Iron Overload-Induced Ferroptosis Impairs Porcine Oocyte Maturation and Subsequent Embryonic Developmental Competence in vitro
Accumulating evidence indicates that ferroptosis is an iron-dependent form of regulated cell death. This type of iron-dependent programmed cell death is different from traditional forms of regulated cell death, such as apoptosis and autophagy. However, the role of ferroptosis in porcine oocyte matur...
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doaj-15499e641d4240ef87bef5ed406774cf2021-05-28T08:55:27ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2021-05-01910.3389/fcell.2021.673291673291Iron Overload-Induced Ferroptosis Impairs Porcine Oocyte Maturation and Subsequent Embryonic Developmental Competence in vitroWeiyi Hu0Yan Zhang1Yan Zhang2Dali Wang3Tingting Yang4Jiajia Qi5Yonghong Zhang6Hao Jiang7Jiabao Zhang8Boxing Sun9Shuang Liang10Department of Animals Sciences, College of Animal Sciences, Jilin University, Changchun, ChinaDepartment of Animals Sciences, College of Animal Sciences, Jilin University, Changchun, ChinaDepartment of Animal Science, Chungbuk National University, Cheongju-si, South KoreaDepartment of Animals Sciences, College of Animal Sciences, Jilin University, Changchun, ChinaDepartment of Animals Sciences, College of Animal Sciences, Jilin University, Changchun, ChinaDepartment of Animals Sciences, College of Animal Sciences, Jilin University, Changchun, ChinaDepartment of Animals Sciences, College of Animal Sciences, Jilin University, Changchun, ChinaDepartment of Animals Sciences, College of Animal Sciences, Jilin University, Changchun, ChinaDepartment of Animals Sciences, College of Animal Sciences, Jilin University, Changchun, ChinaDepartment of Animals Sciences, College of Animal Sciences, Jilin University, Changchun, ChinaDepartment of Animals Sciences, College of Animal Sciences, Jilin University, Changchun, ChinaAccumulating evidence indicates that ferroptosis is an iron-dependent form of regulated cell death. This type of iron-dependent programmed cell death is different from traditional forms of regulated cell death, such as apoptosis and autophagy. However, the role of ferroptosis in porcine oocyte maturation and the associated mechanism remain unclear. In the present research, we investigated the effects of ferric ammonium citrate (FAC), a specific ferroptosis inducer, on porcine oocyte meiotic maturation and quality and subsequent embryonic developmental competence. FAC treatment caused obvious accumulation of intracellular ferrous ions in porcine oocytes. At the end of the in vitro maturation (IVM) period, there was a significant decrease in the polar body (PB) extrusion rate and an increase in the percentage of abnormal oocytes in the FAC treatment groups, indicating that iron overload-induced ferroptosis may suppress the meiotic process during porcine oocyte maturation. We also found that after FAC treatment, the subsequent two-cell rate, four-cell rate and blastocyst formation rate were significantly decreased in porcine parthenogenetic activation (PA) embryos, indicating that iron overload-induced ferroptosis decreased porcine oocyte quality. Further analysis revealed that FAC treatment not only enhanced intracellular reactive oxygen species (ROS) generation, decreased intracellular free thiol levels and induced mitochondrial dysfunction but also triggered autophagy in porcine oocytes. Taken together, these findings suggest that iron overload-induced ferroptosis impairs porcine oocyte meiosis and decreases porcine oocyte quality, possibly by increasing oxidative stress, inducing mitochondrial dysfunction and triggering autophagy.https://www.frontiersin.org/articles/10.3389/fcell.2021.673291/fulliron overloadferroptosisporcine oocyteoxidative stressmitochondrial function |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Weiyi Hu Yan Zhang Yan Zhang Dali Wang Tingting Yang Jiajia Qi Yonghong Zhang Hao Jiang Jiabao Zhang Boxing Sun Shuang Liang |
spellingShingle |
Weiyi Hu Yan Zhang Yan Zhang Dali Wang Tingting Yang Jiajia Qi Yonghong Zhang Hao Jiang Jiabao Zhang Boxing Sun Shuang Liang Iron Overload-Induced Ferroptosis Impairs Porcine Oocyte Maturation and Subsequent Embryonic Developmental Competence in vitro Frontiers in Cell and Developmental Biology iron overload ferroptosis porcine oocyte oxidative stress mitochondrial function |
author_facet |
Weiyi Hu Yan Zhang Yan Zhang Dali Wang Tingting Yang Jiajia Qi Yonghong Zhang Hao Jiang Jiabao Zhang Boxing Sun Shuang Liang |
author_sort |
Weiyi Hu |
title |
Iron Overload-Induced Ferroptosis Impairs Porcine Oocyte Maturation and Subsequent Embryonic Developmental Competence in vitro |
title_short |
Iron Overload-Induced Ferroptosis Impairs Porcine Oocyte Maturation and Subsequent Embryonic Developmental Competence in vitro |
title_full |
Iron Overload-Induced Ferroptosis Impairs Porcine Oocyte Maturation and Subsequent Embryonic Developmental Competence in vitro |
title_fullStr |
Iron Overload-Induced Ferroptosis Impairs Porcine Oocyte Maturation and Subsequent Embryonic Developmental Competence in vitro |
title_full_unstemmed |
Iron Overload-Induced Ferroptosis Impairs Porcine Oocyte Maturation and Subsequent Embryonic Developmental Competence in vitro |
title_sort |
iron overload-induced ferroptosis impairs porcine oocyte maturation and subsequent embryonic developmental competence in vitro |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Cell and Developmental Biology |
issn |
2296-634X |
publishDate |
2021-05-01 |
description |
Accumulating evidence indicates that ferroptosis is an iron-dependent form of regulated cell death. This type of iron-dependent programmed cell death is different from traditional forms of regulated cell death, such as apoptosis and autophagy. However, the role of ferroptosis in porcine oocyte maturation and the associated mechanism remain unclear. In the present research, we investigated the effects of ferric ammonium citrate (FAC), a specific ferroptosis inducer, on porcine oocyte meiotic maturation and quality and subsequent embryonic developmental competence. FAC treatment caused obvious accumulation of intracellular ferrous ions in porcine oocytes. At the end of the in vitro maturation (IVM) period, there was a significant decrease in the polar body (PB) extrusion rate and an increase in the percentage of abnormal oocytes in the FAC treatment groups, indicating that iron overload-induced ferroptosis may suppress the meiotic process during porcine oocyte maturation. We also found that after FAC treatment, the subsequent two-cell rate, four-cell rate and blastocyst formation rate were significantly decreased in porcine parthenogenetic activation (PA) embryos, indicating that iron overload-induced ferroptosis decreased porcine oocyte quality. Further analysis revealed that FAC treatment not only enhanced intracellular reactive oxygen species (ROS) generation, decreased intracellular free thiol levels and induced mitochondrial dysfunction but also triggered autophagy in porcine oocytes. Taken together, these findings suggest that iron overload-induced ferroptosis impairs porcine oocyte meiosis and decreases porcine oocyte quality, possibly by increasing oxidative stress, inducing mitochondrial dysfunction and triggering autophagy. |
topic |
iron overload ferroptosis porcine oocyte oxidative stress mitochondrial function |
url |
https://www.frontiersin.org/articles/10.3389/fcell.2021.673291/full |
work_keys_str_mv |
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