Article

METTL14-mediated m6A methylation of pri-miR-5099 to facilitate cardiomyocyte pyroptosis in myocardial infarction

Hang Yu1, Qing-sui Li1, Jun-nan Guo2, Zhen Zhang1, Xian-zhi Lang1, Yi-ning Liu1, Long Qin1, Xu Su1, Qing-wei Zhang1, Ya-dong Xue1, Li-ling Gong1, Ning Xu1, Ming Li1, Wen-shuang Zhao1, Xing-miao Zhao1, Wan-yu Zhang1, Yi-jing Yao1, Xi-ming Chen1, Wei Li1, Han-xiang Wang1, Ben-zhi Cai1,3,4, Jia-min Li1,3,4, Ning Wang1,3,4
1 Department of Pharmacy at The Second Affiliated Hospital, and Department of Pharmacology (State Key Laboratory of Frigid Zone Cardiovascular Diseases (SKLFZCD)), College of Pharmacy, Harbin Medical University, Harbin 150081, China
2 Department of Thoracic Surgery, Harbin Medical University Cancer Hospital, Harbin 150040, China
3 Research Unit of Noninfectious Chronic Diseases in Frigid Zone (2019RU070), Chinese Academy of Medical Sciences, Harbin 150081, China
4 Northern Translational Medicine Research and Cooperation Center, Heilongjiang Academy of Medical Sciences, Harbin Medical University, Harbin 150080, China
Correspondence to: Ben-zhi Cai: caibz@ems.hrbmu.edu.cn, Jia-min Li: lijiamin@hrbmu.edu.cn, Ning Wang: wangning@ems.hrbmu.edu.cn,
DOI: 10.1038/s41401-025-01485-y
Received: 30 August 2024
Accepted: 15 January 2025
Advance online: 12 February 2025

Abstract

N6-methyladenosine (m6A) modification is an important mechanism in microRNA processing and maturation. Previous studies show the involvement of pri-miRNA methylation in regulating the occurrence and development of tumor-related diseases. In this study, we investigated the role of its aberrant regulation in cardiac diseases. Myocardial infarction (MI) mouse were established by ligation of the left anterior descending branch of the coronary artery. We showed that the expression of methyltransferase 14 (METTL14) was significantly increased in myocardium of MI mice. We demonstrated that METTL14 methylated the primary transcript miRNA (pri-miR-5099), promoting the recognition by DiGeorge critical region 8 (DGCR8) and the maturation processing of pri-miR-5099. Mature microRNA-5099-3p (miR-5099-3p) inhibited the expression of E74 like ETS transcription factor 1 (ELF1), which transcriptionally regulated pyroptosis factors such as acysteinyl aspartate-specific proteinase 1 (caspase-1) and gasdermin D (GSDMD), ultimately leading to cardiomyocyte pyroptosis. This study reveals that myocardial infarction-induced miR-5099-3p excessive maturation via m6A modification promotes the development and progression of cardiomyocyte pyroptosis.

Keywords: myocardial infarction; m6A modification; METTL14; miRNA-5099-3p; cardiomyocyte pyroptosis; ELF1

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