Reproductive Genetics, Shandong University, Jinan, Shandong 250012, China; Key Laboratory of Reproductive Endocrinology of Ministry of Education, Jinan, Shandong 250001, China; Shandong Provincial Clinical Research Center for Reproductive Health, Jinan, Shandong 250012, ChinaAdvanced Medical Research Institute, Shandong University, Jinan, Shandong 250012, ChinaCenter for Reproductive Medicine, Cheeloo College of Medicine, Shandong University, China; National Research Center for Assisted Reproductive Technology and Reproductive Genetics, Shandong University, Jinan, Shandong 250012, China; Key Laboratory of Reproductive Endocrinology of Ministry of Education, Jinan, Shandong 250001, China; Shandong Provincial Clinical Research Center for Reproductive Health, Jinan, Shandong 250012, ChinaCollege of Life Sciences, Institute of Reproductive Sciences, Qingdao Agricultural University, Qingdao, ChinaAdvanced Medical Research Institute, Shandong University, Jinan, Shandong 250012, China; Center for Cell Structure and Function, Shandong Provincial Key Laboratory of Animal Resistance Biology, College of Life Sciences, Shandong Normal University, Jinan 250014, Shandong, ChinaCenter for Reproductive Medicine, Cheeloo College of Medicine, Shandong University, China; National Research Center for Assisted Reproductive Technology and Reproductive Genetics, Shandong University, Jinan, Shandong 250012, China; Key Laboratory of Reproductive Endocrinology of Ministry of Education, Jinan, Shandong 250001, China; Shandong Provincial Clinical Research Center for Reproductive Health, Jinan, Shandong 250012, China; Corresponding author at: Center for Reproductive Medicine, Cheeloo College of Medicine, Shandong University, China.Oocyte quality is essential for a successful pregnancy. 1-Nitropyrene (1-NP) is a widely distributed pollutant in the environment and is well-known for its mutagenicity and carcinogenicity. However, whether 1-NP has toxic effects on mammalian oocyte quality remains unknown. In the present study, we focused on the effect of 1-NP on oocyte maturation using mouse oocytes as an in vitro model. Our study showed that 1-NP exposure disrupted the meiotic spindle assembly and caused chromosome misalignment, further impaired first polar body extrusion, and significantly decreased the fertilization capability in mouse oocytes. Further investigation showed that the mitochondrial membrane potential (MMP) and ATP levels were decreased, and the expression of genes encoding components of the mitochondrial respiratory chain was inhibited in 1-NP exposed oocytes. Meanwhile, 1-NP exposure increased the levels of reactive oxygen species (ROS), inhibited the expression of genes encoding antioxidant enzymes, and increased the frequency of early apoptotic oocytes. Overall, our data suggest that 1-NP exposure disrupts mitochondrial function and intracellular redox balance, ultimately impairing oocyte maturation. These findings reveal the adverse effect of 1-NP exposure on oocyte quality.http://www.sciencedirect.com/science/article/pii/S0147651322007618Oocyte maturationMitochondriaOxidative stressApoptosisIn vitro fertilization
spellingShingle Xiaoxia Yu
Fei Meng
Ju Huang
Weidong Li
Jiaming Zhang
Shen Yin
Liangran Zhang
Shunxin Wang
1-Nitropyrene exposure induces mitochondria dysfunction and impairs oocyte maturation in mice
Ecotoxicology and Environmental Safety
Oocyte maturation
Mitochondria
Oxidative stress
Apoptosis
In vitro fertilization
title 1-Nitropyrene exposure induces mitochondria dysfunction and impairs oocyte maturation in mice
title_full 1-Nitropyrene exposure induces mitochondria dysfunction and impairs oocyte maturation in mice
title_fullStr 1-Nitropyrene exposure induces mitochondria dysfunction and impairs oocyte maturation in mice
title_full_unstemmed 1-Nitropyrene exposure induces mitochondria dysfunction and impairs oocyte maturation in mice
title_short 1-Nitropyrene exposure induces mitochondria dysfunction and impairs oocyte maturation in mice
title_sort 1 nitropyrene exposure induces mitochondria dysfunction and impairs oocyte maturation in mice
topic Oocyte maturation
Mitochondria
Oxidative stress
Apoptosis
In vitro fertilization
url http://www.sciencedirect.com/science/article/pii/S0147651322007618
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