Nickel exposure induced endoplasmic reticulum stress by disturbing calcium homeostasis and triggered mitochondrial autophagy in domestic animal oocytes

Nickel, a heavy metal with industrial applications and as a feed additive for livestock, can adversely impact reproductive function and gamete quality when present in excessive amounts in the animal feed environment. In this study, the results indicate that nickel exposure hampers polar body extrusi...

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Main Authors: Chengkun Zhong, Shengkui Hou, Jing Guo, Jing Zhao, Jun Wang, Yi Fang, Hongyu Liu, He Ding, Xin Ma, Wenfa Lyu
Format: Article
Language:English
Published: Elsevier 2025-09-01
Series:Ecotoxicology and Environmental Safety
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Online Access:http://www.sciencedirect.com/science/article/pii/S0147651325010139
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author Chengkun Zhong
Shengkui Hou
Jing Guo
Jing Zhao
Jun Wang
Yi Fang
Hongyu Liu
He Ding
Xin Ma
Wenfa Lyu
author_facet Chengkun Zhong
Shengkui Hou
Jing Guo
Jing Zhao
Jun Wang
Yi Fang
Hongyu Liu
He Ding
Xin Ma
Wenfa Lyu
author_sort Chengkun Zhong
collection DOAJ
description Nickel, a heavy metal with industrial applications and as a feed additive for livestock, can adversely impact reproductive function and gamete quality when present in excessive amounts in the animal feed environment. In this study, the results indicate that nickel exposure hampers polar body extrusion and cumulus cell expansion, thereby diminishing oocyte quality and developmental competence. Furthermore, nickel exposure reduces glutathione (GSH) levels in oocytes, leading to excessive accumulation of reactive oxygen species (ROS), provoking oxidative stress and mitochondrial impairment. This cascade initiates mitochondrial autophagy, upregulates the expression of autophagy-related proteins Parkin and PINK1, promotes LC3 binding to autophagosomes. Nickel exposure disrupts calcium homeostasis and induces endoplasmic reticulum stress (ERS). Inhibiting ERS effectively alleviates the deterioration of oocytes quality caused by nickel exposure and inhibits mitochondrial autophagy. Proteomics further confirms nickel’s exposure detrimental effects on mitochondria and ER, impacting cellular processes. Employing bovine oocytes as a model, consistent phenotypes were observed. These results indicate that nickel exposure disrupts intracellular calcium homeostasis, elicits ERS, disrupts cellular calcium homeostasis, diminishes the quality of pig oocytes, impairs oocyte maturation and developmental potential, and instigates mitochondrial autophagy.
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spelling doaj-art-a2daf32d63a84d4b9536469238945ecb2025-08-20T03:41:19ZengElsevierEcotoxicology and Environmental Safety0147-65132025-09-0130211866810.1016/j.ecoenv.2025.118668Nickel exposure induced endoplasmic reticulum stress by disturbing calcium homeostasis and triggered mitochondrial autophagy in domestic animal oocytesChengkun Zhong0Shengkui Hou1Jing Guo2Jing Zhao3Jun Wang4Yi Fang5Hongyu Liu6He Ding7Xin Ma8Wenfa Lyu9Key Laboratory of the Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun, Jilin, China; Jilin Provincial International Joint Research Center of Animal Breeding and Reproduction Technology, Jilin Agricultural University, Changchun, Jilin, China; Jilin Province Key Laboratory of Beef Cattle Germplasm Resources Utilization, Jilin Agricultural University, Changchun, Jilin, ChinaKey Laboratory of the Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun, Jilin, China; Jilin Provincial International Joint Research Center of Animal Breeding and Reproduction Technology, Jilin Agricultural University, Changchun, Jilin, China; Jilin Province Key Laboratory of Beef Cattle Germplasm Resources Utilization, Jilin Agricultural University, Changchun, Jilin, ChinaKey Laboratory of the Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun, Jilin, China; Jilin Provincial International Joint Research Center of Animal Breeding and Reproduction Technology, Jilin Agricultural University, Changchun, Jilin, China; Jilin Province Key Laboratory of Beef Cattle Germplasm Resources Utilization, Jilin Agricultural University, Changchun, Jilin, ChinaKey Laboratory of the Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun, Jilin, China; Jilin Provincial International Joint Research Center of Animal Breeding and Reproduction Technology, Jilin Agricultural University, Changchun, Jilin, China; Jilin Province Key Laboratory of Beef Cattle Germplasm Resources Utilization, Jilin Agricultural University, Changchun, Jilin, ChinaKey Laboratory of the Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun, Jilin, China; Jilin Province Key Laboratory of Beef Cattle Germplasm Resources Utilization, Jilin Agricultural University, Changchun, Jilin, ChinaKey