In vivo HIF-mediated reductive carboxylation is regulated by citrate levels and sensitizes VHL-deficient cells to glutamine deprivation

Cell Metab. 2013 Mar 5;17(3):372-85. doi: 10.1016/j.cmet.2013.02.002.

Abstract

Hypoxic and VHL-deficient cells use glutamine to generate citrate and lipids through reductive carboxylation (RC) of α-ketoglutarate. To gain insights into the role of HIF and the molecular mechanisms underlying RC, we took advantage of a panel of disease-associated VHL mutants and showed that HIF expression is necessary and sufficient for the induction of RC in human renal cell carcinoma (RCC) cells. HIF expression drastically reduced intracellular citrate levels. Feeding VHL-deficient RCC cells with acetate or citrate or knocking down PDK-1 and ACLY restored citrate levels and suppressed RC. These data suggest that HIF-induced low intracellular citrate levels promote the reductive flux by mass action to maintain lipogenesis. Using [(1-13)C]glutamine, we demonstrated in vivo RC activity in VHL-deficient tumors growing as xenografts in mice. Lastly, HIF rendered VHL-deficient cells sensitive to glutamine deprivation in vitro, and systemic administration of glutaminase inhibitors suppressed the growth of RCC cells as mice xenografts.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / metabolism*
  • Carbon Isotopes / metabolism
  • Carboxylic Acids / metabolism
  • Carcinoma, Renal Cell / metabolism*
  • Cell Line, Tumor
  • Citrates / metabolism*
  • Extracellular Fluid / metabolism
  • Gas Chromatography-Mass Spectrometry
  • Glutamine / deficiency*
  • Humans
  • Magnetic Resonance Spectroscopy
  • Mice
  • Models, Biological
  • Oxidation-Reduction
  • Von Hippel-Lindau Tumor Suppressor Protein / metabolism*

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • Carbon Isotopes
  • Carboxylic Acids
  • Citrates
  • Glutamine
  • endothelial PAS domain-containing protein 1
  • Von Hippel-Lindau Tumor Suppressor Protein
  • VHL protein, human