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Article(id=1240972423080759614, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1240972413354176744, articleNumber=null, orderNo=null, doi=10.20043/j.cnki.MPM.202311413, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=null, receivedDate=1700582400000, receivedDateStr=2023-11-22, revisedDate=null, revisedDateStr=null, acceptedDate=null, acceptedDateStr=null, onlineDate=1773800481815, onlineDateStr=2026-03-18, pubDate=1715270400000, pubDateStr=2024-05-10, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1773800481815, onlineIssueDateStr=2026-03-18, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1773800481815, creator=13701087609, updateTime=1773800481815, updator=13701087609, issue=Issue{id=1240972413354176744, tenantId=1146029695717560320, journalId=1227665162245664772, year='2024', volume='51', issue='9', pageStart='1537', pageEnd='1728', issueExtLink='null', onlineDate='null', pubDate='null', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=-1, specialIssue=null, createTime=1773800479495, creator=13701087609, updateTime=1773800596829, updator=13701087609, preIssue=null, nextIssue=null, ext={EN=IssueExt(id=1240972905568334240, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1240972413354176744, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1240972905568334241, tenantId=1146029695717560320, journalId=1227665162245664772, issueId=1240972413354176744, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null}, startPage=1695, endPage=1701, ext={EN=ArticleExt(id=1240972423420498267, articleId=1240972423080759614, tenantId=1146029695717560320, journalId=1227665162245664772, language=EN, title=The role of RIPK1/MLKL/PGAM5 pathway in traffic-related PM2.5-induced heart injury in asthmatic mice, columnId=1228016572065837304, journalTitle=Modern Preventive Medicine, columnName=Experimental Technology and Applications, runingTitle=null, highlight=null, articleAbstract=
Objective

To investigate the role of RIPK1/MLKL/PGAM5 pathway in traffic-related PM2.5-induced heart injury in asthmatic mice.

Methods

In total 50 male BALB/c mice were randomly divided into control group (NS group), asthma group (OVA group), OVA+ low concentration PM2.5 group (LPM2.5, 1.8 mg/ kg ·bw), OVA+ medium concentration PM2.5 group (MPM2.5,3.6 mg/ kg ·bw), and OVA+ high concentration PM2.5 group (HPM2.5, 7.2 mg/ kg ·bw). OVA asthma model mice were instilled with different concentrations of PM2.5 suspension through nasal cavity for 10 times. The pathological changes of heart tissue were observed by HE staining, the apoptosis of heart tissue was detected by Tunnel staining, and the protein and mRNA expression levels of RIPK1, RIPK3, MLKL, PGAM5, DRP1, and mRNA in mouse heart tissue were detected by qRT-PCR and Western blot methods.

Results

Compared with NS group, the arrangement of central muscle fibers in PM2.5 group was obviously disordered, the myocardial fibers in HPM2.5 group were obviously broken, and the number of apoptotic cells was significantly increased. The protein expression of RIPK1, RIPK3, MLKL, PGAM5, DRP1, and p-DRP1 in HPM2.5 group was higher than that in NS group (q1=20.940, P < 0.05; q2=7.311, P < 0.05; q3=4.805, P < 0.05; q4=5.976, P < 0.05; q5=5.096, P < 0.05; q6=10.390,P < 0.05). The expression of RIPK1, RIPK3, and DRP1 genes in HPM2.5 group was significantly higher than that in NS group (q1=7.952, P < 0.05; q2=5.172, P < 0.05; q3=5.430, P < 0.05).

Conclusion

Traffic-related PM2.5 can induce cardiac necrotic apoptosis in asthmatic mice through RIPK1/MLKL/PGAM5 pathway.

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目的

探讨RIPK1/MLKL/PGAM5通路在交通相关PM2.5诱导哮喘小鼠心脏损伤中的作用。

方法

BALB/c雄性小鼠50只，随机分为对照组（NS组）、哮喘组（OVA组）、OVA+低浓度PM2.5组［LPM2.5, 1.8 mg/（kg·bw）］、OVA+中浓度PM2.5组［MPM2.5, 3.6 mg/（kg·bw）］、OVA+高浓度PM2.5组［HPM2.5, 7.2 mg/（kg·bw）］。建立OVA哮喘模型小鼠，经鼻腔滴注不同浓度的PM2.5混悬液10次。HE染色观察心脏组织病理学改变，Tunel染色法检测心脏组织细胞凋亡，qRT-PCR和Western blot法检测小鼠心脏组织中RIPK1、RIPK3、MLKL、PGAM5、DRP1的蛋白及mRNA表达水平。

