Eosinophil trafficking in allergen-mediated pulmonary inflammation relies on IL-13-driven CCL-11 and CCL-24 production by tissue fibroblasts and myeloid cells

J Allergy Clin Immunol Glob. 2023 Jun 26;2(4):100131. doi: 10.1016/j.jacig.2023.100131. eCollection 2023 Nov.

Abstract

Background: The immunologic mechanisms underlying pulmonary type 2 inflammation, including the dynamics of eosinophil recruitment to the lungs, still need to be elucidated.

Objective: We sought to investigate how IL-13-producing TH2 effector cells trigger eosinophil migration in house dust mite (HDM)-driven allergic pulmonary inflammation.

Methods: Multiparameter and molecular profiling of murine lungs with HDM-induced allergy was investigated in the absence of IL-13 signaling by using IL-13Rα1-deficient mice and separately through adoptive transfer of CD4+ T cells from IL-5-deficient mice into TCRα-/- mice before allergic inflammation.

Results: We demonstrated through single-cell techniques that HDM-driven pulmonary inflammation displays a profile characterized by TH2 effector cell-induced IL-13-dominated eosinophilic inflammation. Using HDM-sensitized IL-13Rα1-/- mice, we found a marked reduction in the influx of eosinophils into the lungs along with a significant downregulation of both CCL-11 and CCL-24. We further found that eosinophil trafficking to the lung relies on production of IL-13-driven CCL-11 and CCL-24 by fibroblasts and Ly6C+ (so-called classical) monocytes. Moreover, this IL-13-mediated eotaxin-dependent eosinophil influx to the lung tissue required IL-5-induced eosinophilia. Finally, we demonstrated that this IL-13-driven eosinophil-dominated pulmonary inflammation was critical for limiting bystander lung transiting Ascaris parasites in a model of allergy and helminth interaction.

Conclusion: Our data suggest that IL-5-dependent allergen-specific TH2 effector cell response and subsequent signaling through the IL-13/IL-13Rα1 axis in fibroblasts and myeloid cells regulate the eotaxin-dependent recruitment of eosinophils to the lungs, with multiple downstream consequences, including bystander control of lung transiting parasitic helminths.

Keywords: CCL-11; CCL-24; IL-13 signaling; TH2 cell response; Type 2 inflammation; allergy; asthma; eosinophils; helminth parasites.