Metabolic reprogramming ensures cancer cell survival despite oncogenic signaling blockade

Genes Dev. 2017 Oct 15;31(20):2067-2084. doi: 10.1101/gad.305292.117. Epub 2017 Nov 14.

Abstract

There is limited knowledge about the metabolic reprogramming induced by cancer therapies and how this contributes to therapeutic resistance. Here we show that although inhibition of PI3K-AKT-mTOR signaling markedly decreased glycolysis and restrained tumor growth, these signaling and metabolic restrictions triggered autophagy, which supplied the metabolites required for the maintenance of mitochondrial respiration and redox homeostasis. Specifically, we found that survival of cancer cells was critically dependent on phospholipase A2 (PLA2) to mobilize lysophospholipids and free fatty acids to sustain fatty acid oxidation and oxidative phosphorylation. Consistent with this, we observed significantly increased lipid droplets, with subsequent mobilization to mitochondria. These changes were abrogated in cells deficient for the essential autophagy gene ATG5 Accordingly, inhibition of PLA2 significantly decreased lipid droplets, decreased oxidative phosphorylation, and increased apoptosis. Together, these results describe how treatment-induced autophagy provides nutrients for cancer cell survival and identifies novel cotreatment strategies to override this survival advantage.

Keywords: autophagy; cancer; metabolism; phospholipid; resistance; signaling.

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology*
  • Apoptosis
  • Autophagy
  • Benzamides / pharmacology
  • Cell Line, Tumor
  • Cell Respiration / drug effects
  • Cell Survival
  • Heterocyclic Compounds, 3-Ring / pharmacology
  • Humans
  • Lipid Droplets / metabolism
  • Mice
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Neoplasms / enzymology
  • Neoplasms / metabolism*
  • Neoplasms / pathology
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphoinositide-3 Kinase Inhibitors
  • Phospholipase A2 Inhibitors / pharmacology
  • Phospholipids / metabolism
  • Protein Kinase Inhibitors / pharmacology
  • Proto-Oncogene Proteins c-akt / antagonists & inhibitors
  • Proto-Oncogene Proteins c-akt / metabolism
  • Pyrimidines / pharmacology
  • Signal Transduction / drug effects*
  • Tumor Cells, Cultured

Substances

  • Antineoplastic Agents
  • Benzamides
  • Heterocyclic Compounds, 3-Ring
  • MK 2206
  • Phosphoinositide-3 Kinase Inhibitors
  • Phospholipase A2 Inhibitors
  • Phospholipids
  • Protein Kinase Inhibitors
  • Pyrimidines
  • N-(cyanomethyl)-4-(2-((4-(4-morpholinyl)phenyl)amino)-4-pyrimidinyl)benzamide
  • Proto-Oncogene Proteins c-akt