结果

与NS组相比，PM2.5染毒组的小鼠心脏组织中心肌纤维排列明显无序，且HPM2.5组心肌纤维明显断裂，凋亡细胞数量明显增加，HPM2.5组RIPK1、RIPK3、MLKL、PGAM5、DRP1、p-DRP1蛋白表达均高于NS组(q1=20.940, P<0.05; q2=7.311, P<0.05; q3=4.805, P<0.05; q4=5.976, P<0.05; q5=5.096, P<0.05; q6=10.390, P<0.05)。与NS组相比，HPM2.5组RIPK1、RIPK3、DRP1基因表达显著升高（q1=7.952, P<0.05; q2=5.172, P<0.05; q3=5.430, P<0.05）。

结论

交通相关PM2.5可通过RIPK1/MLKL/PGAM5通路诱导哮喘小鼠心脏发生坏死性凋亡。

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张志红，E-mail:
, copyrightStatement=本刊刊出的所有文章不代表中华预防医学会和本刊编委会的观点，除非特别声明。, copyrightOwner=中华预防医学会和四川大学华西公共卫生学院, extLink=null, articleAbsUrl=null, sourceXml=DsezwOtwwWel0Ilf+B2RQA==, magXml=OAD65pfRMULOv3210jSTjg==, pdfUrl=null, pdf=0NBbBC6gRY2ICl/EGCwnJA==, pdfFileSize=1188143, pdfExtLink=null, richHtmlUrl=null, mobilePdfUrl=null, reviewReport=null, pdfFirstPage=null, abstractGraph=7ADOvvWuuZcCD5UkzsvjJg==, abstractGraphContent=null, abstractVideo=null, citation=null, cebUrl=null, magXmlContent=DdR66ABBSbdS2x/LKoiNHA==, mapNumber=null, authorCompany=null, fund=null, authors=

牛泽宇（1995—），男，硕士在读，研究方向：大气污染的心脏毒性

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2.山西医科大学黄河流域生态公共卫生安全研究中心，山西 太原 030001
3.煤炭环境致病与防治教育部重点实验室，山西 太原 030001, bio={"content":"

牛泽宇（1995—），男，硕士在读，研究方向：大气污染的心脏毒性

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牛泽宇（1995—），男，硕士在读，研究方向：大气污染的心脏毒性

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2.山西医科大学黄河流域生态公共卫生安全研究中心，山西 太原 030001
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2.山西医科大学黄河流域生态公共卫生安全研究中心，山西 太原 030001
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2.山西医科大学黄河流域生态公共卫生安全研究中心，山西 太原 030001
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2.山西医科大学黄河流域生态公共卫生安全研究中心，山西 太原 030001
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注：图A（HE染色，×200）；图B（HE染色，×400）；图C（TUNEL染色，×200）。

, figureFileSmall=OtIwCqanadzLo+xeh4cHNQ==, figureFileBig=Tau6vt4Q0nfT/XgRyFjyQg==, tableContent=null), ArticleFig(id=1240986273528214489, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972423080759614, language=EN, label=Figure 3, caption=Relative expression levels of RIPK1/MLKL/PGAM5 pathway proteins and mRNA in cardiac tissue, figureFileSmall=gRhNzsYb6KN2GbNpPyrQig==, figureFileBig=N9kOxHut+2ksCy679+TjRg==, tableContent=null), ArticleFig(id=1240986273704375260, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972423080759614, language=CN, label=图3, caption=心脏组织中RIPK1/MLKL/PGAM5通路蛋白和mRNA的相对表达量

注：图A为灰度分析定量结果；图B为mRNA表达结果；图C为WB结果；*P<0.05

, figureFileSmall=gRhNzsYb6KN2GbNpPyrQig==, figureFileBig=N9kOxHut+2ksCy679+TjRg==, tableContent=null), ArticleFig(id=1240986273893118941, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972423080759614, language=EN, label=Figure 4, caption=Expression levels of DRP1 protein and mRNA, figureFileSmall=gG79IZ9NVnGTEIEAzxAM1A==, figureFileBig=Zm2M+/Yjci+PWgB51A8/zA==, tableContent=null), ArticleFig(id=1240986273972810722, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972423080759614, language=CN, label=图4, caption=DRP1蛋白和mRNA表达水平

