Acidosis Drives the Reprogramming of Fatty Acid Metabolism in Cancer Cells through Changes in Mitochondrial and Histone Acetylation

Cell Metab. 2016 Aug 9;24(2):311-23. doi: 10.1016/j.cmet.2016.07.003.

Abstract

Bioenergetic preferences of cancer cells foster tumor acidosis that in turn leads to dramatic reduction in glycolysis and glucose-derived acetyl-coenzyme A (acetyl-CoA). Here, we show that the main source of this critical two-carbon intermediate becomes fatty acid (FA) oxidation in acidic pH-adapted cancer cells. FA-derived acetyl-CoA not only fuels the tricarboxylic acid (TCA) cycle and supports tumor cell respiration under acidosis, but also contributes to non-enzymatic mitochondrial protein hyperacetylation, thereby restraining complex I activity and ROS production. Also, while oxidative metabolism of glutamine supports the canonical TCA cycle in acidic conditions, reductive carboxylation of glutamine-derived α-ketoglutarate sustains FA synthesis. Concomitance of FA oxidation and synthesis is enabled upon sirtuin-mediated histone deacetylation and consecutive downregulation of acetyl-CoA carboxylase ACC2 making mitochondrial fatty acyl-CoA degradation compatible with cytosolic lipogenesis. Perturbations of these regulatory processes lead to tumor growth inhibitory effects further identifying FA metabolism as a critical determinant of tumor cell proliferation under acidosis.

MeSH terms

  • Acetyl Coenzyme A / metabolism
  • Acetylation
  • Acidosis / metabolism*
  • Animals
  • Cell Line, Tumor
  • Cell Proliferation
  • Cell Respiration
  • Cellular Reprogramming*
  • Electron Transport Complex I / metabolism
  • Fatty Acids / metabolism*
  • Female
  • Glutamine / metabolism
  • Histones / metabolism*
  • Humans
  • Hydrogen-Ion Concentration
  • Metabolic Networks and Pathways
  • Mice, Nude
  • Mitochondria / metabolism*
  • Models, Biological
  • Neoplasms / metabolism*
  • Neoplasms / pathology
  • Oxidation-Reduction
  • Reactive Oxygen Species / metabolism

Substances

  • Fatty Acids
  • Histones
  • Reactive Oxygen Species
  • Glutamine
  • Acetyl Coenzyme A
  • Electron Transport Complex I