Sevoflurane reduces brain edema and improves blood-brain barrier by downregulating CaMKII to inhibit TMEM16A after cerebral ischemia injury both in vivo and in vitro

This study aimed to investigate whether sevoflurane could reduce brain edema and protect blood-brain barrier (BBB) after cerebral-ischemia injury in vivo and in vitro via calmodulin-dependent protein kinase II (CaMKII)/ transmembrane protein 16A (TMEM16A) pathway. Adult male Sprague-Dawley rats and...

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Main Authors: Jingbin Zhang, Yuhe Tian, Ruixue Wang, Xinlei Qin, Quntao Li, Ketao Ma, Junqiang Si, Dong Zhao, Yan Li, Jiangwen Yin
Format: Article
Language:English
Published: Elsevier 2025-09-01
Series:Brain Research Bulletin
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Online Access:http://www.sciencedirect.com/science/article/pii/S0361923025002916
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author Jingbin Zhang
Yuhe Tian
Ruixue Wang
Xinlei Qin
Quntao Li
Ketao Ma
Junqiang Si
Dong Zhao
Yan Li
Jiangwen Yin
author_facet Jingbin Zhang
Yuhe Tian
Ruixue Wang
Xinlei Qin
Quntao Li
Ketao Ma
Junqiang Si
Dong Zhao
Yan Li
Jiangwen Yin
author_sort Jingbin Zhang
collection DOAJ
description This study aimed to investigate whether sevoflurane could reduce brain edema and protect blood-brain barrier (BBB) after cerebral-ischemia injury in vivo and in vitro via calmodulin-dependent protein kinase II (CaMKII)/ transmembrane protein 16A (TMEM16A) pathway. Adult male Sprague-Dawley rats and the brain slices were respectively subjected to middle cerebral artery occlusion (MCAO) in vivo and oxygen-glucose deprivation (OGD) in vitro. Sevoflurane was intervened through a combination of pre-treatment and post-treatment in entire process. TMEM16A overexpression and knockdown was performed by adeno-associated virus. And using agonist and inhibitor affected CaMKII. Neurologic function, ultrastructure, brain water content and the integrity of blood-brain barrier were assessed. Protein levels were investigated by immunofluorescence and western blot. TMEM16A and AQP4 levels, brain water content, leakage of BBB increased in MCAO group. Claudin5 and ZO-1 levels decreased and neurological damage was aggravated after MCAO injury. Sevoflurane reduced brain edema, improved neurological function and protected BBB after MCAO by increasing Claudin5 and ZO-1 levels and decreasing TMEM16A and AQP4 levels. The effect of sevoflurane was weakened by overexpression of TMEM16A and enhanced by knockout of its expression. And when using the inhibitor KN-93, CaMKII level increased while TMEM16A level decreased, enhancing the neuroprotective effect of sevoflurane. Conversely, the effect of sevoflurane was weakened after using the agonist CALP1. Similarly, these manifestations were also observed after OGD injury. In brief, our findings suggest sevoflurane could reduce brain edema, and protect the BBB after cerebral ischemia-reperfusion injury which are related to the downregulation of CaMKII to inhibit TMEM16A.
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spelling doaj-art-b4f9541663f949daadc57a08157df3872025-08-20T03:22:48ZengElsevierBrain Research Bulletin1873-27472025-09-0122911147910.1016/j.brainresbull.2025.111479Sevoflurane reduces brain edema and improves blood-brain barrier by downregulating CaMKII to inhibit TMEM16A after cerebral ischemia injury both in vivo and in vitroJingbin Zhang0Yuhe Tian1Ruixue Wang2Xinlei Qin3Quntao Li4Ketao Ma5Junqiang Si6Dong Zhao7Yan Li8Jiangwen Yin9Department of Anesthesiology, The First Affiliated Hospital of Shihezi University, Shihezi 832003, China; National Health Commission (NHC) Key Laboratory of Prevention and Treatment of Central Asia High Incidence Diseases (Co-construction), The First Affiliated Hospital of Shihezi University, Shihezi 832003, ChinaDepartment of Anesthesiology, The First Affiliated Hospital of Shihezi University, Shihezi 832003, China; Department of Physiology, Shihezi University School of Medicine, Shihezi 832003, China; National Health Commission (NHC) Key Laboratory of Prevention and Treatment of Central Asia High Incidence Diseases (Co-construction), The First Affiliated Hospital of Shihezi University, Shihezi 832003, China; Key Laboratory of Xinjiang Endemic and Ethnic Diseases, Ministry of Education, Shihezi University School of Medicine, Shihezi 832003, ChinaDepartment of Anesthesiology, The First Affiliated Hospital of Shihezi University, Shihezi 832003, China; National Health Commission (NHC) Key Laboratory of Prevention and Treatment of Central Asia High Incidence Diseases (Co-construction), The First Affiliated Hospital of Shihezi University, Shihezi 832003, ChinaDepartment of Anesthesiology, The First Affiliated Hospital of Shihezi University, Shihezi 832003, China; National Health Commission (NHC) Key Laboratory of Prevention and Treatment of Central Asia High Incidence Diseases (Co-construction), The First Affiliated Hospital of Shihezi University, Shihezi 832003, ChinaDepartment of Anesthesiology, The First Affiliated Hospital of Shihezi University, Shihezi 832003, China; National Health Commission (NHC) Key Laboratory of Prevention and Treatment of Central Asia High Incidence Diseases (Co-construction), The First Affiliated Hospital of Shihezi University, Shihezi 832003, ChinaDepartment of Physiology, Shihezi University School of Medicine, Shihezi 832003, China; Key Laboratory of Xinjiang Endemic and Ethnic Diseases, Ministry of Education, Shihezi University School of Medicine, Shihezi 832003, ChinaDepartment of Anesthesiology, The First Affiliated