Acid-exposed and hypoxic cancer cells do not overlap but are interdependent for unsaturated fatty acid resources

Nat Commun. 2024 Nov 21;15(1):10107. doi: 10.1038/s41467-024-54435-3.

Abstract

Cancer cells in acidic tumor regions are aggressive and a key therapeutic target, but distinguishing between acid-exposed and hypoxic cells is challenging. Here, we use carbonic anhydrase 9 (CA9) antibodies to mark acidic areas in both hypoxic and respiring tumor areas, along with an HRE-GFP reporter for hypoxia, to isolate distinct cell populations from 3D tumor spheroids. Transcriptomic analysis of CA9-positive, hypoxia-negative cells highlights enriched fatty acid desaturase activity. Inhibiting or silencing stearoyl-CoA desaturase-1 (SCD1) induces ferroptosis in CA9-positive acidic cancer cells and delays mouse tumor growth, an effect enhanced by omega-3 fatty acid supplementation. Using acid-exposed cancer cells and patient-derived tumor organoids, we show that SCD1 inhibition increases acidic cancer cell reliance on external mono-unsaturated fatty acids, depriving hypoxic cells of essential resources. This bystander effect provides unbiased evidence for a lack of full overlap between hypoxic and acidic tumor compartments, highlighting a rationale for targeting desaturase activity in cancer.

MeSH terms

  • Animals
  • Antigens, Neoplasm
  • Carbonic Anhydrase IX* / genetics
  • Carbonic Anhydrase IX* / metabolism
  • Cell Hypoxia / drug effects
  • Cell Line, Tumor
  • Fatty Acids, Omega-3 / metabolism
  • Fatty Acids, Omega-3 / pharmacology
  • Fatty Acids, Unsaturated* / metabolism
  • Fatty Acids, Unsaturated* / pharmacology
  • Female
  • Ferroptosis* / drug effects
  • Humans
  • Mice
  • Neoplasms / drug therapy
  • Neoplasms / genetics
  • Neoplasms / metabolism
  • Neoplasms / pathology
  • Organoids / drug effects
  • Organoids / metabolism
  • Spheroids, Cellular / drug effects
  • Spheroids, Cellular / metabolism
  • Spheroids, Cellular / pathology
  • Stearoyl-CoA Desaturase* / genetics
  • Stearoyl-CoA Desaturase* / metabolism

Substances

  • Stearoyl-CoA Desaturase
  • Fatty Acids, Unsaturated
  • Carbonic Anhydrase IX
  • SCD1 protein, human
  • CA9 protein, human
  • Fatty Acids, Omega-3
  • Antigens, Neoplasm