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Article(id=1212693247529501685, tenantId=1146029695717560320, journalId=1190317699101192196, issueId=1212693246539649865, articleNumber=1001-2494(2024)19-1825-09, orderNo=null, doi=10.11669/cpj.2024.19.006, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=research-article, receivedDate=1710259200000, receivedDateStr=2024-03-13, revisedDate=null, revisedDateStr=null, acceptedDate=null, acceptedDateStr=null, onlineDate=1767058200958, onlineDateStr=2025-12-30, pubDate=1728316800000, pubDateStr=2024-10-08, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1767058200958, onlineIssueDateStr=2025-12-30, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1767058200958, creator=13701087609, updateTime=1767058200958, updator=13701087609, issue=Issue{id=1212693246539649865, tenantId=1146029695717560320, journalId=1190317699101192196, year='2024', volume='59', issue='19', pageStart='1781', pageEnd='1880', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1767058200723, creator=13701087609, updateTime=1767059042003, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1212696775207600634, tenantId=1146029695717560320, journalId=1190317699101192196, issueId=1212693246539649865, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1212696775207600635, tenantId=1146029695717560320, journalId=1190317699101192196, issueId=1212693246539649865, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=1825, endPage=1833, ext={EN=ArticleExt(id=1212693247802131447, articleId=1212693247529501685, tenantId=1146029695717560320, journalId=1190317699101192196, language=EN, title=The Role of NLRP3 Inflammasome-mediated Ferroptosis in Sevoflurane-Induced Postoperative Cognitive Dysfunction in Rats, columnId=null, journalTitle=Chinese Pharmaceutical Journal, columnName=null, runingTitle=null, highlight=null, articleAbstract=

OBJECTIVE To explore the role of NLRP3 inflammasome-mediated ferroptosis in sevoflurane (Sev) induced postoperative cognitive dysfunction (POCD) in rats. METHODS The POCD rat model was established by 4% Sev inhalation anesthesia and abdominal exploration. Firstly, 18-20-month-old SD rats were randomly divided into control group and Sev anesthesia group, with 10 rats in each group. Secondly, SD rats were randomly divided into control group, NLRP3 inflammasome inhibitor group (MCC950), Sev group, and Sev+MCC950 group, with 10 rats in each group. The rats in MCC950 group and Sev+MCC950 group were intraperitoneally injected with 3 mg·kg-1 MCC950 at 1 h before anesthesia. The rats in the control group and Sev group were intraperitoneally injected with the same amount of normal saline. The learning and memory function of the rats was detected by Morris water maze test, the histopathological changes of hippocampus was observed by HE staining, the apoptosis of hippocampal neurons was detected by TUNEL, Prussian blue staining was used to detect iron deposits in the hippocampus, and the expressions of NLRP3 inflammasome-related proteins and ferroptosis-related proteins in hippocampus were detected by Western blot. Detection of oxidative stress levels in hippocampal tissue by ELISA, the content of Fe2+ was detected by colorimetry, and reactive oxygen species (ROS) levels were detected by DHE staining. RESULTS Compared with the control group, there were no significant differences in learning and memory function, hippocampal tissue structure, oxidative stress, ROS and Fe2+ levels, NLRP3 inflammasome-related proteins and ferroptosis-related proteins expression in MCC950 group (P>0.05). In the Sev group and Sev+MCC950 group of rats, there were significant learning and memory dysfunction and pathological injury of hippocampus, the activities of SOD and GSH in hippocampus were significantly decreased, the levels of MDA, ROS and Fe2+ were significantly increased, and the expressions of NLRP3 inflammasome related proteins and ACSL4 proteins were significantly increased, the protein expressions of SLC7A11 and GPX4 were significantly decreased (P<0.05). Compared with the Sev group, the learning and memory function of rats and the degree of pathological damage of hippocampal tissue were significantly alleviated, the activities of SOD and GSH in hippocampal tissue were significantly increased, the levels of MDA, ROS and Fe2+ were significantly decreased, and the expressions of NLRP3 inflammasome-related proteins and ACSL4 proteins were significantly decreased, the protein expressions of SLC7A11 and GPX4 were significantly increased in the Sev+MCC950 (P<0.05). CONCLUSION Sev induces POCD in rats, and its mechanism may be related to the activation of NLRP3 inflammasome-induced neuronal ferroptosis in the hippocampus.

, correspAuthors=Zhen WANG, authorNote=null, correspAuthorsNote=null, copyrightStatement=null, copyrightOwner=null, extLink=null, articleAbsUrl=null, sourceXml=null, magXml=null, pdfUrl=null, pdf=null, pdfFileSize=null, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=null, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=null, mapNumber=null, authorCompany=null, fund=null, authors=null, authorsList=Lei LI, Pengcheng WANG, Guoqing ZHANG, Zhen WANG), CN=ArticleExt(id=1212693250020917289, articleId=1212693247529501685, tenantId=1146029695717560320, journalId=1190317699101192196, language=CN, title=基于NLRP3炎症小体介导的铁死亡探究七氟烷诱导的大鼠术后认知功能障碍的作用机制, columnId=1190352405612040510, journalTitle=中国药学杂志, columnName=论著, runingTitle=null, highlight=null, articleAbstract=

