m6A methyltransferase METTL3 contributes to sympathetic hyperactivity post-MI via promoting TRAF6-dependent mitochondrial ROS production
N6-methyladenosine (m6A) is the most prevalent post-translational modification in eukaryotic mRNA. Recently, m6A editing modified by methyltransferase-like enzyme 3 (METTL3), the core m6A methyltransferase, has been demonstrated to be involved in cardiac sympathetic hyperactivity. This study aimed t...
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Published in | Free radical biology & medicine Vol. 209; no. Pt 2; pp. 342 - 354 |
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Main Authors | , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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Elsevier Inc
20.11.2023
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Abstract | N6-methyladenosine (m6A) is the most prevalent post-translational modification in eukaryotic mRNA. Recently, m6A editing modified by methyltransferase-like enzyme 3 (METTL3), the core m6A methyltransferase, has been demonstrated to be involved in cardiac sympathetic hyperactivity. This study aimed to clarify the effects and underlying mechanisms of METTL3 in the paraventricular nucleus (PVN) in mediating sympathetic activity following myocardial infarction (MI).
We established rat MI models by left anterior descending coronary artery ligation. m6A quantification was performed.The expression of METTL3 and its downstream gene, tumor necrosis factor (TNF) receptor-associated factor 6 (TRAF6), were determined. The functional role of METTL3 in sympathetic hyperactivity and electrical conduction stability were verified by assessing renal sympathetic nerve activity (RSNA), norepinephrine (NE) levels, and programmed electrical stimulation. Rescue experiments were also conducted. The mechanism by which m6A is involved in mitochondrial reactive oxygen species (mROS) production, mediated by TRAF6/ECSIT pathway, was explored in lipopolysaccharide (LPS) treated primary microglial cells.
METTL3 was predominantly localized in the microglia and significantly increased within the PVN at 3 days post-MI. Inhibition of METTL3 decreased m6A levels, TRAF6 expression, and mROS production; downregulated sympathoexcitation, indicated by attenuated NE concentration and RSNA; decreased the incidence of ventricular tachycardia or fibrillation; and improved cardiac function. Mechanistically, downregulation of METTL3 prevented TRAF6 translocation to the mitochondria in the microglia and subsequent TRAF6/ECSIT pathway activation, resulting in decreased mROS production.
This study demonstrates that METTL3-mediated m6A modification promotes sympathetic hyperactivity through TRAF6/ECSIT pathway and mitochondrial oxidative stress in the PVN, thereby leading to ventricular arrhythmias post-MI.
The schematic of the hypothesis demonstrating the critical role and mechanism of m6A editing regulated by methyltransferase METTL3 on sympathetic hyperactivity within the PVN post-MI. [Display omitted]
•METTL3-mediated m6A in the PVN was involved in sympathetic hyperactivity by TRAF6/ECSIT pathway and mROS production post-MI.•METTL3 was predominantly located in microglia, regulated m6A levels, increased expression of downstream molecules TRAF6, ECSIT and mitochondrial ROS, improved cardiac function post-MI.•Inhibition of METTL3 partly decreased TRAF6 translocation to the mitochondria, TRAF6/ECSIT pathway activation and oxidative stress in microglia. |
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AbstractList | OBJECTIVESN6-methyladenosine (m6A) is the most prevalent post-translational modification in eukaryotic mRNA. Recently, m6A editing modified by methyltransferase-like enzyme 3 (METTL3), the core m6A methyltransferase, has been demonstrated to be involved in cardiac sympathetic hyperactivity. This study aimed to clarify the effects and underlying mechanisms of METTL3 in the paraventricular nucleus (PVN) in mediating sympathetic activity following myocardial infarction (MI).METHODSWe established rat MI models by left anterior descending coronary artery ligation. m6A quantification was performed.The expression of METTL3 and its downstream gene, tumor necrosis factor (TNF) receptor-associated factor 6 (TRAF6), were determined. The functional role of METTL3 in sympathetic hyperactivity and electrical conduction stability were verified by assessing renal sympathetic nerve activity (RSNA), norepinephrine (NE) levels, and programmed electrical stimulation. Rescue experiments were also conducted. The mechanism by which m6A is involved in mitochondrial reactive oxygen species (mROS) production, mediated by TRAF6/ECSIT pathway, was explored in lipopolysaccharide (LPS) treated primary microglial cells.RESULTSMETTL3 was predominantly localized in the microglia and significantly increased within the PVN at 3 days post-MI. Inhibition of METTL3 decreased m6A levels, TRAF6 expression, and mROS production; downregulated sympathoexcitation, indicated by attenuated NE concentration and RSNA; decreased the incidence of ventricular tachycardia or fibrillation; and improved cardiac function. Mechanistically, downregulation of