Suppression of PINK1 autophosphorylation attenuates pilocarpine-induced seizures and neuronal injury in rats

PTEN-induced kinase 1 (PINK1) autophosphorylation triggers the PINK1/Parkin pathway, which is the main mitophagic pathway in the mammalian nervous system. In the present study, we aimed to mechanistically explore the role of PINK1 in pilocarpine-induced status epilepticus (SE) in Sprague-Dawley rats...

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Main Authors: Yujie Zhai, Yi Yuan, Yaru Cui, Xiaoqian Wang, Hua Zhou, Qian Teng, Hongjin Wang, Bohan Sun, Hongliu Sun, Jianhua Tang
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:Brain Research Bulletin
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Online Access:http://www.sciencedirect.com/science/article/pii/S036192302400251X
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author Yujie Zhai
Yi Yuan
Yaru Cui
Xiaoqian Wang
Hua Zhou
Qian Teng
Hongjin Wang
Bohan Sun
Hongliu Sun
Jianhua Tang
author_facet Yujie Zhai
Yi Yuan
Yaru Cui
Xiaoqian Wang
Hua Zhou
Qian Teng
Hongjin Wang
Bohan Sun
Hongliu Sun
Jianhua Tang
author_sort Yujie Zhai
collection DOAJ
description PTEN-induced kinase 1 (PINK1) autophosphorylation triggers the PINK1/Parkin pathway, which is the main mitophagic pathway in the mammalian nervous system. In the present study, we aimed to mechanistically explore the role of PINK1 in pilocarpine-induced status epilepticus (SE) in Sprague-Dawley rats. Evidence from immunohistochemistry, western blotting, biochemical assays, and behavioral testing showed that pilocarpine-induced SE led to increased levels of PINK1 phosphorylation, mitophagy, mitochondrial oxidative stress, neuronal damage and learning and memory deficits. Using shRNA interference to suppress the expression of translocase outer mitochondrial membrane 7, a positive regulator of PINK1 autophosphorylation, lowered the increased levels of phosphorylated PINK1 following pilocarpine administration. It also reduced the levels of mitophagy, mitochondrial oxidative stress and neuronal damage, and attenuated seizure severity and cognitive deficits. In contrast, suppressing the expression of overlapping with the m-AAA protease 1 homolog, a negative regulator of PINK1 autophosphorylation, led to higher levels of phosphorylated PINK1 following pilocarpine administration. It also led to more serious mitophagy, neuronal damage, as well as worsened seizure severity and cognitive deficits. Our results indicate that PINK1 autophosphorylation plays a vital role in epileptic seizures and neuronal injury by mediating mitophagy. Regulating PINK1 autophosphorylation may change the adverse consequences of epilepsy, and may be an effective neuroprotective strategy.
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spelling doaj-art-d2d929bfaa3a45898c07a19c289314792025-08-20T01:54:18ZengElsevierBrain Research Bulletin1873-27472024-12-0121911111710.1016/j.brainresbull.2024.111117Suppression of PINK1 autophosphorylation attenuates pilocarpine-induced seizures and neuronal injury in ratsYujie Zhai0Yi Yuan1Yaru Cui2Xiaoqian Wang3Hua Zhou4Qian Teng5Hongjin Wang6Bohan Sun7Hongliu Sun8Jianhua Tang9School of Pharmaceutical Sciences, Binzhou Medical University, Yantai 264003, ChinaSchool of Pharmaceutical Sciences, Binzhou Medical University, Yantai 264003, ChinaSchool of Pharmaceutical Sciences, Binzhou Medical University, Yantai 264003, ChinaSchool of Pharmaceutical Sciences, Binzhou Medical University, Yantai 264003, ChinaSchool of Pharmaceutical Sciences, Binzhou Medical University, Yantai 264003, ChinaSchool of Pharmaceutical Sciences, Binzhou Medical University, Yantai 264003, ChinaSchool of Pharmaceutical Sciences, Binzhou Medical University, Yantai 264003, ChinaSchool of Pharmaceutical Sciences, Binzhou Medical University, Yantai 264003, ChinaSchool of Pharmaceutical Sciences, Binzhou Medical University, Yantai 264003, China; Corresponding authors.Affiliated Yantai Mountain Hospital, Binzhou Medical University, Yantai 264003, China; Corresponding authors.PTEN-induced kinase 1 (PINK1) autophosphorylation triggers the PINK1/Parkin pathway, which is the main mitophagic pathway in the mammalian nervous system. In the present study, we aimed to mechanistically explore the role of PINK1 in pilocarpine-induced status epilepticus (SE) in Sprague-Dawley rats. Evidence from immunohistochemistry, western blotting, biochemical assays, and behavioral testing showed that pilocarpine-induced SE led to increased levels of PINK1 phosphorylation, mitophagy, mitochondrial oxidative stress, neuronal damage and learning and memory deficits. Using shRNA interference to suppress the expression of translocase outer mitochondrial membrane 7, a positive regulator of PINK1 autophosphorylation, lowered the increased levels of phosphorylated PINK1 following pilocarpine administration. It also reduced the levels of mitophagy, mitochondrial oxidative stress and neuronal damage, and attenuated seizure severity and cognitive deficits. In contrast, suppressing the expression of overlapping with the m-AAA protease 1 homolog, a negative regulator of PINK1 autophosphorylation, led to higher levels of phosphorylated PINK1 following pilocarpine administration. It also led to more serious mitophagy, neuronal damage, as well as worsened seizure severity and cognitive deficits. Our results indicate that PINK1 autophosphorylation plays a vital role in epileptic seizures and neuronal injury by mediating mitophagy. Regulating PINK1 autophosphorylation may change the adverse consequences of epilepsy, and may be an effective neuroprotective strategy.http://www.sciencedirect.com/science/article/pii/S036192302400251XPTEN-induced kinase 1Status epilepticusMitophagyMitochondrial oxidative stressNeuronal injury
spellingShingle Yujie Zhai
Yi Yuan
Yaru Cui
Xiaoqian Wang
Hua Zhou
Qian Teng
Hongjin Wang
Bohan Sun
Hongliu Sun
Jianhua Tang
Suppression of PINK1 autophosphorylation attenuates pilocarpine-induced seizures and neuronal injury in rats
Brain Research Bulletin
PTEN-induced kinase 1
Status epilepticus
Mitophagy
Mitochondrial oxidative stress
Neuronal injury
title Suppression of PINK1 autophosphorylation attenuates pilocarpine-induced seizures and neuronal injury in rats
title_full Suppression of PINK1 autophosphorylation attenuates pilocarpine-induced seizures and neuronal injury in rats
title_fullStr Suppression of PINK1 autophosphorylation attenuates pilocarpine-induced seizures and neuronal injury in rats
title_full_unstemmed Suppression of PINK1 autophosphorylation attenuates pilocarpine-induced seizures and neuronal injury in rats
title_short Suppression of PINK1 autophosphorylation attenuates pilocarpine-induced seizures and neuronal injury in rats
title_sort suppression of pink1 autophosphorylation attenuates pilocarpine induced seizures and neuronal injury in rats
topic PTEN-induced kinase 1
Status epilepticus
Mitophagy
Mitochondrial oxidative stress
Neuronal injury
url http://www.sciencedirect.com/science/article/pii/S036192302400251X
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