目的 探究NOD样受体蛋白3(NOD-like receptor protein 3,NLRP3)炎症小体介导的铁死亡机制在七氟烷(Sev)诱导大鼠术后认知功能障碍(POCD)中的作用。方法 采取体积分数4% Sev吸入麻醉及腹腔探查术构建POCD大鼠模型。首先,将18~20月龄SD大鼠随机分为对照组(Control)和Sev麻醉组,每组各10只。其次,将SD大鼠随机分为Control组、NOD样受体蛋白3(NLRP3)炎症小体抑制剂组(MCC950)、Sev组、Sev+MCC950组,每组各10只。MCC950组和Sev+MCC950组大鼠麻醉前1 h腹腔注射3 mg·kg-1 MCC950;Control组和Sev组大鼠腹腔注射等量的生理盐水。通过Morris水迷宫实验检测大鼠学习记忆功能,HE染色观察海马组织病理学变化,TUNEL检测海马神经元细胞凋亡情况,普鲁士蓝染色检测海马组织铁离子沉积情况,Western blot检测海马组织NLRP3炎症小体相关蛋白及细胞铁死亡相关蛋白表达,ELISA检测海马组织氧化应激水平,比色法检测Fe2+含量,二氢乙锭(DHE)染色法检测活性氧(ROS)水平。结果 与Control组相比,MCC950组大鼠学习记忆功能、海马组织结构形态、海马组织氧化应激、ROS及Fe2+水平、NLRP3炎症小体相关蛋白及细胞铁死亡相关蛋白表达均无明显差异(P>0.05),Sev和Sev+MCC950组大鼠出现明显的学习记忆功能障碍和海马组织病理损伤,海马组织超氧化物歧化酶(SOD)、谷胱甘肽过氧化物酶(GSH)活性显著降低,丙二醛(MDA)、ROS、Fe2+水平显著升高,NLRP3炎症小体相关蛋白和ACSL4蛋白表达显著升高,SLC7A11、GPX4蛋白表达显著降低(P<0.05)。与Sev组相比,Sev+MCC950组大鼠学习记忆功能,海马组织病理损伤程度明显减轻,海马组织SOD、GSH活性显著增强,MDA、ROS、Fe2+水平显著降低,NLRP3炎症小体相关蛋白和ACSL4蛋白表达显著降低,SLC7A11、GPX4蛋白表达显著升高(P<0.05)。结论 Sev诱导大鼠POCD,其机制可能与激活NLRP3炎症小体诱导的海马神经元细胞铁死亡有关。

, correspAuthors=王震, authorNote=null, correspAuthorsNote=
* 王震,男,本科,副主任医师 研究方向:麻醉学临床及其机制研究 Tel:(0396)2726003
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李磊,男,本科,主治医师 研究方向:麻醉学临床及其机制研究

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李磊,男,本科,主治医师 研究方向:麻醉学临床及其机制研究

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李磊,男,本科,主治医师 研究方向:麻醉学临床及其机制研究

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A-effect of Sev on escape latency in rats; B-Sev on the number of crossing the platform; C-effect of Sev on percentage of target quadrant dwell time; D-pathological staining of hippocampal CA1 region (HE, 200×); E-effect of Sev on apoptosis of hippocampal neurons (TUNEL, 200×); F-Neuropathological evaluation; G-Percentage of TUNEL positive cells; 1)P<0.05, vs control.

, figureFileSmall=vvRJ/ZY9Y1ub/E51MqEQNQ==, figureFileBig=B2Hiz+NCGe/x9KIAU3viXg==, tableContent=null), ArticleFig(id=1212795877413011544, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1212693247529501685, language=CN, label=图1, caption=七氟烷(Sev)对大鼠神经功能的影响。n=6,$\stackrel{-}{x}$±s

A-Sev对大鼠逃避潜伏期的影响;B-Sev对大鼠穿越平台次数的影响;C-Sev对目标象限停留时间占比的影响;D-海马组织CA1区域病理学染色(HE,200×);E-Sev对海马神经元细胞凋亡的影响(TUNEL,200×);F-神经病理学评估;G-TUNEL阳性细胞比率;与Control组相比,1)P<0.05。

, figureFileSmall=vvRJ/ZY9Y1ub/E51MqEQNQ==, figureFileBig=B2Hiz+NCGe/x9KIAU3viXg==, tableContent=null), ArticleFig(id=1212795877522063457, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1212693247529501685, language=EN, label=Fig.2, caption=Effects of sevoflurane on the expression of NLRP3 inflammasome related proteins in rat hippocampal tissue.n=6,$\stackrel{-}{x}$±s

1)P<0.05, vs control.

, figureFileSmall=A86vFAo6WsnrmLeDPmSphQ==, figureFileBig=ST+nLtl7oGDnrs86KnNnPw==, tableContent=null), ArticleFig(id=1212795877652086886, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1212693247529501685, language=CN, label=图2, caption=Sev对大鼠海马组织NOD样受体蛋白3(NLRP3)炎症小体相关蛋白表达的影响。n=6,$\stackrel{-}{x}$±s

与Control组相比,1)P<0.05。

, figureFileSmall=A86vFAo6WsnrmLeDPmSphQ==, figureFileBig=ST+nLtl7oGDnrs86KnNnPw==, tableContent=null), ArticleFig(id=1212795877740167274, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1212693247529501685, language=EN, label=Fig.3, caption=Effects of sevoflurane on ferroptosis in rat neuronal cells. n=6,$\stackrel{-}{x}$±s

A-effect of Sev on SOD activity in hippocampus; B-effect of Sev on MDA content in hippocampus; C-effect of Sev on GSH activity in hippocampus; D-effect of Sev on Fe2+ level in hippocampus; E-iron deposits of CA1 in hippocampus were detected by Prussian blue staining (400×); F-effect of Sev on ROS levels in hippocampus (DHE, 400×); G-Histogram of ROS levels in hippocampal tissue; H-The expression of ACSL4, SLC7A11, GPX4 proteins; I-Histogram of ACSL4 protein expression; J-Histogram of SLC7A11 protein expression; K-Histogram of GPX4 protein expression; 1)P<0.05, vs control.

