TNF-anti-TNF Immune Complexes Inhibit IL-12/IL-23 Secretion by Inflammatory Macrophages via an Fc-dependent Mechanism

J Crohns Colitis. 2018 Aug 29;12(9):1122-1130. doi: 10.1093/ecco-jcc/jjy075.

Abstract

Background and aims: We have recently shown that the mode of action of IgG1 anti-tumour necrosis factor [TNF] antibodies in inflammatory bowel disease [IBD] requires Fcγ-receptor [FcγR] engagement on macrophages. Here we examine the effect of Fcγ-receptor signalling by anti-TNF on macrophage IL-12/IL-23 secretion.

Methods: Cytokine production by human inflammatory macrophages was assessed at the level of RNA and protein. TNF-anti-TNF immune complex formation was determined by size-exclusion chromatography and signalling visualized by immunofluorescence. IL-12/IL-23p40 was measured in CD14+ lamina propria cells from IBD patients.

Results: Infliximab and adalimumab potently suppressed IL-12/IL-23 production by inflammatory macrophages, but Fab' fragment certolizumab did not. IL-12/IL-23 suppression depended on Syk activity and was mediated at the level of IL-12/IL-23p40 mRNA. Etanercept, a soluble TNF receptor fused to an Fc-region, did not inhibit IL-12/L-23 secretion, suggesting that the presence of an Fc-region was not sufficient. Infliximab and adalimumab formed immune complexes with soluble TNF whereas etanercept did not, suggesting that FcγR-mediated suppression of IL-12/IL-23 required the formation of immune complexes. Indeed, non-specific IgG1 immune complexes, but not uncomplexed IgG1, similarly suppressed IL-12/IL-23 secretion. Finally, infliximab significantly decreased IL-12/IL-23p40 production in myeloid cells isolated from the lamina propria of IBD patients.

Conclusions: TNF-anti-TNF antibody immune complexes potently inhibit IL-12/IL-23 expression by inflammatory macrophages. Our data suggest that anti-TNFs and antibodies against IL-12/IL-23 may therefore have partially overlapping modes of action in patients with IBD.

Keywords: Anti-TNF; IL-12/IL-23 axis; macrophage.

MeSH terms

  • Adalimumab / pharmacology
  • Antibodies, Monoclonal / pharmacology
  • Antigen-Antibody Complex
  • Cell Culture Techniques
  • Certolizumab Pegol / pharmacology
  • Crohn Disease / drug therapy*
  • Crohn Disease / metabolism
  • Crohn Disease / pathology
  • Etanercept / pharmacology
  • Gastrointestinal Agents / pharmacology*
  • Humans
  • Immunoglobulin Fab Fragments
  • Immunoglobulin G / metabolism
  • Infliximab / pharmacology
  • Interleukin-12 / metabolism*
  • Interleukin-23 / metabolism*
  • Macrophages / drug effects*
  • Macrophages / physiology
  • Tumor Necrosis Factor-alpha / antagonists & inhibitors*

Substances

  • Antibodies, Monoclonal
  • Antigen-Antibody Complex
  • Gastrointestinal Agents
  • Immunoglobulin Fab Fragments
  • Immunoglobulin G
  • Interleukin-23
  • Tumor Necrosis Factor-alpha
  • Interleukin-12
  • golimumab
  • Infliximab
  • Adalimumab
  • Etanercept
  • Certolizumab Pegol