Synergistic Signaling of TLR and IFNα/β Facilitates Escape of IL-18 Expression from Endotoxin Tolerance

Am J Respir Crit Care Med. 2020 Mar 1;201(5):526-539. doi: 10.1164/rccm.201903-0659OC.

Abstract

Rationale: IL-18 is a member of the IL-1 cytokine family, and elevated blood IL-18 concentrations associate with disease activity in macrophage activation syndrome (MAS) and poor clinical outcomes in severe inflammatory and septic conditions.Objectives: Although recent investigations provide mechanistic evidence for a contribution of IL-18 to inflammation and hyperinflammation in sepsis and MAS, we sought to study regulatory mechanisms underlying human IL-18 expression.Methods: Samples from in vivo and in vitro endotoxin rechallenge experiments, patients with inflammatory disease, and isolated human monocytes treated with various stimulants and drugs were tested for cytokine gene and protein expression. Serum IL-18 expression with or without JAK/STAT inhibition was analyzed in two MAS mouse models and in a patient with recurrent MAS.Measurements and Main Results: Peripheral blood and monocytic IL-18 expression escaped LPS-induced immunoparalysis. LPS-stimulated primary human monocytes revealed specific IL-18 expression kinetics controlled by IFNα/β signaling. JAK/STAT inhibition or IFNβ neutralization during LPS stimulation blunted cytokine expression. Similarly, microtubule-destabilizing drugs abrogated LPS-induced IL18 expression, but this effect could be fully reversed by addition of IFNα/β. Ex vivo analysis of inflammatory disease patients' whole blood revealed strong correlation of type I IFN score and IL18 expression, whereas JAK/STAT inhibition strongly reduced IL-18 serum levels in two MAS mouse models and in a patient with recurrent MAS.Conclusions: Our data indicate that IL-18 (but not IL-1β) production from human monocytes requires cooperative Toll-like receptor and IFNα/β signaling. Interference with IFNα/β expression or signaling following JAK/STAT inhibition may control catastrophic hyperinflammation in MAS.

Keywords: IL-18; endotoxin tolerance; experimental human endotoxemia; macrophage activation syndrome; type I IFN.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Animals
  • Antibodies, Monoclonal, Humanized / pharmacology
  • Disease Models, Animal
  • Endotoxins
  • Gene Expression
  • Humans
  • Immune Tolerance / immunology*
  • In Vitro Techniques
  • Interferon-alpha / drug effects
  • Interferon-alpha / immunology*
  • Interferon-beta / drug effects
  • Interferon-beta / immunology*
  • Interleukin 1 Receptor Antagonist Protein / pharmacology
  • Interleukin-18 / genetics
  • Interleukin-18 / immunology*
  • Interleukin-18 / metabolism
  • Interleukin-1beta / drug effects
  • Interleukin-1beta / immunology
  • Janus Kinase Inhibitors / pharmacology
  • Lipopolysaccharides / pharmacology
  • Macrophage Activation Syndrome / genetics
  • Macrophage Activation Syndrome / immunology*
  • Macrophage Activation Syndrome / metabolism
  • Male
  • Mice
  • Monocytes / drug effects
  • Monocytes / immunology
  • Piperidines / pharmacology
  • Pyrimidines / pharmacology
  • Pyrroles / pharmacology
  • Signal Transduction
  • Toll-Like Receptors / immunology*
  • Tumor Necrosis Factor Inhibitors / pharmacology

Substances

  • Antibodies, Monoclonal, Humanized
  • Endotoxins
  • Interferon-alpha
  • Interleukin 1 Receptor Antagonist Protein
  • Interleukin-18
  • Interleukin-1beta
  • Janus Kinase Inhibitors
  • Lipopolysaccharides
  • Piperidines
  • Pyrimidines
  • Pyrroles
  • Toll-Like Receptors
  • Tumor Necrosis Factor Inhibitors
  • canakinumab
  • Interferon-beta
  • tofacitinib
  • tocilizumab