Breast cancer secretes anti-ferroptotic MUFAs and depends on selenoprotein synthesis for metastasis

EMBO Mol Med. 2024 Nov;16(11):2749-2774. doi: 10.1038/s44321-024-00142-x. Epub 2024 Oct 21.

Abstract

The limited availability of therapeutic options for patients with triple-negative breast cancer (TNBC) contributes to the high rate of metastatic recurrence and poor prognosis. Ferroptosis is a type of cell death caused by iron-dependent lipid peroxidation and counteracted by the antioxidant activity of the selenoprotein GPX4. Here, we show that TNBC cells secrete an anti-ferroptotic factor in the extracellular environment when cultured at high cell densities but are primed to ferroptosis when forming colonies at low density. We found that secretion of the anti-ferroptotic factors, identified as monounsaturated fatty acid (MUFA) containing lipids, and the vulnerability to ferroptosis of single cells depends on the low expression of stearyl-CoA desaturase (SCD) that is proportional to cell density. Finally, we show that the inhibition of Sec-tRNAsec biosynthesis, an essential step for selenoprotein production, causes ferroptosis and impairs the lung seeding of circulating TNBC cells that are no longer protected by the MUFA-rich environment of the primary tumour.

Keywords: Breast Cancer; Ferroptosis; Lipid Metabolism; Metastasis; Selenium Metabolism.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Female
  • Ferroptosis* / drug effects
  • Humans
  • Mice
  • Neoplasm Metastasis
  • Phospholipid Hydroperoxide Glutathione Peroxidase / genetics
  • Phospholipid Hydroperoxide Glutathione Peroxidase / metabolism
  • RNA, Transfer, Amino Acid-Specific
  • Selenoproteins* / metabolism
  • Stearoyl-CoA Desaturase / genetics
  • Stearoyl-CoA Desaturase / metabolism
  • Triple Negative Breast Neoplasms* / metabolism
  • Triple Negative Breast Neoplasms* / pathology

Substances

  • Selenoproteins
  • Stearoyl-CoA Desaturase
  • Phospholipid Hydroperoxide Glutathione Peroxidase
  • tRNA, selenocysteine-
  • RNA, Transfer, Amino Acid-Specific