METTL3, m6A modification, and EGR1: interplay affecting myocardial I/R injury outcomes

Cell Biol Toxicol. 2024 Dec 21;41(1):7. doi: 10.1007/s10565-024-09937-7.

Abstract

The occurrence of severe myocardial ischemia/reperfusion (I/R) injury is associated with the clinical application of reestablishment technique for heart disease, and understanding its underlying mechanisms is currently an urgent issue. Prior investigations have demonstrated the potential enhancement of MIRI through EGR1 suppression, although the precise underlying regulatory pathways require further elucidation. The core focus of this investigation is to examine the molecular pathways through EGR1 regulates mitophagy-mediated myocardial cell pyroptosis and its impact on MIRI. Cardiomyocyte hypoxia/reoxygenation (H/R) injury models and mouse models of myocardial I/R injury were used to investigate the involvement of EGR1 in regulating mitophagy-mediated myocardial cell pyroptosis in myocardial I/R injury. The research outcomes demonstrated that under H/R conditions, EGR1 expression was upregulated and inhibited the JAK2/STAT3 pathway, leading to enhanced mitophagy and disrupted mitochondrial fusion/fission dynamics, ultimately resulting in myocardial cell pyroptosis. Further research revealed that the upregulation of EGR1 expression was mediated by methyltransferase like 3 (METTL3)-mediated m6A modification of EGR1 mRNA and depended on the binding of insulin like growth factor 2 mrna binding protein 2 (IGF2BP2) to the N6-methyladenosine (m6A) modification site to enhance mRNA stability. In vivo animal experiments confirmed that METTL3 upregulated EGR1 expression through IGF2BP2 and suppressed activation of the janus kinase 2 (JAK2) /signal transducer and activator of transcription 3 (STAT3) pathway, thereby inhibiting mitophagy, disrupting mitochondrial dynamics, promoting myocardial cell pyroptosis, and exacerbating I/R injury.

Keywords: EGR1; Janus Kinase 2/Signal Transducer and Activator of Transcription 3 Pathway; M6A Modification; Mitophagy; Myocardial Cell Pyroptosis; Myocardial Ischemia/Reperfusion Injury.

MeSH terms

  • Adenosine* / analogs & derivatives
  • Adenosine* / metabolism
  • Animals
  • Early Growth Response Protein 1* / genetics
  • Early Growth Response Protein 1* / metabolism
  • Janus Kinase 2 / metabolism
  • Male
  • Methyltransferases* / genetics
  • Methyltransferases* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mitochondrial Dynamics
  • Mitophagy*
  • Myocardial Reperfusion Injury* / genetics
  • Myocardial Reperfusion Injury* / metabolism
  • Myocardial Reperfusion Injury* / pathology
  • Myocytes, Cardiac* / metabolism
  • Myocytes, Cardiac* / pathology
  • Pyroptosis
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism
  • STAT3 Transcription Factor / genetics
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction

Substances

  • Early Growth Response Protein 1
  • Methyltransferases
  • Egr1 protein, mouse
  • Adenosine
  • Mettl3 protein, mouse
  • STAT3 Transcription Factor
  • N-methyladenosine
  • RNA-Binding Proteins
  • Janus Kinase 2