MicroRNA miR-24-3p reduces DNA damage responses, apoptosis, and susceptibility to chronic obstructive pulmonary disease

JCI Insight. 2021 Jan 25;6(2):e134218. doi: 10.1172/jci.insight.134218.

Abstract

The pathogenesis of chronic obstructive pulmonary disease (COPD) involves aberrant responses to cellular stress caused by chronic cigarette smoke (CS) exposure. However, not all smokers develop COPD and the critical mechanisms that regulate cellular stress responses to increase COPD susceptibility are not understood. Because microRNAs are well-known regulators of cellular stress responses, we evaluated microRNA expression arrays performed on distal parenchymal lung tissue samples from 172 subjects with and without COPD. We identified miR-24-3p as the microRNA that best correlated with radiographic emphysema and validated this finding in multiple cohorts. In a CS exposure mouse model, inhibition of miR-24-3p increased susceptibility to apoptosis, including alveolar type II epithelial cell apoptosis, and emphysema severity. In lung epithelial cells, miR-24-3p suppressed apoptosis through the BH3-only protein BIM and suppressed homology-directed DNA repair and the DNA repair protein BRCA1. Finally, we found BIM and BRCA1 were increased in COPD lung tissue, and BIM and BRCA1 expression inversely correlated with miR-24-3p. We concluded that miR-24-3p, a regulator of the cellular response to DNA damage, is decreased in COPD, and decreased miR-24-3p increases susceptibility to emphysema through increased BIM and apoptosis.

Keywords: Apoptosis; COPD; DNA repair; Pulmonology.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Aged
  • Animals
  • Apoptosis / genetics*
  • BRCA1 Protein / genetics
  • BRCA1 Protein / metabolism
  • Bcl-2-Like Protein 11 / genetics
  • Bcl-2-Like Protein 11 / metabolism
  • Cell Line
  • Cigarette Smoking / adverse effects
  • Cohort Studies
  • DNA Damage / genetics*
  • DNA Repair
  • Disease Models, Animal
  • Disease Susceptibility
  • Female
  • Humans
  • Lung / metabolism
  • Lung / pathology
  • Male
  • Mice
  • Mice, Inbred AKR
  • MicroRNAs / antagonists & inhibitors
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism
  • Middle Aged
  • Pulmonary Disease, Chronic Obstructive / etiology
  • Pulmonary Disease, Chronic Obstructive / genetics*
  • Pulmonary Disease, Chronic Obstructive / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Transcriptome

Substances

  • BRCA1 Protein
  • BRCA1 protein, human
  • Bcl-2-Like Protein 11
  • MIRN24 microRNA, human
  • MicroRNAs
  • Mirn24 microRNA, mouse
  • RNA, Messenger