The hydrophobicity of the CARD8 N-terminus tunes inflammasome activation

Cell Chem Biol. 2024 Sep 19;31(9):1699-1713.e8. doi: 10.1016/j.chembiol.2024.06.004. Epub 2024 Jul 10.

Abstract

Mounting evidence indicates that proteotoxic stress is a primary activator of the CARD8 inflammasome, but the complete array of signals that control this inflammasome have not yet been established. Notably, we recently discovered that several hydrophobic radical-trapping antioxidants (RTAs), including JSH-23, potentiate CARD8 inflammasome activation through an unknown mechanism. Here, we report that these RTAs directly alkylate several cysteine residues in the N-terminal disordered region of CARD8. These hydrophobic modifications destabilize the repressive CARD8 N-terminal fragment and accelerate its proteasome-mediated degradation, thereby releasing the inflammatory CARD8 C-terminal fragment from autoinhibition. Consistently, we also found that unrelated (non-RTA) hydrophobic electrophiles as well as genetic mutation of the CARD8 cysteine residues to isoleucines similarly potentiate inflammasome activation. Overall, our results not only provide further evidence that protein folding stress is a key CARD8 inflammasome-activating signal, but also indicate that the N-terminal cysteines can play key roles in tuning the response to this stress.

Keywords: CARD8; cysteines; degradation; hydrophobicit; inflammasome; proteasome; protein disorder; pyroptosis.

MeSH terms

  • Animals
  • Antioxidants / chemistry
  • Antioxidants / metabolism
  • Antioxidants / pharmacology
  • CARD Signaling Adaptor Proteins* / chemistry
  • CARD Signaling Adaptor Proteins* / metabolism
  • Cysteine / chemistry
  • Cysteine / metabolism
  • HEK293 Cells
  • Humans
  • Hydrophobic and Hydrophilic Interactions*
  • Inflammasomes* / metabolism
  • Mice
  • Neoplasm Proteins / chemistry
  • Neoplasm Proteins / metabolism

Substances

  • CARD Signaling Adaptor Proteins
  • Inflammasomes
  • CARD8 protein, human
  • Antioxidants
  • Cysteine
  • Neoplasm Proteins