注：图A为灰度分析定量结果；图B为mRNA表达结果；图C为WB结果；*P<0.05。

, figureFileSmall=gG79IZ9NVnGTEIEAzxAM1A==, figureFileBig=Zm2M+/Yjci+PWgB51A8/zA==, tableContent=null), ArticleFig(id=1240986274044113894, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972423080759614, language=EN, label=Table 1, caption=

The primer sequences for each gene

, figureFileSmall=null, figureFileBig=null, tableContent=
基因引物序列（5′-3′）
RIPK1（forward）GAAGACAGACCTAGACAGCGG
RIPK1（reverse）CCAGTAGCTTCACCACTCGAC
RIPK3（forward）CAGTGGGACTTCGTGTCCG
RIPK3（reverse）CAAGCTGTGTAGGTAGCACATC
MLKL（forward）GGATTGCCCTGAGTTGTTGC
MLKL（reverse）AACCGCAGACAGTCTCTCCA
PGAM（forward）ATCTGGAGAAGACGAGTTGACA
PGAM5（reverse）CCTGTTCCCGACCTAATGGT
DRP1（forward）GGACCCACTAGGTGGCCTTA
DRP1（reverse）ACGCTTAATCTGACGTTTGACC
β-actin小鼠 ACTB 内参引物（生工生物B661302）
), ArticleFig(id=1240986274216080363, tenantId=1146029695717560320, journalId=1227665162245664772, articleId=1240972423080759614, language=CN, label=表1, caption=

各基因引物序列

, figureFileSmall=null, figureFileBig=null, tableContent=
基因引物序列（5′-3′）
RIPK1（forward）GAAGACAGACCTAGACAGCGG
RIPK1（reverse）CCAGTAGCTTCACCACTCGAC
RIPK3（forward）CAGTGGGACTTCGTGTCCG
RIPK3（reverse）CAAGCTGTGTAGGTAGCACATC
MLKL（forward）GGATTGCCCTGAGTTGTTGC
MLKL（reverse）AACCGCAGACAGTCTCTCCA
PGAM（forward）ATCTGGAGAAGACGAGTTGACA
PGAM5（reverse）CCTGTTCCCGACCTAATGGT
DRP1（forward）GGACCCACTAGGTGGCCTTA
DRP1（reverse）ACGCTTAATCTGACGTTTGACC
β-actin小鼠 ACTB 内参引物（生工生物B661302）
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RIPK1/MLKL/PGAM5通路在交通相关PM2.5诱导哮喘小鼠心脏损伤中的作用
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牛泽宇 1, 2, 3 , 王彩红 1, 2, 3 , 张妍 1, 2, 3 , 田家瑜 1, 2, 3 , 刘楠楠 1, 2, 3 , 宋露露 1, 2, 3 , 赵利芳 1, 2, 3 , 张志红 1, 2, 3
现代预防医学 | 实验技术及其应用 2024,51(9): 1695-1701
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现代预防医学 | 实验技术及其应用 2024, 51(9): 1695-1701
RIPK1/MLKL/PGAM5通路在交通相关PM2.5诱导哮喘小鼠心脏损伤中的作用
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牛泽宇1, 2, 3, 王彩红1, 2, 3, 张妍1, 2, 3, 田家瑜1, 2, 3, 刘楠楠1, 2, 3, 宋露露1, 2, 3, 赵利芳1, 2, 3, 张志红1, 2, 3
作者信息
  • 1.山西医科大学公共卫生学院环境卫生学教研室，山西 太原 030001
  • 2.山西医科大学黄河流域生态公共卫生安全研究中心，山西 太原 030001
  • 3.煤炭环境致病与防治教育部重点实验室，山西 太原 030001

    • 牛泽宇（1995—），男，硕士在读，研究方向：大气污染的心脏毒性

通讯作者:

张志红，E-mail:
The role of RIPK1/MLKL/PGAM5 pathway in traffic-related PM2.5-induced heart injury in asthmatic mice
Ze-yu NIU1, 2, 3, Cai-hong WANG1, 2, 3, Yan ZHANG1, 2, 3, Jia-yu TIAN1, 2, 3, Nan-nan LIU1, 2, 3, Lu-lu SONG1, 2, 3, Li-fang ZHAO1, 2, 3, Zhi-hong ZHANG1, 2, 3
Affiliations
  • Department of Environmental Health, School of Public Health, Shanxi Medical University, Taiyuan, Shanxi 030001, China
出版时间: 2024-05-10 doi: 10.20043/j.cnki.MPM.202311413
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摘要
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目的

