Liu-Gen Cui , Shu-Hui Wang , Sumra Komal , Jian-Jian Yin , Miao-Miao Zhai , Yue-Jiao Zhou , Qing-Wen Yu , Cong Wang , Pei Wang , Zhi-Mo Wang , Aliza Muhammad Zafar , Muhammad Shakeel , Li-Rong Zhang , Sheng-Na Han
{"title":"ALKBH5通过Notch1/NLRP3途径促进心肌梗死后心肌成纤维细胞焦亡。","authors":"Liu-Gen Cui , Shu-Hui Wang , Sumra Komal , Jian-Jian Yin , Miao-Miao Zhai , Yue-Jiao Zhou , Qing-Wen Yu , Cong Wang , Pei Wang , Zhi-Mo Wang , Aliza Muhammad Zafar , Muhammad Shakeel , Li-Rong Zhang , Sheng-Na Han","doi":"10.1016/j.cellsig.2024.111574","DOIUrl":null,"url":null,"abstract":"<div><div>Through bioinformatics screening, we previously found that AlkB homolog 5 (ALKBH5) expression, an m<sup>6</sup>A demethylase, was higher in patients with heart failure than in the normal population. This study aimed to investigate the molecular mechanisms by which ALKBH5 regulates heart failure. We established a myocardial infarction (MI)-induced heart failure model in rats in vivo and an in vitro hypoxia model using rat primary cardiac fibroblasts (RCFs). M<sup>6</sup>A sequencing, RNA immunoprecipitation assay, RNA pull-down assay, proximity ligation assay, gain-of-function and loss-of-function experiments, and transcriptomic analysis were performed to confirm the pyroptosis-promoting effects of ALKBH5. The effects of two small-molecule inhibitors (ZINC78774792 and ZINC00546946) on ALKBH5 expression were examined. The expression of m<sup>6</sup>A demethyltransferase ALKBH5 was significantly elevated in hypoxia-induced RCFs. Transcriptional profiling revealed Notch receptor 1 (Notch1) as an m<sup>6</sup>A modification target of ALKBH5, and Notch1 mRNA m<sup>6</sup>A modifications were increased in ALKBH5-deficient RCFs. Moreover, Notch1 and NOD-, LRR-, and pyrin domain-containing protein 3 (NLRP3) are associated. ALKBH5 knockdown alleviated hypoxia-induced RCF cell pyroptosis by inhibiting Notch1, NLRP3 inflammasome activation, and pyroptosis-associated protein (N-GSDMD), whereas ALKBH5 overexpression had the opposite effect. Targeting ALKBH5 with two small-molecule inhibitors (ZINC78774792 and ZINC00546946) reduced hypoxia-induced RCF pyroptosis, and ZINC00546946 alleviated cell pyroptosis after myocardial infarction in mice. Our results indicate that ALKBH5 promotes cardiac fibroblast pyroptosis after myocardial infarction through the Notch1/NLRP3 pathway. Therefore, inhibiting ALKBH5 may be a strategy for treating cardiovascular diseases.</div></div>","PeriodicalId":9902,"journal":{"name":"Cellular signalling","volume":"127 ","pages":"Article 111574"},"PeriodicalIF":4.4000,"publicationDate":"2024-12-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"ALKBH5 promotes cardiac fibroblasts pyroptosis after myocardial infarction through Notch1/NLRP3 pathway\",\"authors\":\"Liu-Gen Cui , Shu-Hui Wang , Sumra Komal , Jian-Jian Yin , Miao-Miao Zhai , Yue-Jiao Zhou , Qing-Wen Yu , Cong Wang , Pei Wang , Zhi-Mo Wang , Aliza Muhammad Zafar , Muhammad Shakeel , Li-Rong Zhang , Sheng-Na Han\",\"doi\":\"10.1016/j.cellsig.2024.111574\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<div><div>Through bioinformatics screening, we previously found that AlkB homolog 5 (ALKBH5) expression, an m<sup>6</sup>A demethylase, was higher in patients with heart failure than in the normal population. This study aimed to investigate the molecular mechanisms by which ALKBH5 regulates heart failure. We established a myocardial infarction (MI)-induced heart failure model in rats in vivo and an in vitro hypoxia model using rat primary cardiac fibroblasts (RCFs). M<sup>6</sup>A sequencing, RNA immunoprecipitation assay, RNA pull-down assay, proximity ligation assay, gain-of-function and loss-of-function experiments, and transcriptomic analysis were performed to confirm the pyroptosis-promoting effects of ALKBH5. The effects of two small-molecule inhibitors (ZINC78774792 and ZINC00546946) on ALKBH5 expression were examined. The expression of