The aberrant cross-talk of epithelium-macrophages via METTL3-regulated extracellular vesicle miR-93 in smoking-induced emphysema

Cell Biol Toxicol. 2022 Feb;38(1):167-183. doi: 10.1007/s10565-021-09585-1. Epub 2021 Mar 4.

Abstract

Cigarette smoke (CS), a complex chemical indoor air pollutant, induces degradation of elastin, resulting in emphysema. Aberrant cross-talk between macrophages and bronchial epithelial cells is essential for the degradation of elastin that contributes to emphysema, in which extracellular vesicles (EVs) play a critical role. The formation of N6-methyladenosine (m6A) is a modification in miRNA processing, but its role in the development of emphysema remains unclear. Here, we established that production of excess mature microRNA-93 (miR-93) in bronchial epithelial cells via enhanced m6A modification was mediated by overexpressed methyltransferase-like 3 (METTL3) induced by CS. Mature miR-93 was transferred from bronchial epithelial cells into macrophages by EVs. In macrophages, miR-93 activated the JNK pathway by targeting dual-specificity phosphatase 2 (DUSP2), which elevated the levels of matrix metalloproteinase 9 (MMP9) and matrix metalloproteinase 12 (MMP12) and induced elastin degradation, leading to emphysema. These results demonstrate that METTL3-mediated formation of EV miR-93, facilitated by m6A, is implicated in the aberrant cross-talk of epithelium-macrophages, indicating that this process is involved in the smoking-related emphysema. EV miR-93 may use as a novel risk biomarker for CS-induced emphysema.

Keywords: Cigarette smoke; Emphysema; Extracellular vesicles; MicroRNAs; N6-methyladenosine.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Elastin
  • Emphysema*
  • Epithelium / metabolism
  • Extracellular Vesicles*
  • Humans
  • Macrophages / metabolism
  • Methyltransferases / genetics
  • Methyltransferases / metabolism
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • Smoking / adverse effects

Substances

  • MIRN93 microRNA, human
  • MicroRNAs
  • Elastin
  • Methyltransferases
  • METTL3 protein, human