探讨RIPK1/MLKL/PGAM5通路在交通相关PM2.5诱导哮喘小鼠心脏损伤中的作用。

方法

BALB/c雄性小鼠50只，随机分为对照组（NS组）、哮喘组（OVA组）、OVA+低浓度PM2.5组［LPM2.5, 1.8 mg/（kg·bw）］、OVA+中浓度PM2.5组［MPM2.5, 3.6 mg/（kg·bw）］、OVA+高浓度PM2.5组［HPM2.5, 7.2 mg/（kg·bw）］。建立OVA哮喘模型小鼠，经鼻腔滴注不同浓度的PM2.5混悬液10次。HE染色观察心脏组织病理学改变，Tunel染色法检测心脏组织细胞凋亡，qRT-PCR和Western blot法检测小鼠心脏组织中RIPK1、RIPK3、MLKL、PGAM5、DRP1的蛋白及mRNA表达水平。

结果

与NS组相比，PM2.5染毒组的小鼠心脏组织中心肌纤维排列明显无序，且HPM2.5组心肌纤维明显断裂，凋亡细胞数量明显增加，HPM2.5组RIPK1、RIPK3、MLKL、PGAM5、DRP1、p-DRP1蛋白表达均高于NS组(q1=20.940, P<0.05; q2=7.311, P<0.05; q3=4.805, P<0.05; q4=5.976, P<0.05; q5=5.096, P<0.05; q6=10.390, P<0.05)。与NS组相比，HPM2.5组RIPK1、RIPK3、DRP1基因表达显著升高（q1=7.952, P<0.05; q2=5.172, P<0.05; q3=5.430, P<0.05）。

结论

交通相关PM2.5可通过RIPK1/MLKL/PGAM5通路诱导哮喘小鼠心脏发生坏死性凋亡。

交通相关PM2.5  /  坏死性凋亡  /  哮喘  /  心脏损伤
Objective

To investigate the role of RIPK1/MLKL/PGAM5 pathway in traffic-related PM2.5-induced heart injury in asthmatic mice.

Methods

In total 50 male BALB/c mice were randomly divided into control group (NS group), asthma group (OVA group), OVA+ low concentration PM2.5 group (LPM2.5, 1.8 mg/ kg ·bw), OVA+ medium concentration PM2.5 group (MPM2.5,3.6 mg/ kg ·bw), and OVA+ high concentration PM2.5 group (HPM2.5, 7.2 mg/ kg ·bw). OVA asthma model mice were instilled with different concentrations of PM2.5 suspension through nasal cavity for 10 times. The pathological changes of heart tissue were observed by HE staining, the apoptosis of heart tissue was detected by Tunnel staining, and the protein and mRNA expression levels of RIPK1, RIPK3, MLKL, PGAM5, DRP1, and mRNA in mouse heart tissue were detected by qRT-PCR and Western blot methods.

Results

Compared with NS group, the arrangement of central muscle fibers in PM2.5 group was obviously disordered, the myocardial fibers in HPM2.5 group were obviously broken, and the number of apoptotic cells was significantly increased. The protein expression of RIPK1, RIPK3, MLKL, PGAM5, DRP1, and p-DRP1 in HPM2.5 group was higher than that in NS group (q1=20.940, P < 0.05; q2=7.311, P < 0.05; q3=4.805, P < 0.05; q4=5.976, P < 0.05; q5=5.096, P < 0.05; q6=10.390,P < 0.05). The expression of RIPK1, RIPK3, and DRP1 genes in HPM2.5 group was significantly higher than that in NS group (q1=7.952, P < 0.05; q2=5.172, P < 0.05; q3=5.430, P < 0.05).

Conclusion

Traffic-related PM2.5 can induce cardiac necrotic apoptosis in asthmatic mice through RIPK1/MLKL/PGAM5 pathway.

