NLRP1 inflammasome promotes senescence and senescence-associated secretory phenotype

Inflamm Res. 2024 Aug;73(8):1253-1266. doi: 10.1007/s00011-024-01892-7. Epub 2024 Jun 21.

Abstract

Background: Senescence is a cellular aging-related process triggered by different stresses and characterized by the secretion of various inflammatory factors referred to as senescence-associated secretory phenotype (SASP), some of which are produced by the NLRP3 inflammasome. Here, we present evidence that the NLRP1 inflammasome is a DNA damage sensor and a key mediator of senescence.

Methods: Senescence was induced in fibroblasts in vitro and in mice. Cellular senescence was assessed by Western blot analysis of several proteins, including p16, p21, p53, and SASP factors, released in the culture media or serum. Inflammasome components, including NLRP1, NLRP3 and GSDMD were knocked out or silenced using siRNAs.

Results: In vitro and in vivo results suggest that the NLRP1 inflammasome promotes senescence by regulating the expression of p16, p21, p53, and SASP factors in a Gasdermin D (GSDMD)-dependent manner. Mechanistically, the NLRP1 inflammasome is activated in response to genomic damage detected by the cytosolic DNA sensor cGMP-AMP (cGAMP) synthase (cGAS).

Conclusion: Our findings show that NLRP1 is a cGAS-dependent DNA damage sensor during senescence and a mediator of SASP release through GSDMD. This study advances the knowledge on the biology of the NLRP1 inflammasome and highlights this pathway as a potential pharmcological target to modulate senescence.

Keywords: Aging; NLRP1 inflammasome; SASP; Senescence.

MeSH terms

  • Adaptor Proteins, Signal Transducing* / genetics
  • Adaptor Proteins, Signal Transducing* / metabolism
  • Animals
  • Apoptosis Regulatory Proteins / genetics
  • Apoptosis Regulatory Proteins / metabolism
  • Cells, Cultured
  • Cellular Senescence*
  • DNA Damage*
  • Fibroblasts* / metabolism
  • Gasdermins
  • Humans
  • Inflammasomes* / metabolism
  • Intracellular Signaling Peptides and Proteins* / genetics
  • Intracellular Signaling Peptides and Proteins* / metabolism
  • Mice
  • Mice, Inbred C57BL*
  • Mice, Knockout
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLR Proteins / genetics
  • NLR Proteins / metabolism
  • Nucleotidyltransferases / genetics
  • Nucleotidyltransferases / metabolism
  • Phosphate-Binding Proteins* / genetics
  • Phosphate-Binding Proteins* / metabolism
  • Senescence-Associated Secretory Phenotype*
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Inflammasomes
  • Phosphate-Binding Proteins
  • Intracellular Signaling Peptides and Proteins
  • Adaptor Proteins, Signal Transducing
  • NALP1 protein, mouse
  • Gsdmd protein, mouse
  • Apoptosis Regulatory Proteins
  • NLR Proteins
  • Nucleotidyltransferases
  • cGAS protein, mouse
  • Tumor Suppressor Protein p53
  • Nlrp3 protein, mouse
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Gasdermins