Spatial single-cell isotope tracing reveals heterogeneity of de novo fatty acid synthesis in cancer

Nat Metab. 2024 Sep;6(9):1695-1711. doi: 10.1038/s42255-024-01118-4. Epub 2024 Sep 9.

Abstract

While heterogeneity is a key feature of cancer, understanding metabolic heterogeneity at the single-cell level remains a challenge. Here we present 13C-SpaceM, a method for spatial single-cell isotope tracing that extends the previously published SpaceM method with detection of 13C6-glucose-derived carbons in esterified fatty acids. We validated 13C-SpaceM on spatially heterogeneous models using liver cancer cells subjected to either normoxia-hypoxia or ATP citrate lyase depletion. This revealed substantial single-cell heterogeneity in labelling of the lipogenic acetyl-CoA pool and in relative fatty acid uptake versus synthesis hidden in bulk analyses. Analysing tumour-bearing brain tissue from mice fed a 13C6-glucose-containing diet, we found higher glucose-dependent synthesis of saturated fatty acids and increased elongation of essential fatty acids in tumours compared with healthy brains. Furthermore, our analysis uncovered spatial heterogeneity in lipogenic acetyl-CoA pool labelling in tumours. Our method enhances spatial probing of metabolic activities in single cells and tissues, providing insights into fatty acid metabolism in homoeostasis and disease.

MeSH terms

  • Acetyl Coenzyme A / metabolism
  • Animals
  • Carbon Isotopes
  • Cell Line, Tumor
  • Fatty Acids* / biosynthesis
  • Fatty Acids* / metabolism
  • Glucose / metabolism
  • Humans
  • Lipogenesis
  • Liver Neoplasms / metabolism
  • Mice
  • Neoplasms / metabolism
  • Single-Cell Analysis* / methods

Substances

  • Fatty Acids
  • Acetyl Coenzyme A
  • Glucose
  • Carbon Isotopes