NOS inhibition sensitizes metaplastic breast cancer to PI3K inhibition and taxane therapy via c-JUN repression

Nat Commun. 2024 Dec 30;15(1):10737. doi: 10.1038/s41467-024-54651-x.

Abstract

Metaplastic breast cancer (MpBC) is a highly chemoresistant subtype of breast cancer with no standardized therapy options. A clinical study in anthracycline-refractory MpBC patients suggested that nitric oxide synthase (NOS) inhibitor NG-monomethyl-l-arginine (L-NMMA) may augment anti-tumor efficacy of taxane. We report that NOS blockade potentiated response of human MpBC cell lines and tumors to phosphoinositide 3-kinase (PI3K) inhibitor alpelisib and taxane. Mechanistically, NOS blockade leads to a decrease in the S-nitrosylation of c-Jun NH2-terminal kinase (JNK)/c-Jun complex to repress its transcriptional output, leading to enhanced tumor differentiation and associated chemosensitivity. As a result, combined NOS and PI3K inhibition with taxane targets MpBC stem cells and improves survival in patient-derived xenograft models relative to single-/dual-agent therapy. Similarly, biopsies from MpBC tumors that responded to L-NMMA+taxane therapy showed a post-treatment reversal of epithelial-to-mesenchymal transition and decreased stemness. Our findings suggest that combined inhibition of iNOS and PI3K is a unique strategy to decrease chemoresistance and improve clinical outcomes in MpBC.

MeSH terms

  • Animals
  • Breast Neoplasms* / drug therapy
  • Breast Neoplasms* / genetics
  • Breast Neoplasms* / metabolism
  • Breast Neoplasms* / pathology
  • Bridged-Ring Compounds / pharmacology
  • Bridged-Ring Compounds / therapeutic use
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm / drug effects
  • Female
  • Humans
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • Metaplasia
  • Mice
  • Nitric Oxide Synthase / metabolism
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphoinositide-3 Kinase Inhibitors* / pharmacology
  • Proto-Oncogene Proteins c-jun / metabolism
  • Taxoids* / pharmacology
  • Taxoids* / therapeutic use
  • Thiazoles
  • Xenograft Model Antitumor Assays*

Substances

  • Phosphoinositide-3 Kinase Inhibitors
  • Taxoids
  • taxane
  • Bridged-Ring Compounds
  • Nitric Oxide Synthase
  • Phosphatidylinositol 3-Kinases
  • Alpelisib
  • JNK Mitogen-Activated Protein Kinases
  • Proto-Oncogene Proteins c-jun
  • Thiazoles