Characteristics of Electroacupuncture Preconditioning and Treatment on Regulation of the Brain Transcriptome in Rats with Ischemic Stroke

Background: Accumulating evidence suggests that acupuncture may serve as a potent strategy to mitigate the deleterious effects of ischemic stroke on neural tissue. The present investigation delineated the neuroprotective potential of electroacupuncture (EA) administered pre-and post-stroke, with a f...

Full description

Bibliographic Details
Main Authors: Shuping Fu, Bufan Wu, Rou Peng, Houxi Xu, Xinyue Jing, Ling OuYang, Min Zhang, Tanqing Xu, Chang Chen, Shengfeng Lu
Format: Article
Language:English
Published: IMR Press 2023-11-01
Series:Frontiers in Bioscience-Landmark
Subjects:
Online Access:https://www.imrpress.com/journal/FBL/28/11/10.31083/j.fbl2811291
_version_ 1827592722445238272
author Shuping Fu
Bufan Wu
Rou Peng
Houxi Xu
Xinyue Jing
Ling OuYang
Min Zhang
Tanqing Xu
Chang Chen
Shengfeng Lu
author_facet Shuping Fu
Bufan Wu
Rou Peng
Houxi Xu
Xinyue Jing
Ling OuYang
Min Zhang
Tanqing Xu
Chang Chen
Shengfeng Lu
author_sort Shuping Fu
collection DOAJ
description Background: Accumulating evidence suggests that acupuncture may serve as a potent strategy to mitigate the deleterious effects of ischemic stroke on neural tissue. The present investigation delineated the neuroprotective potential of electroacupuncture (EA) administered pre-and post-stroke, with a focus on determining the commonalities and disparities between these two therapeutic approaches in ameliorating ischemic stroke-induced brain injury. The ultimate objective is to inform optimal timing for acupuncture intervention in the clinical management and prevention of stroke. Methods: The extent of cerebral infarction was quantified with 2,3,5-triphenyltetrazolium chloride staining. The integrity of the blood–brain barrier was assessed by evaluating the extravasation of Evans blue (EB) dye, while neurological function was appraised using the Longa neurological scoring system. RNA sequencing was employed to examine the transcriptomic landscape of ischemic brain tissue, with subsequent bioinformatics annotation of the sequencing data facilitated by Metascape. Results: (1) A notable decrease in the ischemic infarct volume was observed in both the EA-preconditioned plus middle cerebral artery occlusion (MCAO), EA-preconditioned plus middle cerebral artery occlusion (EAM) and MCAO plus EA-treated (MEA) groups, compared to the MCAO group. Furthermore, the decreased leakage of EB and reduction in neurological function impairment scores were evident in the EAM and MEA groups compared with the MCAO group. (2) Relative to the Sham group, the MCAO group exhibited a total of 4798 differentially expressed genes (DEGs), with 67.84% demonstrating an expression fold change (FC) greater than 1.5, and 34.16% exceeding a FC of 2. The EAM and MEA groups displayed 4020 and 1956 DEGs, respectively, compared to the MCAO group. In both groups, more than 55% of DEGs showed an expression FC surpassing 1.5, whereas only approximately 10% exhibited a change greater than 2-fold. Remarkably, EA preconditioning and EA treatment resulted in the reversal of 18.72% and 28.91% of DEGs, respectively, in the MCAO group. (3) The DEGs upregulated in response to ischemic stroke were predominantly implicated in immune inflammatory processes and cellular apoptosis, whereas the downregulated DEGs were associated with neurogenesis and neuronal signal transduction. The MEA-induced upregulated DEGs were primarily involved in neural transmission and metabolic processes, whereas the downregulated DEGs were linked to excessive inflammatory responses to physical and chemical stimuli, as well as cell matrix adhesion chemotaxis. In the context of EAM, the upregulated DEGs were chiefly related to protein biosynthesis, and energy and metabolic processes, whereas the downregulated genes were connected to gene transcriptional activity, synaptic function, and neuronal architecture. Conclusions: Both preconditioning and post-event treatment with acupuncture demonstrated efficacy in mitigating pathological damage to brain tissue in a rat model of ischemic stroke, albeit with some divergences in their gene targets. The integration of EA preconditioning and treatment may potentially confer enhanced neuroprotection in the clinical management of stroke patients.
