Ameliorative Effect of Itaconic Acid/IRG1 Against Endoplasmic Reticulum Stress-Induced Necroptosis in Granulosa Cells via PERK-ATF4-AChE Pathway in Bovine

The necroptosis of granulosa cells has been proven to be one of the important triggers of follicular atresia, which is an important cause of reduced reproductive capacity in cows. The rapid growth of granulosa cells is accompanied by endoplasmic reticulum stress (ERS), leading to granulosa cell deat...

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Main Authors: Xiaorui Yang, Yue Chen, Xinzi Wang, Gaoqing Xu, Hongjie Wang, Xinqi Shu, He Ding, Xin Ma, Jing Guo, Jun Wang, Jing Zhao, Yi Fang, Hongyu Liu, Wenfa Lu
Format: Article
Language:English
Published: MDPI AG 2025-03-01
Series:Cells
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Online Access:https://www.mdpi.com/2073-4409/14/6/419
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author Xiaorui Yang
Yue Chen
Xinzi Wang
Gaoqing Xu
Hongjie Wang
Xinqi Shu
He Ding
Xin Ma
Jing Guo
Jun Wang
Jing Zhao
Yi Fang
Hongyu Liu
Wenfa Lu
author_facet Xiaorui Yang
Yue Chen
Xinzi Wang
Gaoqing Xu
Hongjie Wang
Xinqi Shu
He Ding
Xin Ma
Jing Guo
Jun Wang
Jing Zhao
Yi Fang
Hongyu Liu
Wenfa Lu
author_sort Xiaorui Yang
collection DOAJ
description The necroptosis of granulosa cells has been proven to be one of the important triggers of follicular atresia, which is an important cause of reduced reproductive capacity in cows. The rapid growth of granulosa cells is accompanied by endoplasmic reticulum stress (ERS), leading to granulosa cell death. However, the link between ERS and necroptosis, as well as its mechanism in bovine granulosa cells is still unclear. Itaconic acid is an endogenous anti-inflammatory and antioxidant small-molecule compound that can alleviate ERS. Therefore, the aim of the current study is to evaluate the effect of ERS on necroptosis and investigate the ameliorative effect of itaconic acid against ERS-induced necroptosis in granulosa cells. Bovine granulosa cells were treated with tunicamycin (Tm) to induce ERS. After the addition of the necroptosis inhibitor Nec-1 and the detection of the necroptosis inducer acetylcholinesterase (AChE), flow cytometry, transmission electron microscopy, and mass spectrometry were used to analyze the expression of itaconic acid and IRG1 in the granulosa cells. In addition, the role of the PERK pathway downstream of ERS in ERS-induced necroptosis was also investigated. We report here that ERS can induce necroptosis in granulosa cells. Itaconic acid supplementation significantly attenuates the effect of ERS-induced damage. In summary, this research provides a scientific basis and a drug reference for treating follicular atresia and improving bovine reproductive capacity.
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spelling doaj-art-5d6fe7236d3349d1814bd0cb428fae892025-08-20T03:43:11ZengMDPI AGCells2073-44092025-03-0114641910.3390/cells14060419Ameliorative Effect of Itaconic Acid/IRG1 Against Endoplasmic Reticulum Stress-Induced Necroptosis in Granulosa Cells via PERK-ATF4-AChE Pathway in BovineXiaorui Yang0Yue Chen1Xinzi Wang2Gaoqing Xu3Hongjie Wang4Xinqi Shu5He Ding6Xin Ma7Jing Guo8Jun Wang9Jing Zhao10Yi Fang11Hongyu Liu12Wenfa Lu13Key Laboratory of Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun 130118, ChinaKey Laboratory of Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun 130118, ChinaKey Laboratory of Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun 130118, ChinaKey Laboratory of Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun 130118, ChinaKey Laboratory of Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun 130118, ChinaKey Laboratory of Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun 130118, ChinaKey Laboratory of Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun 130118, ChinaKey Laboratory of Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun 130118, ChinaKey Laboratory of Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun 130118, ChinaKey Laboratory of Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun 130118, ChinaKey Laboratory of Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun 130118, ChinaKey Laboratory of Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun 130118, ChinaKey Laboratory of Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun 130118, ChinaKey Laboratory of Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun 130118, ChinaThe necroptosis of granulosa cells has been proven to be one of the important triggers of follicular atresia, which is an important cause of reduced reproductive capacity in cows. The rapid growth of granulosa cells is accompanied by endoplasmic reticulum stress (ERS), leading to granulosa cell death. However, the link between ERS and necroptosis, as well as its mechanism in bovine granulosa cells is still unclear. Itaconic acid is an endogenous anti-inflammatory and antioxidant small-molecule compound that can alleviate ERS. Therefore, the aim of the current study is to evaluate the effect of ERS on necroptosis and investigate the ameliorative effect of itaconic acid against ERS-induced necroptosis in granulosa cells. Bovine granulosa cells were treated with tunicamycin (Tm) to induce ERS. After the addition of the necroptosis inhibitor Nec-1 and the detection of the necroptosis inducer acetylcholinesterase (AChE), flow cytometry, transmission electron microscopy, and mass spectrometry were used to analyze the expression of itaconic acid and IRG1 in the granulosa cells. In addition, the role of the PERK pathway downstream of ERS in ERS-induced necroptosis was also investigated. We report here that ERS can induce necroptosis in granulosa cells. Itaconic acid supplementation significantly attenuates the effect of ERS-induced damage. In summary, this research provides a scientific basis and a drug reference for treating follicular atresia and improving bovine reproductive capacity.https://www.mdpi.com/2073-4409/14/6/419itaconic acidERSgranulosa cellsnecroptosis
spellingShingle Xiaorui Yang
Yue Chen
Xinzi Wang
Gaoqing Xu
Hongjie Wang
Xinqi Shu
He Ding
Xin Ma
Jing Guo
Jun Wang
Jing Zhao
Yi Fang
Hongyu Liu
Wenfa Lu
Ameliorative Effect of Itaconic Acid/IRG1 Against Endoplasmic Reticulum Stress-Induced Necroptosis in Granulosa Cells via PERK-ATF4-AChE Pathway in Bovine
Cells
itaconic acid
ERS
granulosa cells
necroptosis
title Ameliorative Effect of Itaconic Acid/IRG1 Against Endoplasmic Reticulum Stress-Induced Necroptosis in Granulosa Cells via PERK-ATF4-AChE Pathway in Bovine
title_full Ameliorative Effect of Itaconic Acid/IRG1 Against Endoplasmic Reticulum Stress-Induced Necroptosis in Granulosa Cells via PERK-ATF4-AChE Pathway in Bovine
title_fullStr Ameliorative Effect of Itaconic Acid/IRG1 Against Endoplasmic Reticulum Stress-Induced Necroptosis in Granulosa Cells via PERK-ATF4-AChE Pathway in Bovine
title_full_unstemmed Ameliorative Effect of Itaconic Acid/IRG1 Against Endoplasmic Reticulum Stress-Induced Necroptosis in Granulosa Cells via PERK-ATF4-AChE Pathway in Bovine
title_short Ameliorative Effect of Itaconic Acid/IRG1 Against Endoplasmic Reticulum Stress-Induced Necroptosis in Granulosa Cells via PERK-ATF4-AChE Pathway in Bovine
title_sort ameliorative effect of itaconic acid irg1 against endoplasmic reticulum stress induced necroptosis in granulosa cells via perk atf4 ache pathway in bovine
topic itaconic acid
ERS
granulosa cells
necroptosis
url https://www.mdpi.com/2073-4409/14/6/419
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