, figureFileSmall=59SuLYRB1NsVAYLhsgqWpA==, figureFileBig=4l4R8GBhoIYVNJ0PKgZycQ==, tableContent=null), ArticleFig(id=1212795877824053358, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1212693247529501685, language=CN, label=图3, caption=Sev对大鼠神经元细胞铁死亡的影响。n=6,$\stackrel{-}{x}$±s

A-Sev对海马组织超氧化物歧化酶(SOD)活性的影响;B-Sev对海马组织丙二醛(MDA)含量的影响;C-Sev对海马组织谷胱甘肽过氧化物酶(GSH)活性的影响;D-Sev对海马组织Fe2+水平的影响;E-普鲁士蓝染色检测海马组织第一区域(cornu ammonis 1)铁沉积(400×);F-Sev对海马组织活性氧(ROS)水平的影响(DHE,400×);G-海马组织ROS水平统计柱状图;H-ACSL4、SLC7A11、GPX4蛋白表达;I-ACSL4蛋白表达统计柱状图;J-SLC7A11蛋白表达统计柱状图;K-GPX4蛋白表达统计柱状图;与control组相比,1)P<0.05。

, figureFileSmall=59SuLYRB1NsVAYLhsgqWpA==, figureFileBig=4l4R8GBhoIYVNJ0PKgZycQ==, tableContent=null), ArticleFig(id=1212795877928910967, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1212693247529501685, language=EN, label=Fig.4, caption=Effects of MCC950 on neural function in POCD rats. n=6,$\stackrel{-}{x}$±s

A-Morris water maze experiment was used to detect the learning and memory function of rats; B-pathological staining of hippocampal CA1 region (HE, 200×); 1)P<0.05, vs Control; 2)P<0.05, vs Sev.

, figureFileSmall=IW333I0WYSqce4RFK3h5Rw==, figureFileBig=5PX5kp96ltuBQi0M8jEXuw==, tableContent=null), ArticleFig(id=1212795878004408441, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1212693247529501685, language=CN, label=图4, caption=MCC950对术后认知功能障碍(POCD)大鼠神经功能的影响。n=6,$\stackrel{-}{x}$±s

A-Morris水迷宫实验检测各组大鼠学习记忆功能;B-海马组织CA1区域病理学染色(HE,200×);与Control组相比,1)P<0.05;与Sev组相比,2)P<0.05。

, figureFileSmall=IW333I0WYSqce4RFK3h5Rw==, figureFileBig=5PX5kp96ltuBQi0M8jEXuw==, tableContent=null), ArticleFig(id=1212795878096683134, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1212693247529501685, language=EN, label=Fig.5, caption=Effects of MCC950 on NLRP3 inflammasome in hippocampal tissue of POCD rats.n=6,$\stackrel{-}{x}$±s

1)P<0.05, vs Control; 2)P<0.05, vs Sev.

, figureFileSmall=JHlEhElx6YLOyUUgsdyUdg==, figureFileBig=qRBMUm5DuvHJJWRsYBpDnw==, tableContent=null), ArticleFig(id=1212795878184763523, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1212693247529501685, language=CN, label=图5, caption=MCC950对POCD大鼠海马组织NLRP3炎症小体的影响。n=6,$\stackrel{-}{x}$±s

与Control组相比,1)P<0.05;与Sev组相比,2)P<0.05。

, figureFileSmall=JHlEhElx6YLOyUUgsdyUdg==, figureFileBig=qRBMUm5DuvHJJWRsYBpDnw==, tableContent=null), ArticleFig(id=1212795878277038217, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1212693247529501685, language=EN, label=Fig.6, caption=The effect of MCC950 on oxidative stress levels in POCD rats. n=6,$\stackrel{-}{x}$±s

A-SOD activity in hippocampal tissue of rats in each group; B-MDA content in hippocampus of rats in each group; C-GSH activity in hippocampal tissue of rats in each group; 1)P<0.05, vs Control; 2)P<0.05, vs Sev.

, figureFileSmall=LiDBNxhhDZIsUP3G4gDI5A==, figureFileBig=dgfVxUjFcDyVRHS95rQIBw==, tableContent=null), ArticleFig(id=1212795878365118606, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1212693247529501685, language=CN, label=图6, caption=MCC950对POCD大鼠氧化应激水平的影响。n=6,$\stackrel{-}{x}$±s

A-各组大鼠海马组织SOD活性;B-各组大鼠海马组织MDA含量;C-各组大鼠海马组织GSH活性;与Control组相比,1)P<0.05;与Sev组相比,2)P<0.05。

, figureFileSmall=LiDBNxhhDZIsUP3G4gDI5A==, figureFileBig=dgfVxUjFcDyVRHS95rQIBw==, tableContent=null), ArticleFig(id=1212795878419644561, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1212693247529501685, language=EN, label=Fig.7, caption=Effects of MCC950 on ROS and Fe2+ levels in hippocampal tissue of POCD rats.n=6,$\stackrel{-}{x}$±s

A-Fe2+ level in hippocampal tissue of rats in each group; B-ROS levels in hippocampal tissue of rats in each group; 1)P<0.05, vs Control; 2)P<0.05, vs Sev.

, figureFileSmall=6+UreFCr92zu45MTgy7g0w==, figureFileBig=+BU7JXlb+6koyFKVDtexVA==, tableContent=null), ArticleFig(id=1212795878490947736, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1212693247529501685, language=CN, label=图7, caption=MCC950对POCD大鼠海马组织ROS、Fe2+水平的影响。n=6,$\stackrel{-}{x}$±s

A-各组大鼠海马组织Fe2+水平;B-各组大鼠海马组织ROS水平;与Control组相比,1)P<0.05;与Sev组相比,2)P<0.05。

, figureFileSmall=6+UreFCr92zu45MTgy7g0w==, figureFileBig=+BU7JXlb+6koyFKVDtexVA==, tableContent=null), ArticleFig(id=1212795878583222428, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1212693247529501685, language=EN, label=Fig.8, caption=The effects of MCC950 on ferroptosis in hippocampal neurons of POCD rats.n=6,$\stackrel{-}{x}$±s

A-observation of pathological changes in nerve cells by electron microscopy, the white arrow represents chromatin condensation and marginalization, the black arrow represents abnormal mitochondria, the red box represents the enlarged part of the cytoplasm of nerve cells; B-Western blot detection of ACSL4, SLC7A11, and GPX4 protein expression in hippocampal tissue;1)P<0.05, vs Control; 2)P<0.05, vs Sev.