METTL3 prevented TRAF6 translocation to the mitochondria in the microglia and subsequent TRAF6/ECSIT pathway activation, resulting in decreased mROS production.CONCLUSIONSThis study demonstrates that METTL3-mediated m6A modification promotes sympathetic hyperactivity through TRAF6/ECSIT pathway and mitochondrial oxidative stress in the PVN, thereby leading to ventricular arrhythmias post-MI. N6-methyladenosine (m6A) is the most prevalent post-translational modification in eukaryotic mRNA. Recently, m6A editing modified by methyltransferase-like enzyme 3 (METTL3), the core m6A methyltransferase, has been demonstrated to be involved in cardiac sympathetic hyperactivity. This study aimed to clarify the effects and underlying mechanisms of METTL3 in the paraventricular nucleus (PVN) in mediating sympathetic activity following myocardial infarction (MI). We established rat MI models by left anterior descending coronary artery ligation. m6A quantification was performed.The expression of METTL3 and its downstream gene, tumor necrosis factor (TNF) receptor-associated factor 6 (TRAF6), were determined. The functional role of METTL3 in sympathetic hyperactivity and electrical conduction stability were verified by assessing renal sympathetic nerve activity (RSNA), norepinephrine (NE) levels, and programmed electrical stimulation. Rescue experiments were also conducted. The mechanism by which m6A is involved in mitochondrial reactive oxygen species (mROS) production, mediated by TRAF6/ECSIT pathway, was explored in lipopolysaccharide (LPS) treated primary microglial cells. METTL3 was predominantly localized in the microglia and significantly increased within the PVN at 3 days post-MI. Inhibition of METTL3 decreased m6A levels, TRAF6 expression, and mROS production; downregulated sympathoexcitation, indicated by attenuated NE concentration and RSNA; decreased the incidence of ventricular tachycardia or fibrillation; and improved cardiac function. Mechanistically, downregulation of METTL3 prevented TRAF6 translocation to the mitochondria in the microglia and subsequent TRAF6/ECSIT pathway activation, resulting in decreased mROS production. This study demonstrates that METTL3-mediated m6A modification promotes sympathetic hyperactivity through TRAF6/ECSIT pathway and mitochondrial oxidative stress in the PVN, thereby leading to ventricular arrhythmias post-MI. The schematic of the hypothesis demonstrating the critical role and mechanism of m6A editing regulated by methyltransferase METTL3 on sympathetic hyperactivity within the PVN post-MI. [Display omitted] •METTL3-mediated m6A in the PVN was involved in sympathetic hyperactivity by TRAF6/ECSIT pathway and mROS production post-MI.•METTL3 was predominantly located in microglia, regulated m6A levels, increased expression of downstream molecules TRAF6, ECSIT and mitochondrial ROS, improved cardiac function post-MI.•Inhibition of METTL3 partly decreased TRAF6 translocation to the mitochondria, TRAF6/ECSIT pathway activation and oxidative stress in microglia. N6-methyladenosine (m6A) is the most prevalent post-translational modification in eukaryotic mRNA. Recently, m6A editing modified by methyltransferase-like enzyme 3 (METTL3), the core m6A methyltransferase, has been demonstrated to be involved in cardiac sympathetic hyperactivity. This study aimed to clarify the effects and underlying mechanisms of METTL3 in the paraventricular nucleus (PVN) in mediating sympathetic activity following myocardial infarction (MI). We established rat MI models by left anterior descending coronary artery ligation. m6A quantification was performed.The expression of METTL3 and its downstream gene, tumor necrosis factor (TNF) receptor-associated factor 6 (TRAF6), were determined. The functional role of METTL3 in sympathetic hyperactivity and electrical conduction stability were verified by assessing renal sympathetic nerve activity (RSNA), norepinephrine (NE) levels, and programmed electrical stimulation. Rescue experiments were also conducted. The mechanism by which m6A is involved in mitochondrial reactive oxygen species (mROS) production, mediated by TRAF6/ECSIT pathway, was explored in lipopolysaccharide (LPS) treated primary microglial cells. METTL3 was predominantly localized in the microglia and significantly increased within the PVN at 3 days post-MI. Inhibition of METTL3 decreased m6A levels, TRAF6 expression, and mROS production; downregulated sympathoexcitation, indicated by attenuated NE concentration and RSNA; decreased the incidence of ventricular tachycardia or fibrillation; and improved cardiac function. Mechanistically, downregulation of METTL3 prevented TRAF6 translocation to the mitochondria in the microglia and subsequent TRAF6/ECSIT pathway activation, resulting in decreased mROS production. This study demonstrates that METTL3-mediated m6A modification promotes sympathetic hyperactivity through TRAF6/ECSIT pathway and mitochondrial oxidative stress in the PVN, thereby leading to ventricular arrhythmias post-MI. |
Author | Hu, Hesheng Xue, Mei Li, Xiaolu Wang, Yu Shi, Yugen Jing, Yanyan Yang, Peijin Tan, Jiayu Yin, Jie Li, Xinran Wang, Ye Yan, Suhua Li, Yan Ge, Weili |
