IL-27 Derived From Macrophages Facilitates IL-15 Production and T Cell Maintenance Following Allergic Hypersensitivity Responses

Front Immunol. 2021 Sep 30:12:713304. doi: 10.3389/fimmu.2021.713304. eCollection 2021.

Abstract

Crosstalk between T cells, dendritic cells, and macrophages in temporal leukocyte clusters within barrier tissues provides a new concept for T cell activation in the skin. Activated T cells from these leukocyte clusters play critical roles in the efferent phase of allergic contact hypersensitivity (CHS). However, the cytokines driving maintenance and survival of pathogenic T cells during and following CHS remain mostly unknown. Upon epicutaneous allergen challenge, we here report that macrophages produce IL-27 which then induces IL-15 production from epidermal keratinocytes and dermal myeloid cells within leukocyte clusters. In agreement with the known role of IL-15 as a T cell survival factor and growth cytokine, this signaling axis enhances BCL2 and survival of skin T cells. Genetic depletion or pharmacological blockade of IL-27 in CHS mice leads to abrogated epidermal IL-15 production resulting in a decrease in BCL2 expression in T cells and a decline in dermal CD8+ T cells and T cell cluster numbers. These findings suggest that the IL-27 pathway is an important cytokine for regulating cutaneous T cell immunity.

Keywords: BCL2; CD172a; IL-15; IL-27; STAT1; contact hypersensitivity; dermal leukocyte cluster; human allergic contact dermatitis.

Publication types

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

MeSH terms

  • Allergens / immunology
  • Animals
  • Biomarkers
  • Disease Models, Animal
  • Disease Susceptibility
  • Humans
  • Hypersensitivity / immunology*
  • Hypersensitivity / metabolism*
  • Hypersensitivity / pathology
  • Interleukin-15 / biosynthesis*
  • Interleukin-27 / metabolism*
  • Keratinocytes / immunology
  • Keratinocytes / metabolism
  • Macrophages / immunology*
  • Macrophages / metabolism*
  • Mice
  • Myeloid Cells / immunology
  • Myeloid Cells / metabolism
  • Skin / immunology
  • Skin / metabolism
  • Skin / pathology
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism*
  • THP-1 Cells

Substances

  • Allergens
  • Biomarkers
  • Interleukin-15
  • Interleukin-27