Unopposed IL-18 signaling leads to severe TLR9-induced macrophage activation syndrome in mice

Blood. 2018 Mar 29;131(13):1430-1441. doi: 10.1182/blood-2017-06-789552. Epub 2018 Jan 2.

Abstract

The term macrophage activation syndrome (MAS) defines a severe, potentially fatal disorder characterized by overwhelming inflammation and multiorgan involvement. Interleukin-18 (IL-18) is a proinflammatory cytokine belonging to the IL-1 family, the activity of which is regulated by its endogenous inhibitor IL-18 binding protein (IL-18BP). Elevated IL-18 levels have been reported in patients with MAS. Herein, we show that on repeated toll-like receptor 9 (TLR9) stimulation with unmethylated cytosine guanine dinucleotide containing single-stranded DNA (CpG), IL-18BP-/- mice display severe MAS manifestations, including increased weight loss, splenomegaly, anemia, thrombocytopenia, hyperferritinemia, and bone marrow hemophagocytosis as compared with wild-type mice. Serum-free IL-18 was detected in CpG-treated IL-18BP-/- mice only. Levels of interferon-γ (IFN-γ) and of IFN-γ signature genes, such as the chemokine Cxcl9 or the transcription factor CIIta, were significantly increased in IL-18BP-/- mice. Blocking IL-18 receptor signaling attenuated the severity of MAS and IFN-γ responses in IL-18BP-/- mice. Blocking IFN-γ had comparable effects to IL-18 inhibition on most MAS manifestations. Our data indicate that endogenous IL-18BP exerts a protective role in CpG-induced MAS and that IL-18, which acts upstream of IFN-γ, is involved in the severity of MAS.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Chemokine CXCL9 / genetics
  • Chemokine CXCL9 / immunology
  • Intercellular Signaling Peptides and Proteins / genetics
  • Intercellular Signaling Peptides and Proteins / immunology
  • Interferon-gamma / genetics
  • Interferon-gamma / immunology
  • Interleukin-18 / genetics
  • Interleukin-18 / immunology*
  • Macrophage Activation Syndrome / chemically induced
  • Macrophage Activation Syndrome / genetics
  • Macrophage Activation Syndrome / immunology*
  • Macrophage Activation Syndrome / pathology
  • Mice
  • Mice, Knockout
  • Nuclear Proteins / genetics
  • Nuclear Proteins / immunology
  • Oligodeoxyribonucleotides / adverse effects
  • Oligodeoxyribonucleotides / pharmacology
  • Signal Transduction / drug effects
  • Signal Transduction / genetics
  • Signal Transduction / immunology*
  • Toll-Like Receptor 9 / agonists
  • Toll-Like Receptor 9 / genetics
  • Toll-Like Receptor 9 / immunology*
  • Trans-Activators / genetics
  • Trans-Activators / immunology

Substances

  • CPG-oligonucleotide
  • Chemokine CXCL9
  • Cxcl9 protein, mouse
  • IFNG protein, mouse
  • Intercellular Signaling Peptides and Proteins
  • Interleukin-18
  • MHC class II transactivator protein
  • Nuclear Proteins
  • Oligodeoxyribonucleotides
  • Tlr9 protein, mouse
  • Toll-Like Receptor 9
  • Trans-Activators
  • interleukin-18 binding protein
  • Interferon-gamma