Wang Yong-Wang, Dong Hong-Zhi, Tan Yong-Xing, Bao Xu, Su Ying-Man, Li Xin, Jiang Fang, Liang Jing, Huang Zhen-Cai, Ren Yan-Ling, Xu Yu-Li, Su Qiang
Department of Anesthesiology, Affiliated Hospital of Guilin Medical University, Guilin, 541001, Guangxi, Zhuang Autonomous Region, P. R. China.
Department of Cardiology, Tianjin Chest Hospital, Tianjin, 300222, P. R. China.
Cell Death Discov. 2022 Apr 8;8(1):178. doi: 10.1038/s41420-022-00969-8.
Myocardial infarction (MI) is a fatal heart disease that affects millions of lives worldwide each year. This study investigated the roles of HIF-1α/lncRNA-TUG1 in mitochondrial dysfunction and pyroptosis in MI. CCK-8, DHE, lactate dehydrogenase (LDH) assays, and JC-1 staining were performed to measure proliferation, reactive oxygen species (ROS), LDH leakage, and mitochondrial damage in hypoxia/reoxygenation (H/R)-treated cardiomyocytes. Enzyme-linked immunoassay (ELISA) and flow cytometry were used to detect LDH, creatine kinase (CK), and its isoenzyme (CK-MB) levels and caspase-1 activity. Chromatin immunoprecipitation (ChIP), luciferase assay, and RNA-immunoprecipitation (RIP) were used to assess the interaction between HIF-1α, TUG1, and FUS. Quantitative real-time polymerase chain reaction (qRT-PCR), Western blotting, and immunohistochemistry were used to measure HIF-1α, TUG1 and pyroptosis-related molecules. Hematoxylin and eosin (HE), 2,3,5-triphenyltetrazolium chloride (TTC), and terminal deoxynucleotidyl transferase dUTP risk end labelling (TUNEL) staining were employed to examine the morphology, infarction area, and myocardial injury in the MI mouse model. Mitochondrial dysfunction and pyroptosis were induced in H/R-treated cardiomyocytes, accompanied by an increase in the expression of HIF-α and TUG1. HIF-1α promoted TUG1 expression by directly binding to the TUG1 promoter. TUG1 silencing inhibited H/R-induced ROS production, mitochondrial injury and the expression of the pyroptosis-related proteins NLRP3, caspase-1 and GSDMD. Additionally, H/R elevated FUS levels in cardiomyocytes, which were directly inhibited by TUG1 silencing. Fused in sarcoma (FUS) overexpression reversed the effect of TUG1 silencing on mitochondrial damage and caspase-1 activation. However, the ROS inhibitor N-acetylcysteine (NAC) promoted the protective effect of TUG1 knockdown on H/R-induced cardiomyocyte damage. The in vivo MI model showed increased infarction, myocardial injury, ROS levels and pyroptosis, which were inhibited by TUG1 silencing. HIF-1α targeting upregulated TUG1 promotes mitochondrial damage and cardiomyocyte pyroptosis by combining with FUS, thereby promoting the occurrence of MI. HIF-1α/TUG1/FUS may serve as a potential treatment target for MI.
心肌梗死(MI)是一种致命的心脏病,每年影响着全球数百万人的生命。本研究调查了缺氧诱导因子-1α(HIF-1α)/长链非编码核糖核酸TUG1(lncRNA-TUG1)在心肌梗死中线粒体功能障碍和细胞焦亡中的作用。采用细胞计数试剂盒-8(CCK-8)、二氢乙锭(DHE)、乳酸脱氢酶(LDH)检测及JC-1染色,检测缺氧/复氧(H/R)处理的心肌细胞的增殖、活性氧(ROS)、LDH泄漏及线粒体损伤情况。采用酶联免疫吸附测定(ELISA)和流式细胞术检测LDH、肌酸激酶(CK)及其同工酶(CK-MB)水平和半胱天冬酶-1(caspase-1)活性。采用染色质免疫沉淀(ChIP)、荧光素酶测定及RNA免疫沉淀(RIP)评估HIF-1α、TUG1和融合蛋白(FUS)之间的相互作用。采用定量实时聚合酶链反应(qRT-PCR)、蛋白质免疫印迹法和免疫组织化学法检测HIF-1α、TUG1及细胞焦亡相关分子。采用苏木精-伊红(HE)染色、2,3,5-氯化三苯基四氮唑(TTC)染色及末端脱氧核苷酸转移酶介导的缺口末端标记(TUNEL)染色,观察心肌梗死小鼠模型的形态、梗死面积及心肌损伤情况。H/R处理的心肌细胞出现线粒体功能障碍和细胞焦亡,同时HIF-α和TUG1的表达增加。HIF-1α通过直接结合TUG1启动子促进TUG1表达。TUG1沉默可抑制H/R诱导的ROS产生、线粒体损伤以及细胞焦亡相关蛋白NLRP3、caspase-1和Gasdermin D(GSDMD)的表达。此外,H/R使心肌细胞中FUS水平升高,而TUG1沉默可直接抑制其升高。过表达FUS可逆转TUG1沉默对线粒体损伤和caspase-激活的影响。然而,ROS抑制剂N-乙酰半胱氨酸(NAC)可增强TUG1基因敲低对H/R诱导的心肌细胞损伤的保护作用。体内心肌梗死模型显示,TUG1沉默可抑制梗死面积增加、心肌损伤、ROS水平升高及细胞焦亡。靶向HIF-1α上调TUG1通过与FUS结合促进线粒体损伤和心肌细胞焦亡,从而促进心肌梗死的发生。HIF-1α/TUG1/FUS可能是心肌梗死的潜在治疗靶点。