Aristolochic acid I exposure decreases oocyte quality
Oocyte quality is a determinant of a successful pregnancy. The final step of oocyte development is oocyte maturation, which is susceptible to environmental exposures. Aristolochic acids (AAs), widely existing in Aristolochia and Asarum plants that have been used in traditional medicine, can result i...
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Frontiers Media S.A.
2022-08-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2022.838992/full |
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| author | Weidong Li Weidong Li Jiaming Zhang Xiaoxia Yu Fei Meng Ju Huang Liangran Zhang Liangran Zhang Shunxin Wang Shunxin Wang Shunxin Wang Shunxin Wang |
| author_facet | Weidong Li Weidong Li Jiaming Zhang Xiaoxia Yu Fei Meng Ju Huang Liangran Zhang Liangran Zhang Shunxin Wang Shunxin Wang Shunxin Wang Shunxin Wang |
| author_sort | Weidong Li |
| collection | DOAJ |
| description | Oocyte quality is a determinant of a successful pregnancy. The final step of oocyte development is oocyte maturation, which is susceptible to environmental exposures. Aristolochic acids (AAs), widely existing in Aristolochia and Asarum plants that have been used in traditional medicine, can result in a smaller ovary and fewer superovulated oocytes after in vivo exposure to mice. However, whether AAs affect oocyte maturation and the underlying mechanism(s) are unclear. In this study, we focused on the effect of Aristolochic acid I (AAI), a major compound of AAs, on the maturation of in vitro cultured mouse oocytes. We showed that AAI exposure significantly decreased oocyte quality, including elevated aneuploidy, accompanied by aberrant chiasma patterns and spindle organization, and decreased first polar body extrusion and fertilization capability. Moreover, embryo development potential was also dramatically decreased. Further analyses revealed that AAI exposure significantly decreased mitochondrial membrane potential and ATP synthesis and increased the level of reactive oxygen species (ROS), implying impaired mitochondrial function. Insufficient ATP supply can cause aberrant spindle assembly and excessive ROS can cause premature loss of sister chromatid cohesion and thus alterations in chiasma patterns. Both aberrant spindles and changed chiasma patterns can contribute to chromosome misalignment and thus aneuploidy. Therefore, AAI exposure decreases oocyte quality probably via impairing mitochondrial function. |
| first_indexed | 2024-12-10T16:01:10Z |
| format | Article |
| id | doaj.art-e4a4cdbbb59f4219937008d8e690671e |
| institution | Directory Open Access Journal |
| issn | 2296-634X |
| language | English |
| last_indexed | 2024-12-10T16:01:10Z |
| publishDate | 2022-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj.art-e4a4cdbbb59f4219937008d8e690671e2022-12-22T01:42:26ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2022-08-011010.3389/fcell.2022.838992838992Aristolochic acid I exposure decreases oocyte qualityWeidong Li0Weidong Li1Jiaming Zhang2Xiaoxia Yu3Fei Meng4Ju Huang5Liangran Zhang6Liangran Zhang7Shunxin Wang8Shunxin Wang9Shunxin Wang10Shunxin Wang11Center for Reproductive Medicine, Cheeloo College of Medicine, Shandong University, Jinan, ChinaAdvanced Medical Research Institute, Shandong University, Jinan, Shandong, ChinaCenter for Reproductive Medicine, Cheeloo College of Medicine, Shandong University, Jinan, ChinaCenter for Reproductive Medicine, Cheeloo College of Medicine, Shandong University, Jinan, ChinaCenter for Reproductive Medicine, Cheeloo College of Medicine, Shandong University, Jinan, ChinaCenter for Reproductive Medicine, Cheeloo College of Medicine, Shandong University, Jinan, ChinaAdvanced Medical Research Institute, Shandong University, Jinan, Shandong, ChinaShandong Provincial Key Laboratory of Animal Resistance Biology, College of Life Sciences, Shandong Normal University, Jinan, Shandong, ChinaCenter for Reproductive Medicine, Cheeloo College of Medicine, Shandong University, Jinan, ChinaNational Research Center for Assisted Reproductive Technology and Reproductive Genetics, Shandong University, Jinan, Shandong, ChinaKey Laboratory of Reproductive Endocrinology of Ministry of Education, Jinan, Shandong, ChinaShandong Provincial Clinical Research Center for Reproductive Health, Jinan, Shandong, ChinaOocyte quality is a determinant of a successful pregnancy. The final step of oocyte development is oocyte maturation, which is susceptible to environmental exposures. Aristolochic acids (AAs), widely existing in Aristolochia and Asarum plants that have been used in traditional medicine, can result in a smaller ovary and fewer superovulated oocytes after in vivo exposure to mice. However, whether AAs affect oocyte maturation and the underlying mechanism(s) are unclear. In this study, we focused on the effect of Aristolochic acid I (AAI), a major compound of AAs, on the maturation of in vitro cultured mouse oocytes. We showed that AAI exposure significantly decreased oocyte quality, including elevated aneuploidy, accompanied by aberrant chiasma patterns and spindle organization, and decreased first polar body extrusion and fertilization capability. Moreover, embryo development potential was also dramatically decreased. Further analyses revealed that AAI exposure significantly decreased mitochondrial membrane potential and ATP synthesis and increased the level of reactive oxygen species (ROS), implying impaired mitochondrial function. Insufficient ATP supply can cause aberrant spindle assembly and excessive ROS can cause premature loss of sister chromatid cohesion and thus alterations in chiasma patterns. Both aberrant spindles and changed chiasma patterns can contribute to chromosome misalignment and thus aneuploidy. Therefore, AAI exposure decreases oocyte quality probably via impairing mitochondrial function.https://www.frontiersin.org/articles/10.3389/fcell.2022.838992/fullaneuploidyoocytespindle assemblymitochondrial dysfunctionaristolochic acids |
| spellingShingle | Weidong Li Weidong Li Jiaming Zhang Xiaoxia Yu Fei Meng Ju Huang Liangran Zhang Liangran Zhang Shunxin Wang Shunxin Wang Shunxin Wang Shunxin Wang Aristolochic acid I exposure decreases oocyte quality Frontiers in Cell and Developmental Biology aneuploidy oocyte spindle assembly mitochondrial dysfunction aristolochic acids |
| title | Aristolochic acid I exposure decreases oocyte quality |
| title_full | Aristolochic acid I exposure decreases oocyte quality |
| title_fullStr | Aristolochic acid I exposure decreases oocyte quality |
| title_full_unstemmed | Aristolochic acid I exposure decreases oocyte quality |
| title_short | Aristolochic acid I exposure decreases oocyte quality |
| title_sort | aristolochic acid i exposure decreases oocyte quality |
| topic | aneuploidy oocyte spindle assembly mitochondrial dysfunction aristolochic acids |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2022.838992/full |
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