Traffic-related PM2.5  /  Necrotic apoptosis  /  Asthma  /  Heart injury
牛泽宇, 王彩红, 张妍, 田家瑜, 刘楠楠, 宋露露, 赵利芳, 张志红. RIPK1/MLKL/PGAM5通路在交通相关PM2.5诱导哮喘小鼠心脏损伤中的作用. 现代预防医学, 2024 , 51 (9) : 1695 -1701 . DOI: 10.20043/j.cnki.MPM.202311413
Ze-yu NIU, Cai-hong WANG, Yan ZHANG, Jia-yu TIAN, Nan-nan LIU, Lu-lu SONG, Li-fang ZHAO, Zhi-hong ZHANG. The role of RIPK1/MLKL/PGAM5 pathway in traffic-related PM2.5-induced heart injury in asthmatic mice[J]. Modern Preventive Medicine, 2024 , 51 (9) : 1695 -1701 . DOI: 10.20043/j.cnki.MPM.202311413
正文
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《2022年全球空气质量报告》指出，空气污染导致每年超过600万人死亡，暴露于空气污染会导致并加重哮喘、肺部疾病和心脏病等，且明确指出PM2.5可导致心血管疾病的发生。在六种主要空气污染物中，细颗粒物（fine particle matter, PM2.5）是对人类最有害的污染物[1]。随着社会的发展，汽车成了重要的交通工具，低空PM2.5的来源逐渐由煤烟型转变为汽车尾气，对人类健康造成了极大危害[2]。流行病学研究发现，人类暴露于与交通有关的空气污染与不良心血管疾病和呼吸系统疾病有关[3]。前期研究发现PM2.5可诱导哮喘大鼠发生内质网应激和自噬，进而导致心脏损伤[4]。
哮喘是一种常见的慢性炎症性气道疾病，可导致肺组织结构重塑和功能障碍[5]。流行病学研究表明，PM2.5暴露与哮喘发作风险增加有关[6]。哮喘可导致肺通气和肺换气功能障碍，造成机体缺氧，进而引起心肌细胞损伤。此外，哮喘个体与非哮喘个体相比，动脉粥样硬化的患病率增加[7]。因此，哮喘人群更易发生心脏损伤。但是PM2.5对哮喘患者的心脏毒性机制尚不清楚。
坏死性凋亡是由丝氨酸/苏氨酸激酶受体相互作用蛋白激酶1（RIPK1）介导，通过激活受体相互作用蛋白激酶3（RIPK3）以及混合谱系激酶结构域样（MLKL）等坏死性凋亡相关因子的一种细胞程序性死亡[8]。在心脏缺血灌注损伤和对小鼠缺血性心力衰竭的研究中均发现有细胞坏死性凋亡的参与[9-10]。线粒体是高度动态的细胞器，它们通过连续融合和裂变以维持适当的线粒体数量。GTP酶动力蛋白相关蛋白1（GTPase dynamin-related protein 1, DRP1）是线粒体裂变的重要调节因子[11]。当DRP1表达过多时，功能性线粒体的数量随着线粒体碎裂的积累减少，进而导致细胞发生坏死性凋亡。磷酸甘油酸变位酶5（phosphoglycerate mutase 5, PGAM5）是一种线粒体外膜的丝氨酸/苏氨酸磷酸酶[12]，有研究显发现其可充当RIPK1/RIPK3/MLKL复合物的靶标，调节DRP1表达。在大鼠缺血再灌注模型和细胞实验中，发现抑制PGAM5可以降低DRP1和p-DRP1（ser616）表达，改善线粒体功能，减少缺血再灌注引起的心肌损伤[13]。但是交通相关PM2.5通过RIPK1/MLKL/PGAM5通路诱导哮喘小鼠心脏损伤尚无文献报道。
故本研究我们构建了哮喘小鼠模型，探讨交通相关PM2.5对哮喘小鼠的心脏毒性及其可能的作用机制。
1　材料与方法
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1.1　PM2.5的采集与处理