Hospital of Shihezi University, Shihezi 832003, China; Department of Physiology, Shihezi University School of Medicine, Shihezi 832003, China; National Health Commission (NHC) Key Laboratory of Prevention and Treatment of Central Asia High Incidence Diseases (Co-construction), The First Affiliated Hospital of Shihezi University, Shihezi 832003, China; Key Laboratory of Xinjiang Endemic and Ethnic Diseases, Ministry of Education, Shihezi University School of Medicine, Shihezi 832003, ChinaDepartment of Neurosurgery, The First Affiliated Hospital of Shihezi University, Shihezi 832003, China; National Health Commission (NHC) Key Laboratory of Prevention and Treatment of Central Asia High Incidence Diseases (Co-construction), The First Affiliated Hospital of Shihezi University, Shihezi 832003, China; Corresponding author at: Department of Neurosurgery, The First Affiliated Hospital of Shihezi University, Shihezi 832003, China.Department of Anesthesiology, The First Affiliated Hospital of Shihezi University, Shihezi 832003, China; National Health Commission (NHC) Key Laboratory of Prevention and Treatment of Central Asia High Incidence Diseases (Co-construction), The First Affiliated Hospital of Shihezi University, Shihezi 832003, China; Corresponding authors at: Department of Anesthesiology, The First Affiliated Hospital of Shihezi University, Shihezi 832003, China.Department of Anesthesiology, The First Affiliated Hospital of Shihezi University, Shihezi 832003, China; National Health Commission (NHC) Key Laboratory of Prevention and Treatment of Central Asia High Incidence Diseases (Co-construction), The First Affiliated Hospital of Shihezi University, Shihezi 832003, China; Corresponding authors at: Department of Anesthesiology, The First Affiliated Hospital of Shihezi University, Shihezi 832003, China.This study aimed to investigate whether sevoflurane could reduce brain edema and protect blood-brain barrier (BBB) after cerebral-ischemia injury in vivo and in vitro via calmodulin-dependent protein kinase II (CaMKII)/ transmembrane protein 16A (TMEM16A) pathway. Adult male Sprague-Dawley rats and the brain slices were respectively subjected to middle cerebral artery occlusion (MCAO) in vivo and oxygen-glucose deprivation (OGD) in vitro. Sevoflurane was intervened through a combination of pre-treatment and post-treatment in entire process. TMEM16A overexpression and knockdown was performed by adeno-associated virus. And using agonist and inhibitor affected CaMKII. Neurologic function, ultrastructure, brain water content and the integrity of blood-brain barrier were assessed. Protein levels were investigated by immunofluorescence and western blot. TMEM16A and AQP4 levels, brain water content, leakage of BBB increased in MCAO group. Claudin5 and ZO-1 levels decreased and neurological damage was aggravated after MCAO injury. Sevoflurane reduced brain edema, improved neurological function and protected BBB after MCAO by increasing Claudin5 and ZO-1 levels and decreasing TMEM16A and AQP4 levels. The effect of sevoflurane was weakened by overexpression of TMEM16A and enhanced by knockout of its expression. And when using the inhibitor KN-93, CaMKII level increased while TMEM16A level decreased, enhancing the neuroprotective effect of sevoflurane. Conversely, the effect of sevoflurane was weakened after using the agonist CALP1. Similarly, these manifestations were also observed after OGD injury. In brief, our findings suggest sevoflurane could reduce brain edema, and protect the BBB after cerebral ischemia-reperfusion injury which are related to the downregulation of CaMKII to inhibit TMEM16A.http://www.sciencedirect.com/science/article/pii/S0361923025002916sevofluranetransmembrane protein 16 Acalmodulin-dependent protein kinase IIcerebral ischemiabrain edemablood-brain barrier
spellingShingle Jingbin Zhang
Yuhe Tian
Ruixue Wang
Xinlei Qin
Quntao Li
Ketao Ma
Junqiang Si
Dong Zhao
Yan Li
Jiangwen Yin
Sevoflurane reduces brain edema and improves blood-brain barrier by downregulating CaMKII to inhibit TMEM16A after cerebral ischemia injury both in vivo and in vitro
Brain Research Bulletin
sevoflurane
transmembrane protein 16 A
calmodulin-dependent protein kinase II
cerebral ischemia
brain edema
blood-brain barrier
title Sevoflurane reduces brain edema and improves blood-brain barrier by downregulating CaMKII to inhibit TMEM16A after cerebral ischemia injury both in vivo and in vitro
title_full Sevoflurane reduces brain edema and improves blood-brain barrier by downregulating CaMKII to inhibit TMEM16A after cerebral ischemia injury both in vivo and in vitro
title_fullStr Sevoflurane reduces brain edema and improves blood-brain barrier by downregulating CaMKII to inhibit TMEM16A after cerebral ischemia injury both in vivo and in vitro
title_full_unstemmed Sevoflurane reduces brain edema and improves blood-brain barrier by downregulating CaMKII to inhibit TMEM16A after cerebral ischemia injury both in vivo and in vitro
title_short Sevoflurane reduces brain edema and improves blood-brain barrier by downregulating CaMKII to inhibit TMEM16A after cerebral ischemia injury both in vivo and in vitro
title_sort sevoflurane reduces brain edema and improves blood brain barrier by downregulating camkii to inhibit tmem16a after cerebral ischemia injury both in vivo and in vitro
topic sevoflurane
transmembrane protein 16 A
calmodulin-dependent protein kinase II
cerebral ischemia
brain edema
blood-brain barrier
url http://www.sciencedirect.com/science/article/pii/S0361923025002916
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