Bisphenol B Exposure Disrupts Mouse Oocyte Meiotic Maturation in vitro Through Affecting Spindle Assembly and Chromosome Alignment

Bisphenol B (BPB), a substitute of bisphenol A (BPA), is widely used in the polycarbonate plastic and resins production. However, BPB proved to be not a safe alternative to BPA, and as an endocrine disruptor, it can harm the health of humans and animals. In the present study, we explored the effects...

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Main Authors: Shou-Xin Zhang, Zhi-Ming Ding, Muhammad Jamil Ahmad, Yong-Sheng Wang, Ze-Qun Duan, Yi-Liang Miao, Jia-Jun Xiong, Li-Jun Huo
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-12-01
Series:Frontiers in Cell and Developmental Biology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcell.2020.616771/full
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spelling doaj-ec61e9bbe005482787ba2fe4791eb4892020-12-17T06:22:49ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2020-12-01810.3389/fcell.2020.616771616771Bisphenol B Exposure Disrupts Mouse Oocyte Meiotic Maturation in vitro Through Affecting Spindle Assembly and Chromosome AlignmentShou-Xin Zhang0Shou-Xin Zhang1Zhi-Ming Ding2Muhammad Jamil Ahmad3Yong-Sheng Wang4Ze-Qun Duan5Yi-Liang Miao6Jia-Jun Xiong7Li-Jun Huo8Li-Jun Huo9Key Laboratory of Agricultural Animal Genetics, Breeding and Reproduction, Education Ministry of China, College of Animal Science and Technology, Huazhong Agricultural University, Wuhan, ChinaBiochip Laboratory, The Affiliated Yantai Yuhuangding Hospital of Qingdao University, Yantai, ChinaKey Laboratory of Agricultural Animal Genetics, Breeding and Reproduction, Education Ministry of China, College of Animal Science and Technology, Huazhong Agricultural University, Wuhan, ChinaKey Laboratory of Agricultural Animal Genetics, Breeding and Reproduction, Education Ministry of China, College of Animal Science and Technology, Huazhong Agricultural University, Wuhan, ChinaKey Laboratory of Agricultural Animal Genetics, Breeding and Reproduction, Education Ministry of China, College of Animal Science and Technology, Huazhong Agricultural University, Wuhan, ChinaKey Laboratory of Agricultural Animal Genetics, Breeding and Reproduction, Education Ministry of China, College of Animal Science and Technology, Huazhong Agricultural University, Wuhan, ChinaKey Laboratory of Agricultural Animal Genetics, Breeding and Reproduction, Education Ministry of China, College of Animal Science and Technology, Huazhong Agricultural University, Wuhan, ChinaKey Laboratory of Agricultural Animal Genetics, Breeding and Reproduction, Education Ministry of China, College of Animal Science and Technology, Huazhong Agricultural University, Wuhan, ChinaKey Laboratory of Agricultural Animal Genetics, Breeding and Reproduction, Education Ministry of China, College of Animal Science and Technology, Huazhong Agricultural University, Wuhan, ChinaHubei Province’s Engineering Research Center in Buffalo Breeding and Products, Wuhan, ChinaBisphenol B (BPB), a substitute of bisphenol A (BPA), is widely used in the polycarbonate plastic and resins production. However, BPB proved to be not a safe alternative to BPA, and as an endocrine disruptor, it can harm the health of humans and animals. In the present study, we explored the effects of BPB on mouse oocyte meiotic maturation in vitro. We found that 150 μM of BPB significantly compromised the first polar body extrusion (PBE) and disrupted the cell cycle progression with meiotic arrest. The spindle assembly and chromosome alignment were disordered after BPB exposure, which was further demonstrated by the aberrant localization of p-MAPK. Also, BPB exposure increased the acetylation levels of α-tubulin. As a result, the spindle assemble checkpoint (SAC) was continuously provoked, contributing to meiotic arrest. We further demonstrated that BPB severely induced DNA damage, but the ROS and ATP production were not altered. Furthermore, the epigenetic modifications were changed after BPB exposure, as indicated by increased K3K9me3 and H3K27me3 levels. Besides, the pattern of estrogen receptor α (ERα) dynamics was disrupted with a mass gathering on the spindle in BPB-exposed oocytes. Our collective results indicated that exposure to BPB compromised meiotic maturation and damaged oocyte quality by affecting spindle assembly and chromosome alignment, acetylation of α-tubulin, DNA damage, epigenetic modifications, and ERα dynamics in mouse oocytes.https://www.frontiersin.org/articles/10.3389/fcell.2020.616771/fullbisphenol Bspindle assemblychromosome alignmentDNA damageepigenetic modifications