, figureFileSmall=7utzGLgz0LymQvOzLntqTA==, figureFileBig=fDL0zGewW0ChZ1iwaMBw+Q==, tableContent=null), ArticleFig(id=1212795878662914207, tenantId=1146029695717560320, journalId=1190317699101192196, articleId=1212693247529501685, language=CN, label=图8, caption=MCC950对POCD大鼠海马神经元细胞铁死亡的影响。n=6,$\stackrel{-}{x}$±s

A-电镜观察神经细胞病理变化,白色箭头-染色质凝集并边缘化,黑色箭头-异常的线粒体,红色方框-神经细胞细胞质放大部位;B-Western blot检测海马组织ACSL4、SLC7A11、GPX4蛋白表达;与Control组相比,1)P<0.05;与Sev组相比,2)P<0.05。

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基于NLRP3炎症小体介导的铁死亡探究七氟烷诱导的大鼠术后认知功能障碍的作用机制
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李磊 , 王鹏程 , 张国庆 , 王震 *
中国药学杂志 | 论著 2024,59(19): 1825-1833
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中国药学杂志 | 论著 2024, 59(19): 1825-1833
基于NLRP3炎症小体介导的铁死亡探究七氟烷诱导的大鼠术后认知功能障碍的作用机制
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李磊, 王鹏程, 张国庆, 王震*
作者信息
  • 驻马店市中心医院麻醉科, 河南 驻马店 463000

    • 李磊,男,本科,主治医师 研究方向:麻醉学临床及其机制研究

通讯作者:

* 王震,男,本科,副主任医师 研究方向:麻醉学临床及其机制研究 Tel:(0396)2726003
The Role of NLRP3 Inflammasome-mediated Ferroptosis in Sevoflurane-Induced Postoperative Cognitive Dysfunction in Rats
Lei LI, Pengcheng WANG, Guoqing ZHANG, Zhen WANG*
Affiliations
  • Department of Anesthesia, Zhumadian Central Hospital, Zhumadian 463000, China
出版时间: 2024-10-08 doi: 10.11669/cpj.2024.19.006
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目的 探究NOD样受体蛋白3(NOD-like receptor protein 3,NLRP3)炎症小体介导的铁死亡机制在七氟烷(Sev)诱导大鼠术后认知功能障碍(POCD)中的作用。方法 采取体积分数4% Sev吸入麻醉及腹腔探查术构建POCD大鼠模型。首先,将18~20月龄SD大鼠随机分为对照组(Control)和Sev麻醉组,每组各10只。其次,将SD大鼠随机分为Control组、NOD样受体蛋白3(NLRP3)炎症小体抑制剂组(MCC950)、Sev组、Sev+MCC950组,每组各10只。MCC950组和Sev+MCC950组大鼠麻醉前1 h腹腔注射3 mg·kg-1 MCC950;Control组和Sev组大鼠腹腔注射等量的生理盐水。通过Morris水迷宫实验检测大鼠学习记忆功能,HE染色观察海马组织病理学变化,TUNEL检测海马神经元细胞凋亡情况,普鲁士蓝染色检测海马组织铁离子沉积情况,Western blot检测海马组织NLRP3炎症小体相关蛋白及细胞铁死亡相关蛋白表达,ELISA检测海马组织氧化应激水平,比色法检测Fe2+含量,二氢乙锭(DHE)染色法检测活性氧(ROS)水平。结果 与Control组相比,MCC950组大鼠学习记忆功能、海马组织结构形态、海马组织氧化应激、ROS及Fe2+水平、NLRP3炎症小体相关蛋白及细胞铁死亡相关蛋白表达均无明显差异(P>0.05),Sev和Sev+MCC950组大鼠出现明显的学习记忆功能障碍和海马组织病理损伤,海马组织超氧化物歧化酶(SOD)、谷胱甘肽过氧化物酶(GSH)活性显著降低,丙二醛(MDA)、ROS、Fe2+水平显著升高,NLRP3炎症小体相关蛋白和ACSL4蛋白表达显著升高,SLC7A11、GPX4蛋白表达显著降低(P<0.05)。与Sev组相比,Sev+MCC950组大鼠学习记忆功能,海马组织病理损伤程度明显减轻,海马组织SOD、GSH活性显著增强,MDA、ROS、Fe2+水平显著降低,NLRP3炎症小体相关蛋白和ACSL4蛋白表达显著降低,SLC7A11、GPX4蛋白表达显著升高(P<0.05)。结论 Sev诱导大鼠POCD,其机制可能与激活NLRP3炎症小体诱导的海马神经元细胞铁死亡有关。