采样地点为在山西省太原市某大型交通路口，采样时间为2020年11月— 2021年1月，每天8:00—20:00。在距离地面1.6 m高度使用武汉天虹大流量采样器以1 m3 /min流量采样，采样后的玻璃纤维滤膜放入干燥器中平衡24 h。将含有PM2.5的滤膜裁剪成1 cm2的小块浸入去离子水中，超声震荡3次，每次30 min，收集三次的浸出液，倒入不锈钢平皿中，用锡箔纸封口并扎孔。-80℃冰箱冷冻48 h，然后置于冷冻干燥器中冷冻干燥，收集的絮状物即为PM2.5颗粒物，保存于-20℃备用。且课题组前期使用电感耦合等离子体-质谱法（ICP-MS）和离子色谱法（IC）对2018年采集的交通相关PM2.5中金属成分及水溶性离子成分进行了测定[14]。
1.2　实验动物以及模型构建
50只雄性BALB/c小鼠（6～8周龄，体重20～25 g）购自北京维通利华实验动物技术有限公司，动物许可证号［SCXK（京）2021-0006）］，动物实验经山西省肿瘤医院动物实验伦理审查委员会批准（2022026）。适应性喂养一周。小鼠随机分为5组，每组10只：对照组（NS组）、哮喘组（OVA组）、OVA +低剂量PM2.5染毒组［LPM2.5, 1.8 mg/（kg·bw）］、OVA +中剂量PM2.5染毒组［MPM2.5, 3.6 mg/（kg·bw）］、OVA +高剂量PM2.5染毒组［HPM2.5, 7.2 mg/（kg·bw）］。于实验的第1、8和15 d对小鼠进行致敏。NS组腹腔注射无菌PBS，其他组腹腔注射含OVA和Al(OH)3的PBS混悬液。从第21 d开始对小鼠进行OVA雾化激发。NS组用无菌PBS雾化，其他各组用2%OVA雾化激发，隔一天雾化激发一次，每次持续30 min，共激发10次。从第20 d开始，小鼠经异氟烷麻醉后，经鼻腔滴注PM2.5染毒液，隔一天一次，共10次。NS组和OVA组鼻腔滴注20 μl空白染毒液，其他组鼻腔滴注20 μl不同浓度的PM2.5染毒液。于第40 d摘眼球取血后，断颈处死小鼠，取材。图1为PM2.5加重小鼠哮喘模型诱导示意图。
1.3　试剂与抗体
OVA、Al(OH)3（美国Sigma公司）；PGAM5、p-DRP1、β-actin（美国SAB公司），RIPK1、RIPK3、MLKL、DRP1（武汉Proteintech公司）；山羊抗鼠二抗、山羊抗兔二抗、蛋白酶抑制剂、BCA蛋白定量试剂盒（武汉博士德生物工程有限公司）；反转录试剂盒、cDNA扩增试剂盒（日本TaKaRa公司）；mRNA引物合成、SDS- PAGE凝胶制备试剂盒（上海生工）；Tunel试剂盒（武汉赛维尔生物科技有限公司）。
1.4　病理学评估
采用4%多聚甲醛对BALB/c小鼠肺组织和心脏组织进行固定，并用石蜡包埋切片，经二甲苯脱蜡，梯度乙醇（100%、90%、80%、70%）分馏后再后水化。清洗切片后按照试剂盒的说明，进行HE染色和Tunel染色。在光学显微镜下观察小鼠肺组织和心脏组织的病理学改变。荧光显微镜心脏观察心脏组织细胞凋亡。
1.5　Western Blot检测心脏组织中蛋白表达水平
20 mg心脏组织在200 μl裂解液（蛋白酶抑制剂：磷酸酶抑制剂：RIPA Buffer=1∶1∶100）中使用超声破碎仪均质，然后在4°C离心机以13 400×g离心15 min，收集上清液。BCA蛋白检测试剂盒测定上清液中总蛋白的浓度。使用SDS-PAGE凝胶分离蛋白质，PVDF膜进行转膜，5%脱脂奶粉将PVDF膜室温封闭2 h。然后，将膜置于目标蛋白一抗稀释液中（RIPK1,1∶1 000；RIPK3, 1∶1 000；MLKL, 1∶1 000；PGAM5, 1∶1 000；DRP1, 1∶1 000；p-DRP1 (ser616), 1∶1 000；β-actin, 1∶4 000），4℃摇床孵育过夜，用TBST冲洗（3×10 min），然后加入二抗室温孵育40 min，用TBST冲洗（3×10 min）。最后，滴加ECL发光液观察免疫反应条带，Image-J进行蛋白定量分析。
1.6　qRT-PCR检测心脏组织中基因表达水平
使用RNAiso Plus从心脏组织中提取总RNA。用PrimeScriptTM RT试剂盒将1 μg总RNA逆转录成cDNA。然后在25 μl PCR反应系统中扩增20 ng cDNA。扩增条件：95°C 30 s，95°C 5 s，60°C 30 s，40个循环。β-actin归一化后，用2-ΔΔCt法测定靶基因的相对表达值。各基因引物序列见表1。
1.7　统计分析
采用SPSS 22.0软件对实验数据进行统计分析。使用Graphpad Prism 8.2处理分析结果并生成图表。采用单因素方差分析（one-way ANOVA）进行多组间数据比较，采用Tukey检验进行多重比较，检验水准α=0.05。