first_indexed 2024-03-09T01:59:33Z
format Article
id doaj.art-4d77a089e7c74bb695afbe2116692adf
institution Directory Open Access Journal
issn 2768-6701
language English
last_indexed 2024-03-09T01:59:33Z
publishDate 2023-11-01
publisher IMR Press
record_format Article
series Frontiers in Bioscience-Landmark
spelling doaj.art-4d77a089e7c74bb695afbe2116692adf2023-12-08T07:49:20ZengIMR PressFrontiers in Bioscience-Landmark2768-67012023-11-01281129110.31083/j.fbl2811291S2768-6701(23)00928-0Characteristics of Electroacupuncture Preconditioning and Treatment on Regulation of the Brain Transcriptome in Rats with Ischemic StrokeShuping Fu0Bufan Wu1Rou Peng2Houxi Xu3Xinyue Jing4Ling OuYang5Min Zhang6Tanqing Xu7Chang Chen8Shengfeng Lu9Key Laboratory of Acupuncture and Medicine Research of Ministry of Education, Nanjing University of Chinese Medicine, 210023 Nanjing, Jiangsu, ChinaKey Laboratory of Acupuncture and Medicine Research of Ministry of Education, Nanjing University of Chinese Medicine, 210023 Nanjing, Jiangsu, ChinaKey Laboratory of Acupuncture and Medicine Research of Ministry of Education, Nanjing University of Chinese Medicine, 210023 Nanjing, Jiangsu, ChinaKey Laboratory of Acupuncture and Medicine Research of Ministry of Education, Nanjing University of Chinese Medicine, 210023 Nanjing, Jiangsu, ChinaKey Laboratory of Acupuncture and Medicine Research of Ministry of Education, Nanjing University of Chinese Medicine, 210023 Nanjing, Jiangsu, ChinaKey Laboratory of Acupuncture and Medicine Research of Ministry of Education, Nanjing University of Chinese Medicine, 210023 Nanjing, Jiangsu, ChinaKey Laboratory of Acupuncture and Medicine Research of Ministry of Education, Nanjing University of Chinese Medicine, 210023 Nanjing, Jiangsu, ChinaKey Laboratory of Acupuncture and Medicine Research of Ministry of Education, Nanjing University of Chinese Medicine, 210023 Nanjing, Jiangsu, ChinaSchool of Elderly Care Services and Management, Nanjing University of Chinese Medicine, 210023 Nanjing, Jiangsu, ChinaKey Laboratory of Acupuncture and Medicine Research of Ministry of Education, Nanjing University of Chinese Medicine, 210023 Nanjing, Jiangsu, ChinaBackground: Accumulating evidence suggests that acupuncture may serve as a potent strategy to mitigate the deleterious effects of ischemic stroke on neural tissue. The present investigation delineated the neuroprotective potential of electroacupuncture (EA) administered pre-and post-stroke, with a focus on determining the commonalities and disparities between these two therapeutic approaches in ameliorating ischemic stroke-induced brain injury. The ultimate objective is to inform optimal timing for acupuncture intervention in the clinical management and prevention of stroke. Methods: The extent of cerebral infarction was quantified with 2,3,5-triphenyltetrazolium chloride staining. The integrity of the blood–brain barrier was assessed by evaluating the extravasation of Evans blue (EB) dye, while neurological function was appraised using the Longa neurological scoring system. RNA sequencing was employed to examine the transcriptomic landscape of ischemic brain tissue, with subsequent bioinformatics annotation of the sequencing data facilitated by Metascape. Results: (1) A notable decrease in the ischemic infarct volume was observed in both the EA-preconditioned plus middle cerebral artery occlusion (MCAO), EA-preconditioned plus middle cerebral artery occlusion (EAM) and MCAO plus EA-treated (MEA) groups, compared to the MCAO group. Furthermore, the decreased leakage of EB and reduction in neurological function impairment scores were evident in the EAM and MEA groups compared with the MCAO group. (2) Relative to the Sham group, the MCAO group exhibited a total of 4798 differentially expressed genes (DEGs), with 67.84% demonstrating an expression fold change (FC) greater than 1.5, and 34.16% exceeding a FC of 2. The EAM and MEA groups displayed 4020 and 1956 DEGs, respectively, compared to the MCAO group. In both groups, more than 55% of DEGs showed an expression FC surpassing 1.5, whereas only approximately 10% exhibited a change