Helminth infection induces a distinct subset of CD101hi lung tissue-infiltrating eosinophils that are differentially regulated by type 2 cytokines

Immunol Cell Biol. 2024 Sep;102(8):734-746. doi: 10.1111/imcb.12796. Epub 2024 Jun 26.

Abstract

Eosinophils play divergent roles in health and disease, contributing to both immunoregulatory and proinflammatory responses. Helminth infection is strongly associated with eosinophilia and the induction of the type 2 cytokines interleukin (IL)-5, IL-4 and IL-13. This study aimed to elucidate the heterogeneity of pulmonary eosinophils in response to helminth infection and the roles of IL-5, IL-4 and IL-13 in driving pulmonary eosinophil responses. Using the murine helminth model Nippostrongylus brasiliensis (Nb), we characterize a subtype of eosinophils, defined by high expression of CD101, that is induced in the lungs of Nb-infected mice and are phenotypically distinct from lung eosinophils that express low levels of CD101. Strikingly, we show that the two eosinophil subtypes have distinct anatomical localization within the lung: CD101low eosinophils are predominantly localized in the lung vasculature, whereas Nb-induced CD101hi eosinophils are predominantly localized in the extravascular lung niche. We show that CD101hi eosinophils are also induced across other models of pulmonary infection and inflammation, including a nonlung-migrating helminth infection, house dust mite-induced allergic inflammation and influenza infection. Furthermore, we demonstrate that the induction of CD101hi tissue eosinophils is independent of IL-5 and IL-4 signaling, but is dependent on intact IL-13 signaling. These results suggest that IL-13 produced during helminth infection and other disease states promotes a pulmonary tissue-infiltrating program in eosinophils defined by high expression of CD101.

Keywords: Nippostrongylus brasiliensis; eosinophils; helminths; lung; tissue infiltrating; type 2 cytokines.

MeSH terms

  • Animals
  • Cytokines* / metabolism
  • Disease Models, Animal
  • Eosinophils* / immunology
  • Female
  • Helminthiasis / immunology
  • Helminthiasis / parasitology
  • Interleukin-13 / metabolism
  • Interleukin-5 / immunology
  • Interleukin-5 / metabolism
  • Lung* / immunology
  • Lung* / parasitology
  • Lung* / pathology
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Nippostrongylus* / immunology
  • Strongylida Infections / immunology
  • Strongylida Infections / parasitology

Substances

  • Cytokines
  • Interleukin-13
  • Interleukin-5