A Jagged 1-Notch 4 molecular switch mediates airway inflammation induced by ultrafine particles

J Allergy Clin Immunol. 2018 Oct;142(4):1243-1256.e17. doi: 10.1016/j.jaci.2018.03.009. Epub 2018 Apr 5.

Abstract

Background: Exposure to traffic-related particulate matter promotes asthma and allergic diseases. However, the precise cellular and molecular mechanisms by which particulate matter exposure acts to mediate these effects remain unclear.

Objective: We sought to elucidate the cellular targets and signaling pathways critical for augmentation of allergic airway inflammation induced by ambient ultrafine particles (UFP).

Methods: We used in vitro cell-culture assays with lung-derived antigen-presenting cells and allergen-specific T cells and in vivo mouse models of allergic airway inflammation with myeloid lineage-specific gene deletions, cellular reconstitution approaches, and antibody inhibition studies.

Results: We identified lung alveolar macrophages (AM) as the key cellular target of UFP in promoting airway inflammation. Aryl hydrocarbon receptor-dependent induction of Jagged 1 (Jag1) expression in AM was necessary and sufficient for augmentation of allergic airway inflammation by UFP. UFP promoted TH2 and TH17 cell differentiation of allergen-specific T cells in a Jag1- and Notch 4-dependent manner. Treatment of mice with an anti-Notch 4 antibody abrogated exacerbation of allergic airway inflammation induced by UFP.

Conclusion: UFP exacerbate allergic airway inflammation by promoting a Jag1-Notch 4-dependent interaction between AM and allergen-specific T cells, leading to augmented TH cell differentiation.

Keywords: Airway hyperresponsiveness; Jagged 1; Notch; Notch 4; allergic airway inflammation; alveolar macrophages; aryl hydrocarbon receptor; asthma; traffic-related particulate matter; ultrafine particles.

Publication types

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

MeSH terms

  • Air Pollutants / toxicity*
  • Animals
  • Antibodies, Monoclonal / therapeutic use
  • Antigen-Presenting Cells / immunology
  • Immunoglobulin G / immunology
  • Jagged-1 Protein / immunology*
  • Macrophages, Alveolar / immunology*
  • Mice, Inbred BALB C
  • Mice, Transgenic
  • Particulate Matter / toxicity*
  • Receptor, Notch4 / antagonists & inhibitors
  • Receptor, Notch4 / immunology*
  • Respiratory Hypersensitivity / drug therapy
  • Respiratory Hypersensitivity / immunology*
  • T-Lymphocytes / immunology*

Substances

  • Air Pollutants
  • Antibodies, Monoclonal
  • Immunoglobulin G
  • Jagged-1 Protein
  • Particulate Matter
  • Receptor, Notch4
  • Notch4 protein, mouse