m<sup>6</sup>A demethyltransferase ALKBH5 was significantly elevated in hypoxia-induced RCFs. Transcriptional profiling revealed Notch receptor 1 (Notch1) as an m<sup>6</sup>A modification target of ALKBH5, and Notch1 mRNA m<sup>6</sup>A modifications were increased in ALKBH5-deficient RCFs. Moreover, Notch1 and NOD-, LRR-, and pyrin domain-containing protein 3 (NLRP3) are associated. ALKBH5 knockdown alleviated hypoxia-induced RCF cell pyroptosis by inhibiting Notch1, NLRP3 inflammasome activation, and pyroptosis-associated protein (N-GSDMD), whereas ALKBH5 overexpression had the opposite effect. Targeting ALKBH5 with two small-molecule inhibitors (ZINC78774792 and ZINC00546946) reduced hypoxia-induced RCF pyroptosis, and ZINC00546946 alleviated cell pyroptosis after myocardial infarction in mice. Our results indicate that ALKBH5 promotes cardiac fibroblast pyroptosis after myocardial infarction through the Notch1/NLRP3 pathway. 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引用次数: 0
摘要
通过生物信息学筛选,我们之前发现AlkB同源物5 (ALKBH5),一种m6A去甲基化酶,在心力衰竭患者中的表达高于正常人群。本研究旨在探讨ALKBH5调控心力衰竭的分子机制。我们利用大鼠原代心脏成纤维细胞(rcf)建立了大鼠心肌梗死(MI)诱导的体内心力衰竭模型和体外缺氧模型。通过M6A测序、RNA免疫沉淀实验、RNA下拉实验、邻近连接实验、功能获得和功能丧失实验以及转录组学分析来证实ALKBH5的促焦作用。研究了两种小分子抑制剂ZINC78774792和ZINC00546946对ALKBH5表达的影响。缺氧诱导的rcf中m6A去甲基转移酶ALKBH5的表达显著升高。转录谱分析显示,Notch受体1 (Notch1)是ALKBH5的m6A修饰靶点,Notch1 mRNA m6A修饰在ALKBH5缺陷rcf中增加。此外,Notch1与NOD-、LRR-和pyrin domain containing protein 3 (NLRP3)相关。ALKBH5敲低可通过抑制Notch1、NLRP3炎性体激活和焦亡相关蛋白(N-GSDMD)减轻缺氧诱导的RCF细胞焦亡,而ALKBH5过表达则具有相反的作用。两种小分子抑制剂(ZINC78774792和ZINC00546946)靶向ALKBH5可降低小鼠缺氧诱导的RCF焦亡,ZINC00546946可减轻小鼠心肌梗死后细胞焦亡。我们的研究结果表明,ALKBH5通过Notch1/NLRP3途径促进心肌梗死后心肌成纤维细胞焦亡。因此,抑制ALKBH5可能是治疗心血管疾病的一种策略。
ALKBH5 promotes cardiac fibroblasts pyroptosis after myocardial infarction through Notch1/NLRP3 pathway
Through bioinformatics screening, we previously found that AlkB homolog 5 (ALKBH5) expression, an m6A demethylase, was higher in patients with heart failure than in the normal population. This study aimed to investigate the molecular mechanisms by which ALKBH5 regulates heart failure. We established a myocardial infarction (MI)-induced heart failure model in rats in vivo and an in vitro hypoxia model using rat primary cardiac fibroblasts (RCFs). M6A sequencing, RNA immunoprecipitation assay, RNA pull-down assay, proximity ligation assay, gain-of-function and loss-of-function experiments, and transcriptomic analysis were performed to confirm the pyroptosis-promoting effects of ALKBH5. The effects of two small-molecule inhibitors (ZINC78774792 and ZINC00546946) on ALKBH5 expression were examined. The expression of m6A demethyltransferase ALKBH5 was significantly elevated in hypoxia-induced RCFs. Transcriptional profiling revealed Notch receptor 1 (Notch1) as an m6A modification target of ALKBH5, and Notch1 mRNA m6A modifications were increased in ALKBH5-deficient RCFs. Moreover, Notch1 and NOD-, LRR-, and pyrin domain-containing protein 3 (NLRP3) are associated. ALKBH5 knockdown alleviated hypoxia-induced RCF cell pyroptosis by inhibiting Notch1, NLRP3 inflammasome activation, and pyroptosis-associated protein (N-GSDMD), whereas ALKBH5 overexpression had the opposite effect. Targeting ALKBH5 with two small-molecule inhibitors (ZINC78774792 and ZINC00546946) reduced hypoxia-induced RCF pyroptosis, and ZINC00546946 alleviated cell pyroptosis after myocardial infarction in mice. Our results indicate that ALKBH5 promotes cardiac fibroblast pyroptosis after myocardial infarction through the Notch1/NLRP3 pathway. Therefore, inhibiting ALKBH5 may be a strategy for treating cardiovascular diseases.
期刊介绍:
Cellular Signalling publishes original research describing fundamental and clinical findings on the mechanisms, actions and structural components of cellular signalling systems in vitro and in vivo.
Cellular Signalling aims at full length research papers defining signalling systems ranging from microorganisms to cells, tissues and higher organisms.