SUMO1 SUMOylates and SENP3 deSUMOylates NLRP3 to orchestrate the inflammasome activation

FASEB J. 2020 Jan;34(1):1497-1515. doi: 10.1096/fj.201901653R. Epub 2019 Dec 2.

Abstract

The NLRP3 inflammasome regulates innate immune and inflammatory responses by promoting caspase1-dependent induction of pro-inflammatory cytokines. However, aberrant inflammasome activation causes diverse diseases, and thus inflammasome activity must be tightly controlled. Here, we reveal a molecular mechanism underlying the regulation of NLRP3 inflammasome. NLRP3 interacts with SUMO-conjugating enzyme (UBC9), which subsequently promotes small ubiquitin-like modifier 1 (SUMO1) to catalyze NLRP3 SUMOylation at residue Lys204. SUMO1-catalyzed SUMOylation of NLRP3 facilitates ASC oligomerization, inflammasome activation, and interleukin-1β secretion. Moreover, this study also reveals that SUMO-specific protease 3 (SENP3) is required for the deSUMOylation of NLRP3. Interestingly, SENP3 deSUMOylates NLRP3 to attenuate ASC recruitment and speck formation, the NLRP3 inflammasome activation, as well as IL-1β cleavage and secretion. In conclusion, we reveal that SUMO1-catalyzed SUMOylation and SENP3-mediated deSUMOylation of NLRP3 orchestrate the inflammasome activation.

Keywords: SUMO1‐catalyzed SUMOylation; inflammasome; innate immune response; interleukin‐1β; posttranslational modification.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cysteine Endopeptidases / genetics
  • Cysteine Endopeptidases / metabolism*
  • HEK293 Cells
  • HeLa Cells
  • Humans
  • Inflammasomes / genetics
  • Inflammasomes / metabolism*
  • Interleukin-1beta / genetics
  • Interleukin-1beta / metabolism
  • NLR Family, Pyrin Domain-Containing 3 Protein / genetics
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism*
  • SUMO-1 Protein / genetics
  • SUMO-1 Protein / metabolism*
  • Sumoylation*
  • Ubiquitin-Conjugating Enzymes / genetics
  • Ubiquitin-Conjugating Enzymes / metabolism

Substances

  • IL1B protein, human
  • Inflammasomes
  • Interleukin-1beta
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLRP3 protein, human
  • SUMO-1 Protein
  • SUMO1 protein, human
  • Ubiquitin-Conjugating Enzymes
  • Cysteine Endopeptidases
  • SENP3 protein, human
  • ubiquitin-conjugating enzyme UBC9