Depletion of microRNA-451 in response to allergen exposure accentuates asthmatic inflammation by regulating Sirtuin2

Am J Physiol Lung Cell Mol Physiol. 2020 May 1;318(5):L921-L930. doi: 10.1152/ajplung.00457.2019. Epub 2020 Mar 11.

Abstract

The incidence of asthma has increased from 5.5% to near 8% of the population, which is a major health concern. The hallmarks of asthma include eosinophilic airway inflammation that is associated with chronic airway remodeling. Allergic airway inflammation is characterized by a complex interplay of resident and inflammatory cells. MicroRNAs (miRNAs) are small noncoding RNAs that function as posttranscriptional modulators of gene expression. However, the role of miRNAs, specifically miR-451, in the regulation of allergic airway inflammation is unexplored. Our previous findings showed that oxidant stress regulates miR-451 gene expression in macrophages during an inflammatory process. In this paper, we examined the role of miR-451 in regulating macrophage phenotype using an experimental poly-allergenic murine model of allergic airway inflammation. We found that miR-451 contributes to the allergic induction of CCL17 in the lung and plays a key role in proasthmatic macrophage activation. Remarkably, administration of a Sirtuin 2 (Sirt2) inhibitor diminished alternate macrophage activation and markedly abrogated triple-allergen [dust mite, ragweed, Aspergillus fumigatus (DRA)]-induced lung inflammation. These data demonstrate a role for miR-451 in modulating allergic inflammation by influencing allergen-mediated macrophages phenotype.

Keywords: alternatively activated macrophage; asthma; eosinophilic lung inflammation; microRNA-451.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Allergens / administration & dosage
  • Animals
  • Anti-Inflammatory Agents / pharmacology
  • Antigens, Plant / administration & dosage
  • Aspergillus / chemistry
  • Aspergillus / immunology
  • Asthma / chemically induced
  • Asthma / genetics*
  • Asthma / pathology
  • Asthma / therapy
  • Chemokine CCL17 / genetics
  • Chemokine CCL17 / immunology
  • Disease Models, Animal
  • Fungi / chemistry
  • Fungi / immunology
  • Furans / pharmacology
  • Gene Expression Regulation
  • Lung / drug effects
  • Lung / immunology
  • Lung / pathology
  • Macrophage Activation / drug effects
  • Macrophages, Alveolar / drug effects
  • Macrophages, Alveolar / immunology*
  • Macrophages, Alveolar / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • MicroRNAs / genetics*
  • MicroRNAs / immunology
  • Plant Extracts / administration & dosage
  • Pneumonia / chemically induced
  • Pneumonia / genetics*
  • Pneumonia / pathology
  • Pneumonia / therapy
  • Pyroglyphidae / chemistry
  • Pyroglyphidae / immunology
  • Quinolines / pharmacology
  • Signal Transduction
  • Sirtuin 2 / antagonists & inhibitors
  • Sirtuin 2 / genetics*
  • Sirtuin 2 / immunology

Substances

  • AGK2 compound
  • Allergens
  • Anti-Inflammatory Agents
  • Antigens, Plant
  • Ccl17 protein, mouse
  • Chemokine CCL17
  • Furans
  • MicroRNAs
  • Mirn451 microRNA, mouse
  • Plant Extracts
  • Quinolines
  • ragweed pollen
  • Sirt2 protein, mouse
  • Sirtuin 2