C-terminal truncation of IFN-γ inhibits proinflammatory macrophage responses and is deficient in autoimmune disease

Nat Commun. 2018 Jun 20;9(1):2416. doi: 10.1038/s41467-018-04717-4.

Abstract

Controlled macrophage differentiation and activation in the initiation and resolution of inflammation is crucial for averting progression to chronic inflammatory and autoimmune diseases. Here we show a negative feedback mechanism for proinflammatory IFN-γ activation of macrophages driven by macrophage-associated matrix metalloproteinase 12 (MMP12). Through C-terminal truncation of IFN-γ at 135Glu↓Leu136 the IFN-γ receptor-binding site was efficiently removed thereby reducing JAK-STAT1 signaling and IFN-γ activation of proinflammatory macrophages. In acute peritonitis this signature was absent in Mmp12 -/- mice and recapitulated in Mmp12 +/+ mice treated with a MMP12-specific inhibitor. Similarly, loss-of-MMP12 increases IFN-γ-dependent proinflammatory markers and iNOS+/MHC class II+ macrophage accumulation with worse lymphadenopathy, arthritic synovitis and lupus glomerulonephritis. In active human systemic lupus erythematosus, MMP12 levels were lower and IFN-γ higher compared to treated patients or healthy individuals. Hence, macrophage proteolytic truncation of IFN-γ attenuates classical activation of macrophages as a prelude for resolving inflammation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arthritis / immunology
  • Arthritis / pathology
  • Biopsy
  • Cell Line
  • Collagen / immunology
  • Disease Models, Animal
  • Female
  • Humans
  • Interferon-gamma / metabolism*
  • Kidney / pathology
  • Lupus Nephritis / immunology*
  • Lupus Nephritis / pathology
  • Macrophage Activation / drug effects
  • Macrophage Activation / immunology*
  • Macrophages / immunology
  • Macrophages / metabolism
  • Male
  • Matrix Metalloproteinase 12 / genetics
  • Matrix Metalloproteinase 12 / metabolism*
  • Matrix Metalloproteinase Inhibitors / pharmacology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Peritonitis / chemically induced
  • Peritonitis / immunology
  • Peritonitis / pathology
  • Primary Cell Culture
  • Proteolysis
  • RAW 264.7 Cells
  • Signal Transduction / drug effects
  • Signal Transduction / immunology
  • THP-1 Cells
  • Thioglycolates / toxicity

Substances

  • IFNG protein, human
  • IFNG protein, mouse
  • Matrix Metalloproteinase Inhibitors
  • Thioglycolates
  • Interferon-gamma
  • Collagen
  • MMP12 protein, human
  • Matrix Metalloproteinase 12
  • matrix metallopeptidase 12, mouse