术后认知功能障碍  /  七氟烷  /  NOD样受体蛋白3炎症小体  /  铁死亡

OBJECTIVE To explore the role of NLRP3 inflammasome-mediated ferroptosis in sevoflurane (Sev) induced postoperative cognitive dysfunction (POCD) in rats. METHODS The POCD rat model was established by 4% Sev inhalation anesthesia and abdominal exploration. Firstly, 18-20-month-old SD rats were randomly divided into control group and Sev anesthesia group, with 10 rats in each group. Secondly, SD rats were randomly divided into control group, NLRP3 inflammasome inhibitor group (MCC950), Sev group, and Sev+MCC950 group, with 10 rats in each group. The rats in MCC950 group and Sev+MCC950 group were intraperitoneally injected with 3 mg·kg-1 MCC950 at 1 h before anesthesia. The rats in the control group and Sev group were intraperitoneally injected with the same amount of normal saline. The learning and memory function of the rats was detected by Morris water maze test, the histopathological changes of hippocampus was observed by HE staining, the apoptosis of hippocampal neurons was detected by TUNEL, Prussian blue staining was used to detect iron deposits in the hippocampus, and the expressions of NLRP3 inflammasome-related proteins and ferroptosis-related proteins in hippocampus were detected by Western blot. Detection of oxidative stress levels in hippocampal tissue by ELISA, the content of Fe2+ was detected by colorimetry, and reactive oxygen species (ROS) levels were detected by DHE staining. RESULTS Compared with the control group, there were no significant differences in learning and memory function, hippocampal tissue structure, oxidative stress, ROS and Fe2+ levels, NLRP3 inflammasome-related proteins and ferroptosis-related proteins expression in MCC950 group (P>0.05). In the Sev group and Sev+MCC950 group of rats, there were significant learning and memory dysfunction and pathological injury of hippocampus, the activities of SOD and GSH in hippocampus were significantly decreased, the levels of MDA, ROS and Fe2+ were significantly increased, and the expressions of NLRP3 inflammasome related proteins and ACSL4 proteins were significantly increased, the protein expressions of SLC7A11 and GPX4 were significantly decreased (P<0.05). Compared with the Sev group, the learning and memory function of rats and the degree of pathological damage of hippocampal tissue were significantly alleviated, the activities of SOD and GSH in hippocampal tissue were significantly increased, the levels of MDA, ROS and Fe2+ were significantly decreased, and the expressions of NLRP3 inflammasome-related proteins and ACSL4 proteins were significantly decreased, the protein expressions of SLC7A11 and GPX4 were significantly increased in the Sev+MCC950 (P<0.05). CONCLUSION Sev induces POCD in rats, and its mechanism may be related to the activation of NLRP3 inflammasome-induced neuronal ferroptosis in the hippocampus.

