Eosinophils promote effector functions of lung group 2 innate lymphoid cells in allergic airway inflammation in mice

J Allergy Clin Immunol. 2023 Aug;152(2):469-485.e10. doi: 10.1016/j.jaci.2023.03.023. Epub 2023 Apr 6.

Abstract

Background: Group 2 innate lymphoid cells (ILC2s) are critical mediators of type 2 respiratory inflammation, releasing IL-5 and IL-13 and promoting the pulmonary eosinophilia associated with allergen provocation. Although ILC2s have been shown to promote eosinophil activities, the role of eosinophils in group 2 innate lymphoid cell (ILC2) responses is less well defined.

Objective: We sought to investigate the role of eosinophils in activation of ILC2s in models of allergic asthma and in vitro.

Methods: Inducible eosinophil-deficient mice were exposed to allergic respiratory inflammation models of asthma, such as ovalbumin or house dust mite challenge, or to innate models of type 2 airway inflammation, such as inhalation of IL-33. Eosinophil-specific IL-4/13-deficient mice were used to address the specific roles for eosinophil-derived cytokines. Direct cell interactions between ILC2s and eosinophils were assessed by in vitro culture experiments.

Results: Targeted depletion of eosinophils resulted in significant reductions of total and IL-5+ and IL-13+ lung ILC2s in all models of respiratory inflammation. This correlated with reductions in IL-13 levels and mucus in the airway. Eosinophil-derived IL-4/13 was necessary for both eosinophil and ILC2 accumulation in lung in allergen models. In vitro, eosinophils released soluble mediators that induced ILC2 proliferation and G protein-coupled receptor-dependent chemotaxis of ILC2s. Coculture of ILC2s and IL-33-activated eosinophils resulted in transcriptome changes in both ILC2s and eosinophils, suggesting potential novel reciprocal interactions.

Conclusion: These studies demonstrate that eosinophils play a reciprocal role in ILC2 effector functions as part of both adaptive and innate type 2 pulmonary inflammatory events.

Keywords: Eosinophil; IL-13; IL-33; IL-4; asthma; eosinophil deficient; group 2 innate lymphoid cell; inflammation; lung.

Publication types

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

MeSH terms

  • Allergens / metabolism
  • Animals
  • Asthma* / metabolism
  • Cytokines / metabolism
  • Eosinophils / metabolism
  • Immunity, Innate*
  • Inflammation / metabolism
  • Interleukin-13 / metabolism
  • Interleukin-33 / metabolism
  • Interleukin-4 / metabolism
  • Interleukin-5 / metabolism
  • Lung
  • Lymphocytes
  • Mice

Substances

  • Interleukin-33
  • Interleukin-13
  • Interleukin-5
  • Interleukin-4
  • Cytokines
  • Allergens