Methoxychlor induces oxidative stress and impairs early embryonic development in pigs

Introduction: Methoxychlor (MXC) is an organochlorine pesticide (OCP) that was formerly used worldwide as an insecticide against pests and mosquitoes. However, MXC is not biodegradable and has lipophilic characteristics; thus, it accumulates in organisms and affects reproductive function. MXC, as an...

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Main Authors: Zhaojun Geng, Yongxun Jin, Fushi Quan, Siyi Huang, Shuming Shi, Bing Hu, Zhichao Chi, Ilkeun Kong, Mingjun Zhang, Xianfeng Yu
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-12-01
Series:Frontiers in Cell and Developmental Biology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcell.2023.1325406/full
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author Zhaojun Geng
Yongxun Jin
Fushi Quan
Siyi Huang
Shuming Shi
Bing Hu
Zhichao Chi
Ilkeun Kong
Ilkeun Kong
Mingjun Zhang
Xianfeng Yu
author_facet Zhaojun Geng
Yongxun Jin
Fushi Quan
Siyi Huang
Shuming Shi
Bing Hu
Zhichao Chi
Ilkeun Kong
Ilkeun Kong
Mingjun Zhang
Xianfeng Yu
author_sort Zhaojun Geng
collection DOAJ
description Introduction: Methoxychlor (MXC) is an organochlorine pesticide (OCP) that was formerly used worldwide as an insecticide against pests and mosquitoes. However, MXC is not biodegradable and has lipophilic characteristics; thus, it accumulates in organisms and affects reproductive function. MXC, as an estrogenic compound, promotes oxidative stress, induces oxidative stress damage to ovarian follicles, and causes miscarriages and stillbirths in females. In this research endeavor, our primary objective was to explore the ramifications of MXC regarding the developmental processes occurring during the initial stages of embryogenesis in pigs.Methods: In this study, we counted the blastocyst rate of early embryos cultured in vitro. We also examined the reactive oxygen species level, glutathione level, mitochondrial membrane potential, mitochondrial copy number and ATP level in four-cell stage embryos. Finally, apoptosis and DNA damage in blastocyst cells, as well as pluripotency-related and apoptosis-related genes in blastocyst cells were detected. The above experiments were used to evaluate the changes of MXC damage on early parthenogenetic embryo development.Results and Discussion: The results showed that early embryos exposed to MXC had a significantly lower cleavage rate, blastocyst rate, hatching rate, and total cell count compared with the control group. It was also of note that MXC not only increased the levels of reactive oxygen species (ROS), but also decreased the mitochondrial membrane potential (ΔΨm) and mitochondrial copy number during the development of early embryos. In addition, after MXC treatment, blastocyst apoptosis and DNA damage were increased, decreased cell proliferation, and the expression of pluripotency-related genes SOX2, NANOG, and OCT4 was down-regulated, while the expression of apoptosis-related genes BAX/BCL-2 and Caspase9 was up-regulated. Our results clearly show that MXC can have deleterious effects on the developmental processes of early porcine embryos, establishing the toxicity of MXC to the reproductive system. In addition, the study of this toxic effect may lead to greater concern about pesticide residues in humans and the use of safer pesticides, thus potentially preventing physiological diseases caused by chemical exposure.
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spelling doaj.art-823c5875ad2b4e2d8d32ceb3aa0938052023-12-01T18:48:57ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2023-12-011110.3389/fcell.2023.13254061325406Methoxychlor induces oxidative stress and impairs early embryonic development in pigsZhaojun Geng0Yongxun Jin1Fushi Quan2Siyi Huang3Shuming Shi4Bing Hu5Zhichao Chi6Ilkeun Kong7Ilkeun Kong8Mingjun Zhang9Xianfeng Yu10Jilin Provincial Key Laboratory of Animal Model, College of Animal Science, Jilin University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Model, College of Animal Science, Jilin University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Model, College of Animal Science, Jilin University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Model, College of Animal Science, Jilin University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Model, College of Animal Science, Jilin University, Changchun, ChinaAnimal Genome Editing Technology Innovation Center, College of Animal Science, Jilin University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Model, College of Animal Science, Jilin University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Model, College of Animal Science, Jilin University, Changchun, ChinaDepartment of Animal Science, Division of Applied Life Science (BK21 Four), Gyeongsang National University, Jinju, Republic of KoreaAnimal Genome Editing Technology Innovation Center, College of Animal Science, Jilin University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Model, College of Animal Science, Jilin University, Changchun, ChinaIntroduction: Methoxychlor (MXC) is an organochlorine pesticide (OCP) that was formerly used worldwide as an insecticide against pests and mosquitoes. However, MXC is not biodegradable and has lipophilic characteristics; thus, it accumulates in organisms and affects reproductive function. MXC, as an estrogenic compound, promotes oxidative stress, induces oxidative stress damage to ovarian follicles, and causes miscarriages and stillbirths in females. In this research endeavor, our primary objective was to explore the ramifications of MXC regarding the developmental processes occurring during the initial stages of embryogenesis in pigs.Methods: In this study, we counted the blastocyst rate of early embryos cultured in vitro. We also examined the reactive oxygen species level, glutathione level, mitochondrial membrane potential, mitochondrial copy number and ATP level in four-cell stage embryos. Finally, apoptosis and DNA damage in blastocyst cells, as well as pluripotency-related and apoptosis-related genes in blastocyst cells were detected. The above experiments were used to evaluate the changes of MXC damage on early parthenogenetic embryo development.Results and Discussion: The results showed that early embryos exposed to MXC had a significantly lower cleavage rate, blastocyst rate, hatching rate, and total cell count compared with the control group. It was also of note that MXC not only increased the levels of reactive oxygen species (ROS), but also decreased the mitochondrial membrane potential (ΔΨm) and mitochondrial copy number during the development of early embryos. In addition, after MXC treatment, blastocyst apoptosis and DNA damage were increased, decreased cell proliferation, and the expression of pluripotency-related genes SOX2, NANOG, and OCT4 was down-regulated, while the expression of apoptosis-related genes BAX/BCL-2 and Caspase9 was up-regulated. Our results clearly show that MXC can have deleterious effects on the developmental processes of early porcine embryos, establishing the toxicity of MXC to the reproductive system. In addition, the study of this toxic effect may lead to greater concern about pesticide residues in humans and the use of safer pesticides, thus potentially preventing physiological diseases caused by chemical exposure.https://www.frontiersin.org/articles/10.3389/fcell.2023.1325406/fullmethoxychlorROSembryoapoptosispig
spellingShingle Zhaojun Geng
Yongxun Jin
Fushi Quan
Siyi Huang
Shuming Shi
Bing Hu
Zhichao Chi
Ilkeun Kong
Ilkeun Kong
Mingjun Zhang
Xianfeng Yu
Methoxychlor induces oxidative stress and impairs early embryonic development in pigs
Frontiers in Cell and Developmental Biology
methoxychlor
ROS
embryo
apoptosis
pig
title Methoxychlor induces oxidative stress and impairs early embryonic development in pigs
title_full Methoxychlor induces oxidative stress and impairs early embryonic development in pigs
title_fullStr Methoxychlor induces oxidative stress and impairs early embryonic development in pigs
title_full_unstemmed Methoxychlor induces oxidative stress and impairs early embryonic development in pigs
title_short Methoxychlor induces oxidative stress and impairs early embryonic development in pigs
title_sort methoxychlor induces oxidative stress and impairs early embryonic development in pigs
topic methoxychlor
ROS
embryo
apoptosis
pig
url https://www.frontiersin.org/articles/10.3389/fcell.2023.1325406/full
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