c-Maf enforces cytokine production and promotes memory-like responses in mouse and human type 2 innate lymphoid cells

EMBO J. 2022 Jun 14;41(12):e109300. doi: 10.15252/embj.2021109300. Epub 2022 Apr 25.

Abstract

Group-2 innate lymphoid cells (ILC2s), which are involved in type 2 inflammatory diseases such as allergy, can exhibit immunological memory, but the basis of this ILC2 "trained immunity" has remained unclear. Here, we found that stimulation with IL-33/IL-25 or exposure to the allergen papain induces the expression of the transcription factor c-Maf in mouse ILC2s. Chronic papain exposure results in high production of IL-5 and IL-13 cytokines and lung eosinophil recruitment, effects that are blocked by c-Maf deletion in ILCs. Transcriptomic analysis revealed that knockdown of c-Maf in ILC2s suppresses expression of type 2 cytokine genes, as well as of genes linked to a memory-like phenotype. Consistently, c-Maf was found highly expressed in human adult ILC2s but absent in cord blood and required for cytokine production in isolated human ILC2s. Furthermore, c-Maf-deficient mouse or human ILC2s failed to exhibit strengthened ("trained") responses upon repeated challenge. Thus, the expression of c-Maf is indispensable for optimal type 2 cytokine production and proper memory-like responses in group-2 innate lymphoid cells.

Keywords: ILC2; c-Maf; immune training; lung inflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cytokines / metabolism
  • Humans
  • Immunity, Innate*
  • Interleukin-33 / genetics
  • Interleukin-33 / metabolism
  • Lung / metabolism
  • Lymphocytes* / metabolism
  • Mice
  • Papain / metabolism
  • Proto-Oncogene Proteins c-maf / metabolism

Substances

  • Cytokines
  • Interleukin-33
  • Maf protein, mouse
  • Proto-Oncogene Proteins c-maf
  • Papain

Associated data

  • GEO/GSE166739