postoperative cognitive dysfunction  /  sevoflurane  /  NLRP3 inflammasome  /  ferroptosis
李磊, 王鹏程, 张国庆, 王震. 基于NLRP3炎症小体介导的铁死亡探究七氟烷诱导的大鼠术后认知功能障碍的作用机制. 中国药学杂志, 2024 , 59 (19) : 1825 -1833 . DOI: 10.11669/cpj.2024.19.006
Lei LI, Pengcheng WANG, Guoqing ZHANG, Zhen WANG. The Role of NLRP3 Inflammasome-mediated Ferroptosis in Sevoflurane-Induced Postoperative Cognitive Dysfunction in Rats[J]. Chinese Pharmaceutical Journal, 2024 , 59 (19) : 1825 -1833 . DOI: 10.11669/cpj.2024.19.006
正文
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术后认知功能障碍(postoperative cognitive dysfunction,POCD)是全身麻醉后影响中枢神经系统的常见并发症之一,临床主要表现注意力、记忆等认知功能障碍[1]。POCD可导致患者术后神经功能恢复时间延长,尤其是对老年患者的生活能力和生活质量影响较为严重[2]。有研究表明,年龄的增加是POCD的独立危险因素,老年患者POCD发病率高达15%~60%,已经成为麻醉学领域研究的热点及社会关注的重点问题[3]。因此,探究POCD的致病机制对于临床防治POCD具有重要意义。
多项研究均已证明,POCD的病理生理机制与神经炎症[4]、氧化应激[5]以及细胞凋亡[6]等相关,但是确切的级联反应机制仍难以确定。NOD样受体蛋白3(NOD-like receptor protein 3,NLRP3)炎症小体作为神经炎症的关键驱动因素能够通过促进炎症细胞因子释放,加重神经功能损伤[7]。此外,NLRP3炎症小体活化是诱导老年大鼠POCD的重要病理机制,而抑制NLRP3炎症小体活化能够有效改善老年大鼠POCD[8],提示NLRP3炎症小体可能是POCD致病的重要机制。
铁死亡是一种新型的细胞可调节性死亡,区别于细胞凋亡、自噬和坏死,是铁依赖的脂质过氧化物代谢异常,进而导致活性氧(reactive oxygen species,ROS)产生增加,诱发脂质过氧化反应,并最终触发细胞死亡[9]。研究显示,在POCD大鼠海马组织中存在神经元铁死亡发生,抑制神经元铁死亡能够明显改善大鼠POCD[10],表明神经元铁死亡可能是POCD的关键调节机制。Wu等[11]研究证实,采用NLRP3炎症小体抑制剂MCC950处理能够降低海马组织ROS聚集,减弱大鼠脑缺血再灌注诱导的神经元铁死亡。
目前有关NLRP3炎症小体与铁死亡的调控关系在POCD中的作用尚不清楚。越来越多的研究证据表明,吸入性麻醉药可引起老年患者神经系统毒性和认知功能减退[12-13]。七氟烷(sevoflurane,Sev)是临床广泛性使用的吸入性麻醉剂,可通过多种分子机制诱发POCD的发生[14]。因此,本研究拟通过Sev诱导建立老年大鼠POCD模型,探究NLRP3炎症小体介导的铁死亡在其中的作用,以期为POCD的致病机制研究提供可靠的实验依据。
1 材料与方法
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1.1 材料
1.1.1 动物
雄性,18~20月龄,SPF级,体质量550~600 g,SD大鼠60只,购自于上海斯莱克实验动物有限责任公司[SCXK(沪)2022-0008]。动物房温度为(25±1)℃,环境相对湿度为50%~60%,房间内光照黑暗交替,动物自由饮食饮水。本研究通过驻马店市中心医院医学研究伦理委员会审批(批准号:LLSC2022010279)。
1.1.2 试剂
Sev(批号:8023469,江苏恒瑞医药有限公司);MCC950(批号:S7809,美国Selleck公司);原位末端标记染色(TUNEL)试剂盒、苏木素-伊红(hematoxylin-eosin,HE)染色试剂盒、蛋白质浓度测定试剂盒、显影液、山羊抗兔二抗、山羊抗小鼠二抗、谷胱甘肽过氧化酶4(glutathione peroxidase 4,GPX4)抗体、溶质载体家族7成员11(recombinant solute carrier family 7, member 11,SLC7A11)抗体及β-actin抗体(批号:C1088、C0105S、P0011、P0018FS、A0409、A0413、AF7020、AF7992、AF0003,上海碧云天生物技术公司);酰基辅酶A合成酶长链家族成员4(acyl-CoA synthetase long chain family member 4,ACSL4)抗体(批号:ab155282,英国Abcam公司);二氢乙锭(dihydroethidium,DHE,批号:D11347,美国Thermo Fisher Scientific公司);超氧化物歧化酶(superoxide dismutase,SOD)、丙二醛(malondialdehyde,MDA)、谷胱甘肽过氧化物酶(glutathione peroxidase,GSH)、Fe2+检测试剂盒(批号:A001-3-2、A003-1-2、A005-1-2、A039-2-1,南京建成生物工程研究所);NLRP3抗体、凋亡相关斑点样蛋白(apoptosis-associated speck-like protein containing a CARD,ASC)抗体、cleaved-caspase-1抗体、IL-1β抗体、IL-18抗体(批号:15101、67824、89332、12242、57058,美国Cell Signaling Technology公司)。
1.1.3 仪器
BX53型光学显微镜、BX43型荧光显微镜(日本Olympus公司);H-2050R-1型离心机(湖南湘仪实验室仪器开发有限公司);LD-96A型酶标仪(山东莱恩德智能科技有限公司);Gel dox XR+型凝胶成像系统(美国Bio-Rad公司)。
1.2 方法
1.2.1 实验分组及POCD大鼠模型构建
首先,将20只SD大鼠随机分为对照组(Control)和POCD模型组,每组各10只。采用4% Sev吸入麻醉6 h及腹腔探查术构建POCD大鼠模型[15-16]:首先将大鼠放置于麻醉诱导箱内麻醉,麻醉箱进气口由麻醉机通入体积分数4% Sev+2 L·min-1 体积分数30%氧气混合气体,待大鼠麻醉后经腹部正中做大约3 cm长度切口,行腹腔探查术,探查术结束后腹腔注射青霉素(16 u·kg-1)抗感染。除Control组外,其余各组大鼠术后迅速置于麻醉诱导箱内,以体积分数4% Sev+30%氧气混合流通气量2 L·min-1速度持续吸入6 h构建大鼠POCD模型。Control组大鼠进行腹腔探查,仅放置于麻醉箱内吸入空气及O2混合气体。其次,将SD大鼠随机分为Control组、MCC950组、Sev组、Sev+MCC950组,每组各10只。除Control组外,其余各组大鼠均采取体积分数4% sev吸入麻醉及腹腔探查术构建POCD大鼠模型。MCC950组和Sev+MCC950组大鼠麻醉前1 h腹腔注射3 mg·kg-1 MCC950[17];Control组和Sev组大鼠腹腔注射等量的生理盐水。
