METTL14-mediated m6A methylation regulates pathological retinal neovascularization by targeting autophagy

Exp Cell Res. 2024 Nov 1;443(1):114291. doi: 10.1016/j.yexcr.2024.114291. Epub 2024 Oct 24.

Abstract

Pathological retinal neovascularization (RNV) is a prevalent characteristic of various ocular diseases, including proliferative diabetic retinopathy (PDR), retinopathy of prematurity (ROP), and retinal vein occlusion (RVO). While the importance of N6-methyladenosine (m6A) modification in diverse disease contexts is well-established, its functional role in pathological RNV remains unclear. Herein, we investigated the involvement of m6A modification and its core methyltransferase, METTL14, in a model of oxygen-induced retinopathy (OIR) to elucidate their contribution to retinal angiogenesis. In this study, we observed heightened levels of m6A modification and elevated expression of METTL14 in the OIR model, suggesting their potential implication in pathological RNV. Employing targeted knockdown of METTL14, we revealed that its depletion activated autophagy flux in human retinal vascular endothelial cells (HRVECs), consequently inhibiting the angiogenic capacity of endothelial cells. Mechanistically, we demonstrated that METTL14 exerts its regulatory influence on autophagy flux by modulating the stability of ATG7, a pivotal protein involved in autophagy. Specifically, METTL14 knockdown led to increased ATG7 expression at both mRNA and protein levels, accompanied by reduced m6A methylation of ATG7 mRNA and enhanced mRNA stability. Moreover, silencing of ATG7 counteracted the effects of METTL14 knockdown on endothelial cell functions, emphasizing ATG7 as a downstream target of METTL14-mediated autophagy in HRVECs. After all, our findings provide valuable insights into the pathogenesis of retinal pathological angiogenesis and potential therapeutic targets for the treatment of ocular neovascular diseases.

Keywords: Angiogenesis; Autophagy; METTL14; N6-methyladenosine modification; Ocular neovascular diseases; Retinal neovascularization.

MeSH terms

  • Adenosine* / analogs & derivatives
  • Adenosine* / metabolism
  • Animals
  • Autophagy* / genetics
  • Autophagy-Related Protein 7 / genetics
  • Autophagy-Related Protein 7 / metabolism
  • Endothelial Cells / metabolism
  • Endothelial Cells / pathology
  • Humans
  • Methylation
  • Methyltransferases* / genetics
  • Methyltransferases* / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Retina / metabolism
  • Retina / pathology
  • Retinal Neovascularization* / genetics
  • Retinal Neovascularization* / metabolism
  • Retinal Neovascularization* / pathology
  • Retinal Vessels / metabolism
  • Retinal Vessels / pathology

Substances

  • Methyltransferases
  • Adenosine
  • METTL14 protein, human
  • N-methyladenosine
  • Mettl14 protein, mouse
  • Autophagy-Related Protein 7
  • ATG7 protein, human