Bisphenol Z exposure inhibits oocyte meiotic maturation by rupturing mitochondrial function
The use of bisphenol A (BPA) has been restricted due to its endocrine-disrupting effects. As a widely used alternative to BPA today, environmental levels of bisphenol Z (BPZ) continue to rise and accumulate in humans. Oocyte quality is critical for a successful pregnancy. Nevertheless, the toxic imp...
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| Format: | Article |
| Language: | English |
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Elsevier
2024-05-01
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| Series: | Ecotoxicology and Environmental Safety |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S0147651324003889 |
| _version_ | 1797210129867735040 |
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| author | Cong Ma Yan Xu Huilei Chen Yue Huang Shanshan Wang Pin Zhang Guojing Li Zuying Xu Xiaofeng Xu Zhiming Ding Huifen Xiang Yunxia Cao |
| author_facet | Cong Ma Yan Xu Huilei Chen Yue Huang Shanshan Wang Pin Zhang Guojing Li Zuying Xu Xiaofeng Xu Zhiming Ding Huifen Xiang Yunxia Cao |
| author_sort | Cong Ma |
| collection | DOAJ |
| description | The use of bisphenol A (BPA) has been restricted due to its endocrine-disrupting effects. As a widely used alternative to BPA today, environmental levels of bisphenol Z (BPZ) continue to rise and accumulate in humans. Oocyte quality is critical for a successful pregnancy. Nevertheless, the toxic impacts of BPZ on the maturation of mammalian oocytes remain unexplored. Therefore, the impacts of BPZ and BPA on oocyte meiotic maturation were compared in an in vitro mouse oocyte culture model. Exposure to 150 μM of both BPZ and BPA disrupted the assembly of the meiotic spindle and the alignment of chromosomes, and BPZ exerted stronger toxicological effects than BPA. Furthermore, BPZ resulted in aberrant expression of F-actin, preventing the formation of the actin cap. Mechanistically, BPZ exposure disrupted the mitochondrial localization pattern, reduced mitochondrial membrane potential and ATP content, leading to impaired mitochondrial function. Further studies revealed that BPZ exposure resulted in oxidative stress and altered expression of genes associated with anti-oxidative stress. Moreover, BPZ induced severe DNA damage and triggered early apoptosis in oocytes, accompanied by impaired lysosomal function. Overall, the data in this study suggest that BPZ is not a safe alternative to BPA. BPZ can trigger early apoptosis by affecting mitochondrial function and causing oxidative stress and DNA damage in oocytes. These processes disrupt cytoskeletal assembly, arrest the cell cycle, and ultimately inhibit oocyte meiotic maturation. |
| first_indexed | 2024-04-24T10:05:42Z |
| format | Article |
| id | doaj.art-d2145b745700405b9cd6f8537a0ab448 |
| institution | Directory Open Access Journal |
| issn | 0147-6513 |
| language | English |
| last_indexed | 2024-04-24T10:05:42Z |
| publishDate | 2024-05-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Ecotoxicology and Environmental Safety |
| spelling | doaj.art-d2145b745700405b9cd6f8537a0ab4482024-04-13T04:20:54ZengElsevierEcotoxicology and Environmental Safety0147-65132024-05-01276116312Bisphenol Z exposure inhibits oocyte meiotic maturation by rupturing mitochondrial functionCong Ma0Yan Xu1Huilei Chen2Yue Huang3Shanshan Wang4Pin Zhang5Guojing Li6Zuying Xu7Xiaofeng Xu8Zhiming Ding9Huifen Xiang10Yunxia Cao11Reproductive Medicine Center, Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, No.218 Jixi Road, Hefei 230022, China; NHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract, Anhui Medical University, No.81 Meishan Road, Hefei 230032, China; Key Laboratory of Population Health Across Life Cycle, Anhui Medical University, Ministry of Education of the People’s Republic of China, No.81 Meishan Road, Hefei 230032, ChinaReproductive Medicine Center, Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, No.218 Jixi Road, Hefei 230022, China; NHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract, Anhui Medical University, No.81 Meishan Road, Hefei 230032, China; Key Laboratory of Population Health Across Life Cycle, Anhui Medical University, Ministry of Education of the People’s Republic of China, No.81 Meishan Road, Hefei 230032, ChinaReproductive Medicine Center, Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, No.218 Jixi Road, Hefei 230022, China; NHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract, Anhui Medical University, No.81 Meishan Road, Hefei 230032, China; Key Laboratory of Population Health Across Life Cycle, Anhui Medical University, Ministry of Education of the People’s Republic of China, No.81 Meishan Road, Hefei 230032, ChinaReproductive Medicine Center, Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, No.218 Jixi Road, Hefei 230022, ChinaReproductive Medicine Center, Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, No.218 Jixi Road, Hefei 230022, ChinaReproductive Medicine Center, Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, No.218 Jixi Road, Hefei 230022, ChinaReproductive Medicine Center, Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, No.218 Jixi Road, Hefei 230022, ChinaReproductive Medicine Center, Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, No.218 Jixi Road, Hefei 230022, China; NHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract, Anhui Medical University, No.81 Meishan Road, Hefei 230032, China; Key Laboratory of Population Health Across Life