1.2.2 Morris水迷宫实验评估大鼠认知功能
大鼠麻醉术后1 d进行Morris水迷宫实验,将水迷宫划分4个象限,任意选择其中1个象限水面下放置隐蔽平台,将大鼠从任意象限入水点放入水中,记录大鼠寻找到隐蔽平台的时间,记为逃避潜伏期。每组大鼠均在4个象限入水点分别训练2次,每次间隔15 min,持续4 d,记录第5天的逃避潜伏期。于第6天对大鼠进行空间探索实验,将隐蔽平台撤去,选择任意入水点放入大鼠,记录各组大鼠在60 s内穿越平台的次数及目标象限停留时间占比。
1.2.3 海马组织HE染色、普鲁士蓝染色
取大鼠脑组织,剥离海马组织,采用浓度0.04 g·mL-1多聚甲醛固定海马组织1 d,经石蜡包埋、切片、脱蜡等步骤,行HE染色和普鲁士蓝染色,并于显微镜下观察海马组织病理学变化。海马神经元损伤程度评级通过半定量方式评估。评级分为5级,海马神经元损伤<20%为1级,20%~40%为2级,40%~60%为3级,60%~80%为4级,80%~100%为5级。
1.2.4 海马神经元细胞凋亡检测
37 ℃下将海马组织用蛋白酶K溶液孵育20 min,将TUNEL染色液与海马组织切片共孵育1 h,最后使用二氨基联苯胺显色液将切片孵育5 min,于显微镜下观察并计数海马神经元凋亡数量,每只大鼠选取3张切片,每张切片随机选取5个不同视野,取平均值。
1.2.5 氧化应激指标、Fe2+水平检测
取各组大鼠海马组织,加入预冷的浓度0.009 g·mL-1的氯化钠溶液充分碾磨,置于高速冷冻离心机内并设置转速3 000 r·min-1,离心时长15 min;吸取上清液,比色法检测海马组织匀浆中Fe2+含量,ELISA法检测匀浆中MDA、SOD、GSH含量。
1.2.6 ROS水平检测
取出OTC冻存液中海马组织,冰冻切片机切片,切片放置在37 ℃ Krebs/Hepes缓冲溶液中孵育30 min,PBS清洗,加入DHE染色液,37 ℃孵育盒内孵育30 min。于400倍显微镜下观察海马组织ROS染色情况。采用ImagePro Plus 6.0软件对海马组织ROS相对水平进行半定量分析。
1.2.7 电镜观察海马神经元病理变化
室温条件下,大鼠海马组织采用质量浓度0.025 g·mL-1的戊二醛固定2 h,继续放置4 ℃条件下过夜,固定的组织使用乙醇脱水并嵌入超薄切片中,最后使用乙酸铀酰和柠檬酸铅进行切片复染,于透射电镜下观察海马组织神经元超微结构变化。
1.2.8 Western blot检测NLRP3炎症小体和铁死亡相关蛋白表达
提取大鼠海马组织蛋白,蛋白质变性、上样、凝胶电泳转膜,脱脂牛奶封闭后加入ACSL4、SLC7A11、GPX4、NLRP3、ASC、cleaved-caspase-1、IL-1β、IL-18(稀释比例均为1∶1 000)及β-actin(1∶5 000)一抗抗体,4 ℃孵育过夜、洗膜,室温下加入对应的二抗孵育2 h,洗膜,滴加显影液并通过发光成像系统显影,拍照。最后使用ImagePro Plus 6.0对上述蛋白条带相对表达定量。
1.2.9 统计学分析
SPSS 22.0软件进行统计学数据处理。计量资料以均数±标准差($\stackrel{-}{x}$±s)表示,多组间比较采用单因素方差分析,组间存在差异采用SNK-q检验进行两两比较;两组间比较采用独立样本t检验,以P<0.05为差异具有统计学意义。
2 结果
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2.1 Sev对大鼠神经功能的影响
与Control组相比,Sev组大鼠逃避潜伏期延长,穿越平台次数和目标象限停留时间占比降低(图1A~C,P<0.05)。显微镜下观察海马CA1区域神经元排列紊乱,有部分神经元结构出现细胞核固缩、坏死等现象,神经元损伤评级明显增加(图1D,P<0.05),且海马区域神经元细胞凋亡率显著升高(图1E,P<0.05)。
2.2 Sev对大鼠海马组织NLRP3炎症小体的影响
与Control组相比,Sev组大鼠海马组织NLRP3、ASC、cleaved-caspase-1、IL-1β和IL-18蛋白表达均显著升高(图2,P<0.05)。
2.3 Sev对大鼠神经元细胞铁死亡的影响
与Control组相比,Sev组大鼠海马组织SOD、GSH活性显著降低,MDA、Fe2+水平显著升高(图3A~3D,P<0.05)。普鲁士蓝染色显示棕黄色颗粒为海马组织铁离子沉积,与Control组相比,Sev组大鼠海马组织CA1区域棕黄色铁离子沉积明显增加(图3E,P<0.05),ROS水平升高(图3F,P<0.05)。Western blot检测显示,与Control组相比,Sev组大鼠海马组织SLC7A11、GPX4蛋白表达显著降低,ACSL4蛋白表达显著升高(图3G,P<0.05)。
2.4 MCC950对POCD大鼠神经功能的影响
与Control组相比,MCC950组大鼠逃避潜伏期、穿越平台次数和目标象限停留时间占比均无显著性差异(P>0.05),Sev组和Sev+MCC950组大鼠逃避潜伏期延长,穿越平台次数和目标象限停留时间占比降低(P<0.05)。与Sev组相比, Sev+MCC950组大鼠逃避潜伏期缩短,穿越平台次数和目标象限停留时间占比增加(图4A,P<0.05)。HE染色显示,Control组和MCC950组大鼠海马CA1区域神经元排列整齐,细胞质着色均匀,轮廓清晰,结构形态无明显异常。Sev组大鼠海马神经元排列紊乱,细胞核固缩,轮廓模糊,且伴有大量神经元坏死,结构出现明显异常。与Sev组相比,Sev+MCC950组大鼠海马CA1区域神经元细胞排列紊乱程度减轻,轮廓较为清晰,且神经元坏死明显减少,结构得到明显恢复(图4B)。
2.5 MCC950对POCD大鼠海马组织NLRP3炎症小体的影响
与Control组相比,MCC950组大鼠海马组织NLRP3、ASC、cleaved-caspase-1、IL-1β和IL-18蛋白表达无显著性差异(P>0.05),Sev组和Sev+MCC950组大鼠海马组织NLRP3、ASC、cleaved-caspase-1、IL-1β和IL-18蛋白表达均显著升高(P<0.05)。与Sev组相比,Sev+MCC950组大鼠海马组织NLRP3、ASC、cleaved-caspase-1、IL-1β和IL-18蛋白表达均显著降低(图5,P<0.05)。
2.6 MCC950对POCD大鼠海马组织氧化应激水平的影响
与Control组相比,MCC950组大鼠海马组织SOD、GSH活性,MDA含量无显著性差异(P>0.05),Sev组和Sev+MCC950组大鼠海马组织SOD、GSH活性降低,MDA含量升高(P<0.05)。与Sev组相比,Sev+MCC950组大鼠海马组织SOD、GSH活性增强,MDA含量降低(图6,P<0.05)。
2.7 MCC950对POCD大鼠海马组织ROS、Fe2+水平的影响
与Control组相比,MCC950组大鼠海马组织ROS、Fe2+水平无显著性差异(P>0.05),Sev组和Sev+MCC950组大鼠海马组织ROS、Fe2+水平升高(P<0.05)。与Sev组相比,Sev+MCC950组大鼠海马组织ROS、Fe2+水平降低(图7,P<0.05)。
