Interleukin-37 exacerbates liver inflammation and promotes IFN-γ production in NK cells

Int Immunopharmacol. 2024 Dec 5;142(Pt A):113086. doi: 10.1016/j.intimp.2024.113086. Epub 2024 Sep 12.

Abstract

Interleukin (IL)-37, a unique member of the IL-1 family, is known for its anti-inflammatory properties. However, its effects on immune-mediated liver diseases, such as primary biliary cholangitis (PBC) and acute immune-mediated hepatitis, remain unclear. Using mouse models of autoimmune cholangitis and hepatitis induced by 2-OA-OVA and concanavalin A (Con A) respectively, we introduced the human IL-37 gene via a liver-preferred adeno-associated virus vector (AAV-IL-37) to mice, as mice lack endogenous IL-37. Our findings reveal that IL-37 did not affect autoimmune cholangitis. Surprisingly, IL-37 exacerbated inflammation in Con A-induced hepatitis rather than mitigating it. Mechanistic insights suggest that this exacerbation involves the interferon (IFN)-γ pathway, supported by elevated serum IFN-γ levels in AAV-IL-37-treated Con A mice. Specifically, IL-37 heightened the number of hepatic NK and NKT cells, increased the production of the NK cell chemoattractant CCL5, and elevated the frequency of hepatic NK and NKT cells expressing IFN-γ. Moreover, IL-37 enhanced IFN-γ secretion from NK cells when combined with other proinflammatory cytokines, highlighting its synergistic effect in promoting IFN-γ production. These unexpected outcomes underscore a novel role for IL-37 in exacerbating liver inflammation during immune-mediated liver diseases, implicating its influence on NK cells and the production of IFN-γ by these cells.

Keywords: Adeno-associated virus vector; IFN-γ; IL-37; Immune-mediated liver disease; NK cells.

MeSH terms

  • Animals
  • Concanavalin A
  • Dependovirus / genetics
  • Disease Models, Animal
  • Female
  • Hepatitis / immunology
  • Hepatitis / pathology
  • Humans
  • Interferon-gamma* / metabolism
  • Interleukin-1* / genetics
  • Interleukin-1* / metabolism
  • Killer Cells, Natural* / immunology
  • Liver / immunology
  • Liver / metabolism
  • Liver / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • Natural Killer T-Cells / immunology

Substances

  • Concanavalin A
  • IL37 protein, human
  • Interferon-gamma
  • Interleukin-1
  • IFNG protein, human
  • IFNG protein, mouse