Cycle, Anhui Medical University, Ministry of Education of the People’s Republic of China, No.81 Meishan Road, Hefei 230032, ChinaReproductive Medicine Center, Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, No.218 Jixi Road, Hefei 230022, China; NHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract, Anhui Medical University, No.81 Meishan Road, Hefei 230032, China; Key Laboratory of Population Health Across Life Cycle, Anhui Medical University, Ministry of Education of the People’s Republic of China, No.81 Meishan Road, Hefei 230032, ChinaNHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract, Anhui Medical University, No.81 Meishan Road, Hefei 230032, China; Key Laboratory of Population Health Across Life Cycle, Anhui Medical University, Ministry of Education of the People’s Republic of China, No.81 Meishan Road, Hefei 230032, China; Corresponding authors at: NHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract, Anhui Medical University, No.81 Meishan Road, Hefei 230032, China.Reproductive Medicine Center, Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, No.218 Jixi Road, Hefei 230022, China; NHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract, Anhui Medical University, No.81 Meishan Road, Hefei 230032, China; Key Laboratory of Population Health Across Life Cycle, Anhui Medical University, Ministry of Education of the People’s Republic of China, No.81 Meishan Road, Hefei 230032, China; Corresponding authors at: NHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract, Anhui Medical University, No.81 Meishan Road, Hefei 230032, China.Reproductive Medicine Center, Department of Obstetrics and Gynecology, The First Affiliated Hospital of Anhui Medical University, No.218 Jixi Road, Hefei 230022, China; NHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract, Anhui Medical University, No.81 Meishan Road, Hefei 230032, China; Key Laboratory of Population Health Across Life Cycle, Anhui Medical University, Ministry of Education of the People’s Republic of China, No.81 Meishan Road, Hefei 230032, China; Engineering Research Center of Biopreservation and Artificial Organs, Ministry of Education, No.81 Meishan Road, Hefei, Anhui 230032, China; Anhui Province Key Laboratory of Reproductive Health and Genetics, No.81 Meishan Road, Hefei 230032, China; Biopreservation and Artificial Organs, Anhui Provincial Engineering Research Center, Anhui Medical University, No.81 Meishan Road, Hefei 230032, China; Anhui Provincial Institute of Translational Medicine, No.81 Meishan Road, Hefei 230032, China; Corresponding authors at: NHC Key Laboratory of Study on Abnormal Gametes and Reproductive Tract, Anhui Medical University, No.81 Meishan Road, Hefei 230032, China.The use of bisphenol A (BPA) has been restricted due to its endocrine-disrupting effects. As a widely used alternative to BPA today, environmental levels of bisphenol Z (BPZ) continue to rise and accumulate in humans. Oocyte quality is critical for a successful pregnancy. Nevertheless, the toxic impacts of BPZ on the maturation of mammalian oocytes remain unexplored. Therefore, the impacts of BPZ and BPA on oocyte meiotic maturation were compared in an in vitro mouse oocyte culture model. Exposure to 150 μM of both BPZ and BPA disrupted the assembly of the meiotic spindle and the alignment of chromosomes, and BPZ exerted stronger toxicological effects than BPA. Furthermore, BPZ resulted in aberrant expression of F-actin, preventing the formation of the actin cap. Mechanistically, BPZ exposure disrupted the mitochondrial localization pattern, reduced mitochondrial membrane potential and ATP content, leading to impaired mitochondrial function. Further studies revealed that BPZ exposure resulted in oxidative stress and altered expression of genes associated with anti-oxidative stress. Moreover, BPZ induced severe DNA damage and triggered early apoptosis in oocytes, accompanied by impaired lysosomal function. Overall, the data in this study suggest that BPZ is not a safe alternative to BPA. BPZ can trigger early apoptosis by affecting mitochondrial function and causing oxidative stress and DNA damage in oocytes. These processes disrupt cytoskeletal assembly, arrest the cell cycle, and ultimately inhibit oocyte meiotic maturation.http://www.sciencedirect.com/science/article/pii/S0147651324003889BPZBPAOocyteMitochondriaMeiosis |
| spellingShingle | Cong Ma Yan Xu Huilei Chen Yue Huang Shanshan Wang Pin Zhang Guojing Li Zuying Xu Xiaofeng Xu Zhiming Ding Huifen Xiang Yunxia Cao Bisphenol Z exposure inhibits oocyte meiotic maturation by rupturing mitochondrial function Ecotoxicology and Environmental Safety BPZ BPA Oocyte Mitochondria Meiosis |
| title | Bisphenol Z exposure inhibits oocyte meiotic maturation by rupturing mitochondrial function |
| title_full | Bisphenol Z exposure inhibits oocyte meiotic maturation by rupturing mitochondrial function |
| title_fullStr | Bisphenol Z exposure inhibits oocyte meiotic maturation by rupturing mitochondrial function |
| title_full_unstemmed | Bisphenol Z exposure inhibits oocyte meiotic maturation by rupturing mitochondrial function |
| title_short | Bisphenol Z exposure inhibits oocyte meiotic maturation by rupturing mitochondrial function |
| title_sort | bisphenol z exposure inhibits oocyte meiotic maturation by rupturing mitochondrial function |
| topic | BPZ BPA Oocyte Mitochondria Meiosis |
| url | http://www.sciencedirect.com/science/article/pii/S0147651324003889 |
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