Lipopolysaccharide Primes the NALP3 Inflammasome by Inhibiting Its Ubiquitination and Degradation Mediated by the SCFFBXL2 E3 Ligase

J Biol Chem. 2015 Jul 17;290(29):18124-18133. doi: 10.1074/jbc.M115.645549. Epub 2015 Jun 2.

Abstract

The inflammasome is a multiprotein complex that augments the proinflammatory response by increasing the generation and cellular release of key cytokines. Specifically, the NALP3 inflammasome requires two-step signaling, priming and activation, to be functional to release the proinflammatory cytokines IL-1β and IL-18. The priming process, through unknown mechanisms, increases the protein levels of NALP3 and pro-IL-1β in cells. Here we show that LPS increases the NALP3 protein lifespan without significantly altering steady-state mRNA in human cells. LPS exposure reduces the ubiquitin-mediated proteasomal processing of NALP3 by inducing levels of an E3 ligase component, FBXO3, which targets FBXL2. The latter is an endogenous mediator of NALP3 degradation. FBXL2 recognizes Trp-73 within NALP3 for interaction and targets Lys-689 within NALP3 for ubiquitin ligation and degradation. A unique small molecule inhibitor of FBXO3 restores FBXL2 levels, resulting in decreased NALP3 protein levels in cells and, thereby, reducing the release of IL-1β and IL-18 in human inflammatory cells after NALP3 activation. Our findings uncover NALP3 as a molecular target for FBXL2 and suggest that therapeutic targeting of the inflammasome may serve as a platform for preclinical intervention.

Keywords: IL-1; NALP3; cytokine induction; inflammasome; inflammation; innate immunity.

Publication types

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

MeSH terms

  • Carrier Proteins / immunology*
  • Carrier Proteins / metabolism
  • Cell Line
  • F-Box Proteins / immunology*
  • F-Box Proteins / metabolism
  • Humans
  • Immunity, Innate
  • Inflammasomes / immunology*
  • Inflammasomes / metabolism
  • Interleukin-18 / immunology
  • Interleukin-1beta / immunology
  • Lipopolysaccharides / immunology*
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Proteolysis
  • SKP Cullin F-Box Protein Ligases / immunology
  • SKP Cullin F-Box Protein Ligases / metabolism
  • Ubiquitin-Protein Ligases / immunology*
  • Ubiquitin-Protein Ligases / metabolism
  • Ubiquitination

Substances

  • Carrier Proteins
  • F-Box Proteins
  • FBXL2 protein, human
  • Fbxo3 protein, human
  • Inflammasomes
  • Interleukin-18
  • Interleukin-1beta
  • Lipopolysaccharides
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLRP3 protein, human
  • SKP Cullin F-Box Protein Ligases
  • Ubiquitin-Protein Ligases