Self double-stranded (ds)DNA induces IL-1β production from human monocytes by activating NLRP3 inflammasome in the presence of anti-dsDNA antibodies

J Immunol. 2013 Feb 15;190(4):1407-15. doi: 10.4049/jimmunol.1201195. Epub 2013 Jan 11.

Abstract

The pathogenic hallmark of systemic lupus erythematosus is the autoimmune response against self nuclear Ags, including dsDNA. The increased expression of the proinflammatory cytokine IL-1β has been found in the cutaneous lesion and PBMCs from lupus patients, suggesting a potential involvement of this cytokine in the pathogenesis of lupus. IL-1β is produced primarily by innate immune cells such as monocytes and can promote a Th17 cell response, which is increased in lupus. IL-1β production requires cleaving pro-IL-β into IL-1β by the caspase-1-associated multiprotein complex called inflammasomes. In this study we show that self dsDNA induces IL-1β production from human monocytes dependent on serum or purified IgG containing anti-dsDNA Abs by activating the nucleotide-binding oligomerization domain-like receptor family pyrin domain-containing 3 (NLRP3) inflammasome. Reactive oxygen species (ROS) and K(+) efflux were involved in this activation. Knocking down the NLRP3 or inhibiting caspase-1, ROS, and K(+) efflux decreased IL-1β production. Supernatants from monocytes treated with a combination of self dsDNA and anti-dsDNA Ab(+) serum promoted IL-17 production from CD4(+) T cells in an IL-1β-dependent manner. These findings provide new insights in lupus pathogenesis by demonstrating that self dsDNA together with its autoantibodies induces IL-1β production from human monocytes by activating the NLRP3 inflammasome through inducing ROS synthesis and K(+) efflux, leading to the increased Th17 cell response.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Autoantibodies / blood
  • Autoantibodies / physiology*
  • Carrier Proteins / blood
  • Carrier Proteins / metabolism*
  • Carrier Proteins / physiology
  • Caspase 1 / physiology
  • Cell Line, Tumor
  • Cells, Cultured
  • DNA / blood
  • DNA / immunology
  • DNA / physiology*
  • Humans
  • Interleukin-1beta / biosynthesis*
  • Interleukin-1beta / blood
  • Jurkat Cells
  • Monocytes / cytology
  • Monocytes / immunology*
  • Monocytes / metabolism*
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Serum / physiology

Substances

  • Autoantibodies
  • Carrier Proteins
  • Interleukin-1beta
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLRP3 protein, human
  • DNA
  • Caspase 1