2.8 MCC950对POCD大鼠海马神经元细胞铁死亡的影响
透射电镜显示,Control组和MCC950组大鼠神经细胞状态良好,线粒体形态结构正常,胞质分布均匀,且染色质形态正常。与Control组相比,Sev组大鼠神经细染色质固缩,边缘化,且伴有线粒体外膜破裂(细胞铁死亡相对特异性形态变化)。与Sev组相比,Sev+MCC950组大鼠神经细胞损伤明显减轻,但是部分细胞仍然有染色质凝集,边缘化,无线粒体外膜破裂,可见线粒体膜密度加深(图8A)。与Control组相比,MCC950组大鼠海马组织ACSL4、SLC7A11、GPX4蛋白表达无显著性差异(P>0.05),Sev组和Sev+MCC950组大鼠海马组织ACSL4蛋白表达显著升高,SLC7A11、GPX4蛋白表达显著降低(P<0.05)。与Sev组相比,Sev+MCC950组大鼠海马组织ACSL4蛋白表达均显著降低,SLC7A11、GPX4蛋白表达显著升高(图8B,P<0.05)。
3 讨论
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Sev是一种新型的卤代羟基醚类吸入性全麻药物,具有诱导迅速、麻醉深度易调节、苏醒快以及对呼吸循环系统抑制程度较轻等优点,是全麻诱导的首选药物[18]。研究表明,吸入性麻醉剂能够通过多种机制诱导神经毒性以及老年患者认知功能损伤[19],但是其具体作用机制尚不完全清楚。麻醉与手术作为一种外源性刺激,被认为是引发老年人群认知功能障碍的危险因素[20]。然而,研究显示Sev诱导的神经毒性与暴露浓度及时间相关,当低于临床麻醉浓度或短时间暴露(<3 h)无神经毒性作用[21]。此外,研究证实,亚麻醉浓度Sev具有一定的器官保护作用,可通过激活钾离子通道以及阻断神经毒性,减轻脑组织损伤,发挥神经功能保护作用[22]。本研究参照文献[16,23]报道体积分数4%的Sev持续性吸入麻醉6 h后能够诱导大鼠认知功能障碍,损伤海马神经功能,导致大鼠POCD。为此本研究拟通过吸入体积分数4%的Sev持续时间6 h和腹腔探查术构建POCD大鼠模型。Sev大鼠出现明显的认知功能障碍及神经元损伤,表明POCD大鼠模型构建成功。
海马区是大脑负责记忆储存和定向转换等功能的重要区域,在炎症、氧化应激等病理因素刺激下会导致神经元细胞出现明显损伤,主要表现为学习、记忆及空间定向能力等认知功能障碍相关症状[24]。NLRP3炎症小体是由NLRP3、ASC、caspase-1组成,广泛表达于多种细胞中,其中神经系统内小胶质细胞是功能性NLRP3炎症小体产生的主要场所[25]。当细胞内ROS或是ATP累积到一定程度会刺激NLRP3炎症小体形成,促进caspase-1活化,进而刺激炎症细胞因子IL-1β、IL-18释放,诱导炎症级联反应[26]。既往研究发现,NLRP3炎症小体介导的炎症反应参与了POCD的发生发展,Sev能够通过ROS-NLRP3炎症小体途径介导的小胶质细胞焦亡诱导老年小鼠POCD,抑制NLRP3炎症小体能够明显减轻Sev诱导的POCD[27]。本研究发现,Sev能够促进NLRP3炎症小体活化。铁死亡是一种新型细胞死亡方式,其核心是脂质过氧化反应失衡,参与了氧化应激、炎症反应等多种病理机制[28]。研究证实,铁死亡的发生参与了POCD的发生发展,主要涉及氧化还原、铁离子稳态及脂质过氧化等[29]。本研究显示,Sev能够抑制氧化应激指标及Fe2+水平。ACSL4、SLC7A11、GPX4蛋白是铁死亡发生的关键调控因子。ACSL4是铁死亡启动的驱动因素,能够促进细胞脂质过氧化产物增多和ROS的堆积,抑制GPX4表达,诱导细胞脂质过氧化反应加重,导致细胞铁死亡发生[30]。SLC7A11介导的胱氨酸/谷氨酸转运系统是合成GSH所需胱氨酸的主要途径,抑制SLC7A11后会降低GSH生物合成,导致GPX4抗氧化能力减低,诱导MDA产生增多,从而导致细胞铁死亡发生[31]。GPX4是细胞中催化还原脂质过氧化产物关键性调控酶,能够降解脂质过氧化产物诱发的细胞毒性[32]。本研究发现,Sev能够抑制细胞铁死亡相关蛋白表达。此外,NLRP3炎症小体活化和铁死亡的发生可能是POCD发生的重要病理机制。但是,有关NLRP3炎症小体活化与铁死亡的调控关系在POCD中的作用尚不清楚。Li等[33]研究证实,在LPS诱导的急性肾损伤小鼠模型中NLRP3炎症小体被显著活化,铁死亡水平明显升高,而抑制NLRP3表达能够降低肾组织炎症和铁死亡改善LPS诱导的小鼠急性肾损伤。此外,Wang等[34]研究也证实,抑制NLRP3炎症小体能够通过调控Keap1-Nrf2信号通路减轻脑缺血再灌注损伤诱导的神经细胞铁死亡。以上研究表明,NLRP3炎症小体可能是铁死亡发生的关键调控因子。为进一步明确NLRP3炎症小体与铁死亡在POCD中的调控机制。为此,本研究通过对POCD的大鼠腹腔注射MCC950,发现抑制NLRP3小体活化能够降低海马神经元铁死亡,减轻Sev诱导的老年大鼠POCD。
综上所述,本研究结果显示,NLRP3炎症小体活化介导的神经元细胞铁死亡机制参与了POCD的发生发展。本研究结果进一步阐明了POCD的致病机制,为POCD治疗研究的干预靶点提供了新的可能。
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2024年第59卷第19期
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doi: 10.11669/cpj.2024.19.006
  • 接收时间：2024-03-13
  • 首发时间：2025-12-30
  • 出版时间：2024-10-08
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  • 收稿日期：2024-03-13
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    驻马店市中心医院麻醉科, 河南 驻马店 463000

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* 王震,男,本科,副主任医师 研究方向:麻醉学临床及其机制研究 Tel:(0396)2726003
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Family		 属数
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genus		 种数
Number of
species		 占总种数比例
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total species (%)		 属
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鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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