Laboratory of the Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun, Jilin, China; Jilin Province Key Laboratory of Beef Cattle Germplasm Resources Utilization, Jilin Agricultural University, Changchun, Jilin, ChinaKey Laboratory of the Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun, Jilin, China; Jilin Provincial International Joint Research Center of Animal Breeding and Reproduction Technology, Jilin Agricultural University, Changchun, Jilin, ChinaKey Laboratory of the Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun, Jilin, China; Jilin Provincial International Joint Research Center of Animal Breeding and Reproduction Technology, Jilin Agricultural University, Changchun, Jilin, ChinaKey Laboratory of the Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun, Jilin, China; Jilin Provincial International Joint Research Center of Animal Breeding and Reproduction Technology, Jilin Agricultural University, Changchun, Jilin, China; Jilin Province Key Laboratory of Beef Cattle Germplasm Resources Utilization, Jilin Agricultural University, Changchun, Jilin, China; Corresponding authors at: Key Laboratory of the Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun, Jilin, ChinaKey Laboratory of the Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun, Jilin, China; Jilin Provincial International Joint Research Center of Animal Breeding and Reproduction Technology, Jilin Agricultural University, Changchun, Jilin, China; Jilin Province Key Laboratory of Beef Cattle Germplasm Resources Utilization, Jilin Agricultural University, Changchun, Jilin, China; Corresponding authors at: Key Laboratory of the Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun, Jilin, ChinaNickel, a heavy metal with industrial applications and as a feed additive for livestock, can adversely impact reproductive function and gamete quality when present in excessive amounts in the animal feed environment. In this study, the results indicate that nickel exposure hampers polar body extrusion and cumulus cell expansion, thereby diminishing oocyte quality and developmental competence. Furthermore, nickel exposure reduces glutathione (GSH) levels in oocytes, leading to excessive accumulation of reactive oxygen species (ROS), provoking oxidative stress and mitochondrial impairment. This cascade initiates mitochondrial autophagy, upregulates the expression of autophagy-related proteins Parkin and PINK1, promotes LC3 binding to autophagosomes. Nickel exposure disrupts calcium homeostasis and induces endoplasmic reticulum stress (ERS). Inhibiting ERS effectively alleviates the deterioration of oocytes quality caused by nickel exposure and inhibits mitochondrial autophagy. Proteomics further confirms nickel’s exposure detrimental effects on mitochondria and ER, impacting cellular processes. Employing bovine oocytes as a model, consistent phenotypes were observed. These results indicate that nickel exposure disrupts intracellular calcium homeostasis, elicits ERS, disrupts cellular calcium homeostasis, diminishes the quality of pig oocytes, impairs oocyte maturation and developmental potential, and instigates mitochondrial autophagy.http://www.sciencedirect.com/science/article/pii/S0147651325010139NickelOocyteEndoplasmic reticulumMitochondriaAutophagyCalcium homeostasis
spellingShingle Chengkun Zhong
Shengkui Hou
Jing Guo
Jing Zhao
Jun Wang
Yi Fang
Hongyu Liu
He Ding
Xin Ma
Wenfa Lyu
Nickel exposure induced endoplasmic reticulum stress by disturbing calcium homeostasis and triggered mitochondrial autophagy in domestic animal oocytes
Ecotoxicology and Environmental Safety
Nickel
Oocyte
Endoplasmic reticulum
Mitochondria
Autophagy
Calcium homeostasis
title Nickel exposure induced endoplasmic reticulum stress by disturbing calcium homeostasis and triggered mitochondrial autophagy in domestic animal oocytes
title_full Nickel exposure induced endoplasmic reticulum stress by disturbing calcium homeostasis and triggered mitochondrial autophagy in domestic animal oocytes
title_fullStr Nickel exposure induced endoplasmic reticulum stress by disturbing calcium homeostasis and triggered mitochondrial autophagy in domestic animal oocytes
title_full_unstemmed Nickel exposure induced endoplasmic reticulum stress by disturbing calcium homeostasis and triggered mitochondrial autophagy in domestic animal oocytes
title_short Nickel exposure induced endoplasmic reticulum stress by disturbing calcium homeostasis and triggered mitochondrial autophagy in domestic animal oocytes
title_sort nickel exposure induced endoplasmic reticulum stress by disturbing calcium homeostasis and triggered mitochondrial autophagy in domestic animal oocytes
topic Nickel
Oocyte
Endoplasmic reticulum
Mitochondria
Autophagy
Calcium homeostasis
url http://www.sciencedirect.com/science/article/pii/S0147651325010139
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