Arf6 exacerbates allergic asthma through cell-to-cell transmission of ASC inflammasomes

JCI Insight. 2021 Aug 23;6(16):e139190. doi: 10.1172/jci.insight.139190.

Abstract

Asthma is a chronic inflammatory disease of the airways associated with excess production of Th2 cytokines and lung eosinophil accumulation. This inflammatory response persists in spite of steroid administration that blocks autocrine/paracrine loops of inflammatory cytokines, and the detailed mechanisms underlying asthma exacerbation remain unclear. Here, we show that asthma exacerbation is triggered by airway macrophages through a prion-like cell-to-cell transmission of extracellular particulates, including ASC protein, that assemble inflammasomes and mediate IL-1β production. OVA-induced allergic asthma and associated IL-1β production were alleviated in mice with small GTPase Arf6-deficient macrophages. The extracellular ASC specks were slightly engulfed by Arf6-/- macrophages, and the IL-1β production was reduced in Arf6-/- macrophages compared with that in WT macrophages. Furthermore, pharmacological inhibition of the Arf6 guanine nucleotide exchange factor suppressed asthma-like allergic inflammation in OVA-challenged WT mice. Collectively, the Arf6-dependent intercellular transmission of extracellular ASC specks contributes to the amplification of allergic inflammation and subsequent asthma exacerbation.

Keywords: Asthma; Inflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ADP-Ribosylation Factor 6 / antagonists & inhibitors
  • ADP-Ribosylation Factor 6 / genetics
  • ADP-Ribosylation Factor 6 / metabolism*
  • Animals
  • Asthma / drug therapy
  • Asthma / immunology*
  • Asthma / pathology
  • CARD Signaling Adaptor Proteins / metabolism
  • Cell Communication / drug effects
  • Cell Communication / immunology*
  • Disease Models, Animal
  • Humans
  • Inflammasomes / drug effects
  • Inflammasomes / immunology*
  • Inflammasomes / metabolism
  • Interleukin-1beta / metabolism
  • Lung / immunology
  • Lung / pathology
  • Macrophages, Alveolar / immunology*
  • Macrophages, Alveolar / metabolism
  • Mice
  • Mice, Knockout
  • Ovalbumin / administration & dosage
  • Ovalbumin / immunology
  • Phagocytosis / drug effects
  • Symptom Flare Up
  • THP-1 Cells
  • Th2 Cells
  • Triazoles / administration & dosage

Substances

  • ADP-Ribosylation Factor 6
  • CARD Signaling Adaptor Proteins
  • IL1B protein, mouse
  • Inflammasomes
  • Interleukin-1beta
  • PYCARD protein, human
  • Pycard protein, mouse
  • SecinH3
  • Triazoles
  • Ovalbumin
  • Arf6 protein, mouse