Caspase-2 kills cells with extra centrosomes

Sci Adv. 2024 Nov;10(44):eado6607. doi: 10.1126/sciadv.ado6607. Epub 2024 Oct 30.

Abstract

Centrosomes are membrane-less organelles that orchestrate a wide array of biological functions by acting as microtubule organizing centers. Here, we report that caspase-2-driven apoptosis is elicited in blood cells failing cytokinesis and that extra centrosomes are necessary to trigger this cell death. Activation of caspase-2 depends on the PIDDosome multi-protein complex, and priming of PIDD1 at extra centrosomes is necessary for pathway activation. Accordingly, loss of its centrosomal adapter, ANKRD26, allows for cell survival and unrestricted polyploidization in response to cytokinesis failure. Mechanistically, cell death is initiated upstream of mitochondria via caspase-2-mediated processing of the BCL2 family protein BID, driving BAX/BAK-dependent mitochondrial outer membrane permeabilization (MOMP). Remarkably, BID-deficient cells enforce apoptosis by engaging p53-dependent proapoptotic transcriptional responses initiated by caspase-2. Consistently, BID and MDM2 act as shared caspase-2 substrates, with BID being kinetically favored. Our findings document that the centrosome limits its own unscheduled duplication by the induction of PIDDosome-driven mitochondrial apoptosis to avoid potentially pathogenic polyploidization events.

MeSH terms

  • Apoptosis*
  • BH3 Interacting Domain Death Agonist Protein* / genetics
  • BH3 Interacting Domain Death Agonist Protein* / metabolism
  • Caspase 2* / genetics
  • Caspase 2* / metabolism
  • Centrosome* / metabolism
  • Cysteine Endopeptidases
  • Death Domain Receptor Signaling Adaptor Proteins* / genetics
  • Death Domain Receptor Signaling Adaptor Proteins* / metabolism
  • Humans
  • Mitochondria* / metabolism
  • Mitochondrial Membranes / metabolism
  • Proto-Oncogene Proteins c-mdm2 / genetics
  • Proto-Oncogene Proteins c-mdm2 / metabolism
  • Tumor Suppressor Protein p53 / genetics
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Caspase 2
  • BH3 Interacting Domain Death Agonist Protein
  • Death Domain Receptor Signaling Adaptor Proteins
  • PIDD1 protein, human
  • CASP2 protein, human
  • Proto-Oncogene Proteins c-mdm2
  • Tumor Suppressor Protein p53
  • BID protein, human
  • MDM2 protein, human
  • Cysteine Endopeptidases