IL-33 promotes type 1 cytokine expression via p38 MAPK in human NK cells

J Leukoc Biol. 2020 Apr;107(4):663-671. doi: 10.1002/JLB.3A0120-379RR. Epub 2020 Feb 4.

Abstract

This study tests the hypothesis that activation of MAPK by physiologically relevant concentrations of IL-33 contributes to enhanced cytokine expression by IL-12 stimulated human NK cells. While IL-33 canonically triggers type 2 cytokine responses, this cytokine can also synergize with type 1 cytokines like IL-12 to provoke IFN-γ. We show that picogram concentrations of IL-12 and IL-33 are sufficient to promote robust secretion of IFN-γ by human NK cells that greatly exceeds resposes to either cytokine alone. Nanogram doses of IL-33, potentially consistent with levels in tissue microenvironments, synergize with IL-12 to induce secretion of additional cytokines, including TNF and GM-CSF. IL-33-induced activation of the p38 MAPK pathway in human NK cells is crucial for enhanced release of IFN-γ and TNF in response to IL-12. Mechanistically, IL-33-induced p38 MAPK signaling enhances stability of IFNG transcripts and triggers A disintegrin and metalloproteinase domain 17 (ADAM17) mediated cleavage of TNF from the cell surface. These data support our hypothesis and suggest that altered sensitivity of NK cells to IL-12 in the presence of IL-33 may have important consequences in diseases associated with mixed cytokine milieus, like asthma and chronic obstructive pulmonary disease.

Keywords: GM-CSF; IL-12; NK; TNF; innate lymphoid cell; synergy.

Publication types

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

MeSH terms

  • ADAM17 Protein / metabolism
  • Cell Line
  • Cytokines / metabolism*
  • Humans
  • Interferon-gamma / genetics
  • Interferon-gamma / metabolism
  • Interleukin-1 Receptor-Like 1 Protein / metabolism
  • Interleukin-12 / metabolism
  • Interleukin-33 / metabolism*
  • Killer Cells, Natural / metabolism*
  • Phosphorylation
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • STAT4 Transcription Factor / metabolism
  • Tumor Necrosis Factor-alpha / metabolism
  • p38 Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • p38 Mitogen-Activated Protein Kinases / metabolism*

Substances

  • Cytokines
  • IL1RL1 protein, human
  • Interleukin-1 Receptor-Like 1 Protein
  • Interleukin-33
  • RNA, Messenger
  • STAT4 Transcription Factor
  • Tumor Necrosis Factor-alpha
  • Interleukin-12
  • Interferon-gamma
  • p38 Mitogen-Activated Protein Kinases
  • ADAM17 Protein