FLT1 activation in cancer cells promotes PARP-inhibitor resistance in breast cancer

EMBO Mol Med. 2024 Aug;16(8):1957-1980. doi: 10.1038/s44321-024-00094-2. Epub 2024 Jul 2.

Abstract

Acquired resistance to PARP inhibitors (PARPi) remains a treatment challenge for BRCA1/2-mutant breast cancer that drastically shortens patient survival. Although several resistance mechanisms have been identified, none have been successfully targeted in the clinic. Using new PARPi-resistance models of Brca1- and Bard1-mutant breast cancer generated in-vivo, we identified FLT1 (VEGFR1) as a driver of resistance. Unlike the known role of VEGF signaling in angiogenesis, we demonstrate a novel, non-canonical role for FLT1 signaling that protects cancer cells from PARPi in-vivo through a combination of cell-intrinsic and cell-extrinsic pathways. We demonstrate that FLT1 blockade suppresses AKT activation, increases tumor infiltration of CD8+ T cells, and causes dramatic regression of PARPi-resistant breast tumors in a T-cell-dependent manner. Moreover, PARPi-resistant tumor cells can be readily re-sensitized to PARPi by targeting Flt1 either genetically (Flt1-suppression) or pharmacologically (axitinib). Importantly, a retrospective series of breast cancer patients treated with PARPi demonstrated shorter progression-free survival in cases with FLT1 activation at pre-treatment. Our study therefore identifies FLT1 as a potential therapeutic target in PARPi-resistant, BRCA1/2-mutant breast cancer.

Keywords: Breast Cancer; FLT1; PARP-Inhibitor-Resistance; VEGFR1.

MeSH terms

  • Animals
  • BRCA1 Protein / genetics
  • BRCA1 Protein / metabolism
  • Breast Neoplasms* / drug therapy
  • Breast Neoplasms* / genetics
  • Breast Neoplasms* / metabolism
  • Breast Neoplasms* / pathology
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm* / genetics
  • Female
  • Humans
  • Mice
  • Poly(ADP-ribose) Polymerase Inhibitors* / pharmacology
  • Poly(ADP-ribose) Polymerase Inhibitors* / therapeutic use
  • Signal Transduction / drug effects
  • Vascular Endothelial Growth Factor Receptor-1* / genetics
  • Vascular Endothelial Growth Factor Receptor-1* / metabolism

Substances

  • Poly(ADP-ribose) Polymerase Inhibitors
  • Vascular Endothelial Growth Factor Receptor-1
  • FLT1 protein, human
  • BRCA1 Protein