MicroRNA-146a is induced by inflammatory stimuli in airway epithelial cells and augments the anti-inflammatory effects of glucocorticoids

PLoS One. 2018 Oct 9;13(10):e0205434. doi: 10.1371/journal.pone.0205434. eCollection 2018.

Abstract

Background: MicroRNAs (miRNAs) are emerging as central regulators of inflammation, but their role in asthma and airway epithelial cells is not well studied. Glucocorticoids are the cornerstone of therapy in asthma and other inflammatory disease, yet their mechanisms of action are not completely elucidated, and it is not clear whether miRNAs modulate their effects.

Objective: We aimed to identify miRNAs that regulate cytokine and chemokine expression in airway epithelial cells and whether these miRNAs are subject to the effects of glucocorticoids.

Methods and results: MicroRNAomic analyses of immortalized, normal human bronchial epithelial cells identified 7 miRNAs that were altered by inflammatory cytokine treatment and 22 that were regulated by glucocorticoids (n = 3 for each treatment condition). MiR-146a emerged as a central candidate, whose expression was induced by TNF-α and repressed by glucocorticoids. Its role as a candidate in asthmatic inflammation was supported by expression profiling in human asthmatics, which showed that plasma miR-146a expression was elevated in asthma and associated with measures related to worse asthma outcomes, including elevated blood eosinophil counts, higher asthma control questionnaire scores, and need for higher doses of inhaled glucocorticoids. However, transfection of miR-146a in A549 cells treated with TNF-α +/- glucocorticoids produced an anti-inflammatory effect and increased efficacy of glucocorticoids.

Conclusions: We propose a model whereby miR-146a is induced by inflammatory conditions as a feedback mechanism to limit inflammation. Exogenous administration of miR-146a augmented the effects of glucocorticoids and could be a novel therapeutic strategy to enhance efficacy of these medications.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • A549 Cells
  • Adult
  • Anti-Inflammatory Agents / pharmacology*
  • Asthma / genetics
  • Asthma / pathology
  • Bronchi / cytology
  • Case-Control Studies
  • Chemokine CCL2 / genetics
  • Chemokine CCL2 / metabolism
  • Dexamethasone / pharmacology
  • Eosinophils / cytology
  • Epithelial Cells / cytology
  • Epithelial Cells / drug effects
  • Epithelial Cells / metabolism
  • Female
  • Glucocorticoids / pharmacology*
  • Humans
  • Interleukin-6 / genetics
  • Interleukin-6 / metabolism
  • Male
  • MicroRNAs / blood
  • MicroRNAs / genetics
  • MicroRNAs / metabolism*
  • Middle Aged
  • Severity of Illness Index
  • Tumor Necrosis Factor-alpha / pharmacology*
  • Up-Regulation / drug effects*

Substances

  • Anti-Inflammatory Agents
  • CCL2 protein, human
  • Chemokine CCL2
  • Glucocorticoids
  • Interleukin-6
  • MIRN146 microRNA, human
  • MicroRNAs
  • Tumor Necrosis Factor-alpha
  • Dexamethasone

Grants and funding

This work was supported in part by a grant from the Doris Duke Charitable Foundation awarded to Faoud T. Ishmael. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.