2　结果
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2.1　交通相关PM2.5对哮喘小鼠心脏组织的毒性作用
如图2A和B所示，NS组心肌纤维完整，排列有序，OVA组轻度紊乱，随着PM2.5染毒浓度增加，心肌纤维明显无序，心肌细胞间隙变大，且在HPM2.5组心肌纤维出现断裂，炎性细胞浸润。图2C所示，NS组凋亡细胞较少，OVA组凋亡细胞数轻微增加，随着PM2.5染毒浓度增加，凋亡细胞数量逐渐增加，说明PM2.5可导致心脏组织发生细胞凋亡，造成心脏损伤。
2.2　交通相关PM2.5对RIPK1/MLKL/PGAM5通路蛋白和mRNA表达水平的影响
如图3A和C所示，OVA组中RIPK1、RIPK3、MLKL、PGAM5蛋白表达量均高于NS组，随着PM2.5染毒浓度增加呈逐渐升高，在HPM2.5组表达量最高。HPM2.5组中坏死性凋亡相关蛋白RIPK1、RIPK3、MLKL表达量均明显高于NS组（q1=20.940, P<0.05; q2=7.311, P<0.05; q3=4.805，P<0.05）；与OVA组相比，HPM2.5组中RIPK1、RIPK3蛋白表达均显著升高（q1=19.570, P<0.05; q2=5.055, P<0.05），MLKL表达轻微升高（q=4.503, P>0.05）。HPM2.5组中PGAM5蛋白表达量最高，与NS组比较差异具有统计学意义（q=5.976, P<0.05）；与OVA相比，PGAM5轻微升高（q=3.691, P>0.05）。
如图3B所示，RIPK1/MLKL/PGAM5通路mRNA表达与蛋白表达水平一致，RIPK1、RIPK3、MLKL、PGAM5的mRNA表达水平随着PM2.5染毒浓度增加逐渐增加，与NS组相比，HPM2.5组中RIPK1、RIPK3表达明显升高（q1=7.952, P<0.05; q2=5.172, P<0.05）；而MLKL、PGAM5轻微升高，差异未见统计学意义（q1=1.765, P>0.05; q2=1.572, P>0.05）。
2.3　PM2.5对DRP1蛋白和mRNA表达水平的影响
如图4A和C所示，OVA组中DRP1及p-DRP1蛋白表达水平均高于NS组，在PM2.5染毒后，表达量进一步升高，在HPM2.5组表达量最高。与OVA组相比，HPM2.5组中p-DRP1(ser616)蛋白表达显著升高（q=9.667, P<0.05）。与NS组相比DRP1及p-DRP1蛋白表达水平均明显升高（q1=5.096, P<0.05; q2=10.390, P<0.05）；DRP1的mRNA表达水平呈上升趋势，在HPM2.5组中表达最高，且明显高于NS组（q=5.430, P<0.05）。
3　讨论
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越来越多的流行病学证据表明，PM2.5与哮喘的发生和加重息息相关[15]，PM2.5粒径小，且可通过呼吸道进入肺组织引发炎症、氧化应激等引起肺组织损伤[16]。随着PM2.5来源的变化，交通相关PM2.5对人健康影响日益加大，因此课题组前期Wu等人[14]对交通来源PM2.5全颗粒进行了成分分析，且进一步研究发现交通相关PM2.5可通过TGF-β1/SMAD3信号通路诱导哮喘大鼠气道纤维化。课题组Wang等[17]通过肺组织HE染色以及测定小鼠血浆OVA特异性IgE证明哮喘模型构建成功，并发现交通相关PM2.5可通过外泌体miR-129-2-3p加重哮喘。Wang等人[18]发现PM2.5诱发肺功能损伤时通过细胞外囊泡（sEV）继发心功能不全，也可通过气血交换，造成心血管系统的损伤。流行病学研究发现PM2.5与心血管疾病发生的风险相关[19]，课题组前期研究发现PM2.5通过自噬和内质网应激引起哮喘大鼠心脏损伤[4]。但是疾病的发生往往是多途径的，从不同的通路进行探讨疾病的发生机制，更有利于疾病的预防与治疗。本研究发现PM2.5可以通过RIPK1/MLKL/PGAM5通路介导线粒体裂变进而引起哮喘小鼠心脏损伤。