greater than 2-fold. Remarkably, EA preconditioning and EA treatment resulted in the reversal of 18.72% and 28.91% of DEGs, respectively, in the MCAO group. (3) The DEGs upregulated in response to ischemic stroke were predominantly implicated in immune inflammatory processes and cellular apoptosis, whereas the downregulated DEGs were associated with neurogenesis and neuronal signal transduction. The MEA-induced upregulated DEGs were primarily involved in neural transmission and metabolic processes, whereas the downregulated DEGs were linked to excessive inflammatory responses to physical and chemical stimuli, as well as cell matrix adhesion chemotaxis. In the context of EAM, the upregulated DEGs were chiefly related to protein biosynthesis, and energy and metabolic processes, whereas the downregulated genes were connected to gene transcriptional activity, synaptic function, and neuronal architecture. Conclusions: Both preconditioning and post-event treatment with acupuncture demonstrated efficacy in mitigating pathological damage to brain tissue in a rat model of ischemic stroke, albeit with some divergences in their gene targets. The integration of EA preconditioning and treatment may potentially confer enhanced neuroprotection in the clinical management of stroke patients.https://www.imrpress.com/journal/FBL/28/11/10.31083/j.fbl2811291ischemic strokeelectroacupuncturerna sequencing
spellingShingle Shuping Fu
Bufan Wu
Rou Peng
Houxi Xu
Xinyue Jing
Ling OuYang
Min Zhang
Tanqing Xu
Chang Chen
Shengfeng Lu
Characteristics of Electroacupuncture Preconditioning and Treatment on Regulation of the Brain Transcriptome in Rats with Ischemic Stroke
Frontiers in Bioscience-Landmark
ischemic stroke
electroacupuncture
rna sequencing
title Characteristics of Electroacupuncture Preconditioning and Treatment on Regulation of the Brain Transcriptome in Rats with Ischemic Stroke
title_full Characteristics of Electroacupuncture Preconditioning and Treatment on Regulation of the Brain Transcriptome in Rats with Ischemic Stroke
title_fullStr Characteristics of Electroacupuncture Preconditioning and Treatment on Regulation of the Brain Transcriptome in Rats with Ischemic Stroke
title_full_unstemmed Characteristics of Electroacupuncture Preconditioning and Treatment on Regulation of the Brain Transcriptome in Rats with Ischemic Stroke
title_short Characteristics of Electroacupuncture Preconditioning and Treatment on Regulation of the Brain Transcriptome in Rats with Ischemic Stroke
title_sort characteristics of electroacupuncture preconditioning and treatment on regulation of the brain transcriptome in rats with ischemic stroke
topic ischemic stroke
electroacupuncture
rna sequencing
url https://www.imrpress.com/journal/FBL/28/11/10.31083/j.fbl2811291
work_keys_str_mv AT shupingfu characteristicsofelectroacupuncturepreconditioningandtreatmentonregulationofthebraintranscriptomeinratswithischemicstroke
AT bufanwu characteristicsofelectroacupuncturepreconditioningandtreatmentonregulationofthebraintranscriptomeinratswithischemicstroke
AT roupeng characteristicsofelectroacupuncturepreconditioningandtreatmentonregulationofthebraintranscriptomeinratswithischemicstroke
AT houxixu characteristicsofelectroacupuncturepreconditioningandtreatmentonregulationofthebraintranscriptomeinratswithischemicstroke
AT xinyuejing characteristicsofelectroacupuncturepreconditioningandtreatmentonregulationofthebraintranscriptomeinratswithischemicstroke
AT lingouyang characteristicsofelectroacupuncturepreconditioningandtreatmentonregulationofthebraintranscriptomeinratswithischemicstroke
AT minzhang characteristicsofelectroacupuncturepreconditioningandtreatmentonregulationofthebraintranscriptomeinratswithischemicstroke
AT tanqingxu characteristicsofelectroacupuncturepreconditioningandtreatmentonregulationofthebraintranscriptomeinratswithischemicstroke
AT changchen characteristicsofelectroacupuncturepreconditioningandtreatmentonregulationofthebraintranscriptomeinratswithischemicstroke
AT shengfenglu characteristicsofelectroacupuncturepreconditioningandtreatmentonregulationofthebraintranscriptomeinratswithischemicstroke