collection DOAJ
language English
format Article
sources DOAJ
author Shou-Xin Zhang
Shou-Xin Zhang
Zhi-Ming Ding
Muhammad Jamil Ahmad
Yong-Sheng Wang
Ze-Qun Duan
Yi-Liang Miao
Jia-Jun Xiong
Li-Jun Huo
Li-Jun Huo
spellingShingle Shou-Xin Zhang
Shou-Xin Zhang
Zhi-Ming Ding
Muhammad Jamil Ahmad
Yong-Sheng Wang
Ze-Qun Duan
Yi-Liang Miao
Jia-Jun Xiong
Li-Jun Huo
Li-Jun Huo
Bisphenol B Exposure Disrupts Mouse Oocyte Meiotic Maturation in vitro Through Affecting Spindle Assembly and Chromosome Alignment
Frontiers in Cell and Developmental Biology
bisphenol B
spindle assembly
chromosome alignment
DNA damage
epigenetic modifications
author_facet Shou-Xin Zhang
Shou-Xin Zhang
Zhi-Ming Ding
Muhammad Jamil Ahmad
Yong-Sheng Wang
Ze-Qun Duan
Yi-Liang Miao
Jia-Jun Xiong
Li-Jun Huo
Li-Jun Huo
author_sort Shou-Xin Zhang
title Bisphenol B Exposure Disrupts Mouse Oocyte Meiotic Maturation in vitro Through Affecting Spindle Assembly and Chromosome Alignment
title_short Bisphenol B Exposure Disrupts Mouse Oocyte Meiotic Maturation in vitro Through Affecting Spindle Assembly and Chromosome Alignment
title_full Bisphenol B Exposure Disrupts Mouse Oocyte Meiotic Maturation in vitro Through Affecting Spindle Assembly and Chromosome Alignment
title_fullStr Bisphenol B Exposure Disrupts Mouse Oocyte Meiotic Maturation in vitro Through Affecting Spindle Assembly and Chromosome Alignment
title_full_unstemmed Bisphenol B Exposure Disrupts Mouse Oocyte Meiotic Maturation in vitro Through Affecting Spindle Assembly and Chromosome Alignment
title_sort bisphenol b exposure disrupts mouse oocyte meiotic maturation in vitro through affecting spindle assembly and chromosome alignment
publisher Frontiers Media S.A.
series Frontiers in Cell and Developmental Biology
issn 2296-634X
publishDate 2020-12-01
description Bisphenol B (BPB), a substitute of bisphenol A (BPA), is widely used in the polycarbonate plastic and resins production. However, BPB proved to be not a safe alternative to BPA, and as an endocrine disruptor, it can harm the health of humans and animals. In the present study, we explored the effects of BPB on mouse oocyte meiotic maturation in vitro. We found that 150 μM of BPB significantly compromised the first polar body extrusion (PBE) and disrupted the cell cycle progression with meiotic arrest. The spindle assembly and chromosome alignment were disordered after BPB exposure, which was further demonstrated by the aberrant localization of p-MAPK. Also, BPB exposure increased the acetylation levels of α-tubulin. As a result, the spindle assemble checkpoint (SAC) was continuously provoked, contributing to meiotic arrest. We further demonstrated that BPB severely induced DNA damage, but the ROS and ATP production were not altered. Furthermore, the epigenetic modifications were changed after BPB exposure, as indicated by increased K3K9me3 and H3K27me3 levels. Besides, the pattern of estrogen receptor α (ERα) dynamics was disrupted with a mass gathering on the spindle in BPB-exposed oocytes. Our collective results indicated that exposure to BPB compromised meiotic maturation and damaged oocyte quality by affecting spindle assembly and chromosome alignment, acetylation of α-tubulin, DNA damage, epigenetic modifications, and ERα dynamics in mouse oocytes.
topic bisphenol B
spindle assembly
chromosome alignment
DNA damage
epigenetic modifications
url https://www.frontiersin.org/articles/10.3389/fcell.2020.616771/full
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