心脏是心血管系统的主要参与者，心脏组织结构与功能的改变与心血管疾病的发生紧密相关。心脏组织器质性改变与心血管疾病发生紧密相关。Wu等人[20]研究发展PM2.5暴露可导致小鼠心肌纤维紊乱、心肌间质水肿、毛细血管扩张和炎性细胞浸润。在本研究中，HE染色发现OVA组与NS相比，心肌纤维轻度紊乱，随着PM2.5染毒增加，心肌纤维间隙变大，且在HPM2.5组出现心肌纤维断裂，炎性细胞浸润。Tunel染色发现，随着PM2.5染毒浓度增加，凋亡细胞数量明显增多，与心脏病理损伤表现一致。提示PM2.5是心脏损伤的危险因子。
坏死性凋亡是由TNF(肿瘤坏死因子)超家族、TLR(Toll样受体)或干扰素受体中的死亡受体激活引发的一种程序性细胞死亡形式，RIPK1、RIPK3、MLKL是坏死性凋亡信号通路的关键分子。表现为质膜破裂、半透明细胞质、线粒体肿胀和核膜保存等形态特征[21]。当受到刺激时，RIPK1与RIPK3相互作用募集下游蛋白MLKL形成坏死小体，细胞发生坏死性凋亡。在临床研究中发现坏死性凋亡抑制剂增加心脏对缺血/再灌注（I/R）的耐受性并降低心肌梗死患者的死亡率[22]。但是PM2.5与哮喘小鼠心脏坏死性凋亡间的联系未见报道。本研究结果表明，与NS组和OVA组相比，PM2.5暴露增加了坏死性凋亡相关分子RIPK1、RIPK3、MLKL基因和蛋白的表达，且在HPM2.5组最显著。说明PM2.5可引起哮喘小鼠心脏发生坏死性凋亡。但是坏死小体是坏死性凋亡的启动者，并非执行者。坏死小体诱导心脏组织执行坏死性凋亡途径尚不清楚。
心脏是一种对能量变化非常敏感的器官，当机体内氧气供应不足，线粒体产生的能量不足以支持心脏对于能量的需求时，即可造成心脏的损伤。哮喘可引起气流受限，导致机体缺氧，而线粒体是机体氧化磷酸化的重要场所，氧含量不足，导致线粒体损伤，线粒体通过融合与裂变来维持线粒体稳态，通过线粒体自噬来清除衰老损伤的线粒体[23]。而线粒体裂变主要受DRP1的调控，当DRP1和p-DRP1(ser616)表达增加，线粒体发生损伤，PGAM5是一种位于线粒体外模的线粒体蛋白，PGAM5可作为坏死性凋亡下游蛋白参与坏死性凋亡的发生，在急性肝损伤研究中发现PGAM5- DRP1轴可诱导肝细胞发生坏死性凋亡[24]。本研究发现随着PM2.5暴露浓度增加，PGAM5、DRP1、p-DRP1(ser616)蛋白表达增加，与之前研究结果一致。
综上所述，本研究表明交通相关PM2.5可通过RIPK1/MLKL/PGAM5通路诱导哮喘小鼠心脏损伤。但是本文仍存在一些不足，一是只对通路进行了验证，并未添加干预措施；二是此实验仅限于体内实验，仍需体外实验进行进一步验证。
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  • 国家自然科学基金(82273595)
  • 中央引导地方科技发展资金(YDZJSX2021A028)
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2024年第51卷第9期
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doi: 10.20043/j.cnki.MPM.202311413
  • 接收时间：2023-11-22
  • 首发时间：2026-03-18
  • 出版时间：2024-05-10
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  • 收稿日期：2023-11-22
基金
国家自然科学基金(82273595)
中央引导地方科技发展资金(YDZJSX2021A028)
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    1.山西医科大学公共卫生学院环境卫生学教研室，山西 太原 030001
    2.山西医科大学黄河流域生态公共卫生安全研究中心，山西 太原 030001
    3.煤炭环境致病与防治教育部重点实验室，山西 太原 030001

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鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
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