Author_xml | – sequence: 1 givenname: Peijin surname: Yang fullname: Yang, Peijin organization: Department of Cardiology, The First Affiliated Hospital of Shandong First Medical University & Shandong Provincial Qianfoshan Hospital, Shandong Medicine and Health Key Laboratory of Cardiac Electrophysiology and Arrhythmia, Jinan, China – sequence: 2 givenname: Yu surname: Wang fullname: Wang, Yu organization: Department of Cardiology, The First Affiliated Hospital of Shandong First Medical University & Shandong Provincial Qianfoshan Hospital, Shandong Medicine and Health Key Laboratory of Cardiac Electrophysiology and Arrhythmia, Jinan, China – sequence: 3 givenname: Weili surname: Ge fullname: Ge, Weili organization: Department of Cardiology, Taizhou Hospital of Zhejiang Province Affiliated to Wenzhou Medical University, Zhejiang, China – sequence: 4 givenname: Yanyan surname: Jing fullname: Jing, Yanyan organization: Department of Cardiology, Yantai Yuhuangding Hospital, Yantai, China – sequence: 5 givenname: Hesheng surname: Hu fullname: Hu, Hesheng organization: Department of Cardiology, The First Affiliated Hospital of Shandong First Medical University & Shandong Provincial Qianfoshan Hospital, Shandong Medicine and Health Key Laboratory of Cardiac Electrophysiology and Arrhythmia, Jinan, China – sequence: 6 givenname: Jie surname: Yin fullname: Yin, Jie organization: Department of Cardiology, The First Affiliated Hospital of Shandong First Medical University & Shandong Provincial Qianfoshan Hospital, Shandong Medicine and Health Key Laboratory of Cardiac Electrophysiology and Arrhythmia, Jinan, China – sequence: 7 givenname: Mei surname: Xue fullname: Xue, Mei organization: Department of Cardiology, The First Affiliated Hospital of Shandong First Medical University & Shandong Provincial Qianfoshan Hospital, Shandong Medicine and Health Key Laboratory of Cardiac Electrophysiology and Arrhythmia, Jinan, China – sequence: 8 givenname: Ye surname: Wang fullname: Wang, Ye organization: Department of Cardiology, The First Affiliated Hospital of Shandong First Medical University & Shandong Provincial Qianfoshan Hospital, Shandong Medicine and Health Key Laboratory of Cardiac Electrophysiology and Arrhythmia, Jinan, China – sequence: 9 givenname: Xiaolu surname: Li fullname: Li, Xiaolu organization: Department of Emergency, The First Affiliated Hospital of Shandong First Medical University, Jinan, China – sequence: 10 givenname: Xinran surname: Li fullname: Li, Xinran organization: Department of Cardiology, The First Affiliated Hospital of Shandong First Medical University & Shandong Provincial Qianfoshan Hospital, Shandong Medicine and Health Key Laboratory of Cardiac Electrophysiology and Arrhythmia, Jinan, China – sequence: 11 givenname: Yugen surname: Shi fullname: Shi, Yugen organization: Department of Cardiology, The First Affiliated Hospital of Shandong First Medical University & Shandong Provincial Qianfoshan Hospital, Shandong Medicine and Health Key Laboratory of Cardiac Electrophysiology and Arrhythmia, Jinan, China – sequence: 12 givenname: Jiayu surname: Tan fullname: Tan, Jiayu organization: Department of Cardiology, The First Affiliated Hospital of Shandong First Medical University & Shandong Provincial Qianfoshan Hospital, Shandong Medicine and Health Key Laboratory of Cardiac Electrophysiology and Arrhythmia, Jinan, China – sequence: 13 givenname: Yan surname: Li fullname: Li, Yan organization: Medical Research Center, The First Affiliated Hospital of Shandong First Medical University & Shandong Provincial Qianfoshan Hospital, Shandong Medicine and Health Key Laboratory of Cardiac Electrophysiology and Arrhythmia, Jinan, China – sequence: 14 givenname: Suhua surname: Yan fullname: Yan, Suhua email: yansuhua296@163.com organization: Department of Cardiology, The First Affiliated Hospital of Shandong First Medical University & Shandong Provincial Qianfoshan Hospital, Shandong Medicine and Health Key Laboratory of Cardiac Electrophysiology and Arrhythmia, Jinan, China |
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Keywords | Myocardial infarction PVN m6A Sympathetic hyperactivity TRAF6/ECSIT pathway METTL3 |
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Snippet | N6-methyladenosine (m6A) is the most prevalent post-translational modification in eukaryotic mRNA. Recently, m6A editing modified by methyltransferase-like... OBJECTIVESN6-methyladenosine (m6A) is the most prevalent post-translational modification in eukaryotic mRNA. Recently, m6A editing modified by... |
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SubjectTerms | Animals m6A Methyltransferases - genetics Methyltransferases - metabolism METTL3 Mitochondria - metabolism Myocardial infarction Myocardial Infarction - metabolism PVN Rats Reactive Oxygen Species - metabolism Sympathetic hyperactivity TNF Receptor-Associated Factor 6 - genetics TNF Receptor-Associated Factor 6 - metabolism TRAF6/ECSIT pathway |
Title | m6A methyltransferase METTL3 contributes to sympathetic hyperactivity post-MI via promoting TRAF6-dependent mitochondrial ROS production |
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