Epithelial IL-33 appropriates exosome trafficking for secretion in chronic airway disease

JCI Insight. 2021 Feb 22;6(4):e136166. doi: 10.1172/jci.insight.136166.

Abstract

IL-33 is a key mediator of chronic airway disease driven by type 2 immune pathways, yet the nonclassical secretory mechanism for this cytokine remains undefined. We performed a comprehensive analysis in human airway epithelial cells, which revealed that tonic IL-33 secretion is dependent on the ceramide biosynthetic enzyme neutral sphingomyelinase 2 (nSMase2). IL-33 is cosecreted with exosomes by the nSMase2-regulated multivesicular endosome (MVE) pathway as surface-bound cargo. In support of these findings, human chronic obstructive pulmonary disease (COPD) specimens exhibited increased epithelial expression of the abundantly secreted IL33Δ34 isoform and augmented nSMase2 expression compared with non-COPD specimens. Using an Alternaria-induced airway disease model, we found that the nSMase2 inhibitor GW4869 abrogated both IL-33 and exosome secretion as well as downstream inflammatory pathways. This work elucidates a potentially novel aspect of IL-33 biology that may be targeted for therapeutic benefit in chronic airway diseases driven by type 2 inflammation.

Keywords: COPD; Cellular immune response; Cytokines; Immunology; Pulmonology.

Publication types

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

MeSH terms

  • Aniline Compounds
  • Animals
  • Benzylidene Compounds
  • Ceramides / metabolism
  • Cytokines / metabolism
  • Epithelial Cells / metabolism
  • Exosomes / metabolism*
  • Humans
  • Immunity, Cellular
  • Inflammation / metabolism
  • Interleukin-33 / genetics
  • Interleukin-33 / immunology*
  • Interleukin-33 / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Pulmonary Disease, Chronic Obstructive / genetics
  • Pulmonary Disease, Chronic Obstructive / immunology*
  • Pulmonary Disease, Chronic Obstructive / metabolism*
  • Pulmonary Disease, Chronic Obstructive / pathology
  • Respiratory System

Substances

  • Aniline Compounds
  • Benzylidene Compounds
  • Ceramides
  • Cytokines
  • GW 4869
  • IL33 protein, human
  • Interleukin-33

Supplementary concepts

  • Pulmonary Disease, Chronic Obstructive, Severe Early-Onset