Blocking XIAP:CASP7-p19 selectively induces apoptosis of CASP3/DR malignancies by a novel reversible small molecule

Cell Death Dis. 2025 Jun 18;16(1):459. doi: 10.1038/s41419-025-07774-y.

Abstract

X-linked inhibitor of apoptosis (XIAP) inhibits caspases 3, 7, and 9, thereby preventing cell apoptosis. Endogenous Second mitochondria-derived activator of caspase (Smac) competes out the binding of caspases with XIAP and causes apoptosis, so that Smac mimetics are under clinical trials for anti-cancer chemotherapy. We demonstrated by selectively alkylating caspase 7 (CASP7) to release the active CASP7 for killing the drug-resistant cancer cells with accumulated XIAP:CASP7 resulted from caspase-3 down-regulation (CASP3/DR). However, finding a reversible inhibitor of the protein-protein interaction (PPI) poses a significant challenge. Here, we identified a reversible XIAP:CASP7 inhibitor, 643943, through a multiple-mode virtual screening strategy. In vitro experiments revealed that 643943 bound to CASP7, released the linker-BIR2 domain of XIAP, and activated the caspase. Removing an essential hydroxyl group on 643943 or replacing the OH-interacting Asp93 on CASP7 caused loss of 643943 cytotoxicity, revealing the binding mode. This compound thus selectively killed MCF-7 and other CASP3/DR triple-negative breast cancer cell lines, but not the cancer and normal cell lines expressing higher levels of CASP3 in vitro and in vivo. Moreover, 643943 overcame chemoresistance via down-regulating β-catenin and its associated ABC transporters in paclitaxel-resistant MCF-7 cells. Our studies not only serve as a proof-of-concept for using XIAP:CASP7 as a drug target, but also provide the first reversible XIAP:CASP7 inhibitor for cancer therapy of CASP3/DR malignancies.

MeSH terms

  • Animals
  • Antineoplastic Agents* / pharmacology
  • Apoptosis* / drug effects
  • Caspase 3* / genetics
  • Caspase 3* / metabolism
  • Caspase 7* / metabolism
  • Cell Line, Tumor
  • Female
  • Humans
  • Mice
  • Mice, Nude
  • Small Molecule Libraries* / chemistry
  • Small Molecule Libraries* / pharmacology
  • X-Linked Inhibitor of Apoptosis Protein* / antagonists & inhibitors
  • X-Linked Inhibitor of Apoptosis Protein* / metabolism

Substances

  • X-Linked Inhibitor of Apoptosis Protein
  • Caspase 3
  • Caspase 7
  • XIAP protein, human
  • Antineoplastic Agents
  • CASP3 protein, human
  • Small Molecule Libraries
  • CASP7 protein, human