Oxidation of alpha-ketoglutarate is required for reductive carboxylation in cancer cells with mitochondrial defects

Cell Rep. 2014 Jun 12;7(5):1679-1690. doi: 10.1016/j.celrep.2014.04.037. Epub 2014 May 22.

Abstract

Mammalian cells generate citrate by decarboxylating pyruvate in the mitochondria to supply the tricarboxylic acid (TCA) cycle. In contrast, hypoxia and other impairments of mitochondrial function induce an alternative pathway that produces citrate by reductively carboxylating α-ketoglutarate (AKG) via NADPH-dependent isocitrate dehydrogenase (IDH). It is unknown how cells generate reducing equivalents necessary to supply reductive carboxylation in the setting of mitochondrial impairment. Here, we identified shared metabolic features in cells using reductive carboxylation. Paradoxically, reductive carboxylation was accompanied by concomitant AKG oxidation in the TCA cycle. Inhibiting AKG oxidation decreased reducing equivalent availability and suppressed reductive carboxylation. Interrupting transfer of reducing equivalents from NADH to NADPH by nicotinamide nucleotide transhydrogenase increased NADH abundance and decreased NADPH abundance while suppressing reductive carboxylation. The data demonstrate that reductive carboxylation requires bidirectional AKG metabolism along oxidative and reductive pathways, with the oxidative pathway producing reducing equivalents used to operate IDH in reverse.

Publication types

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

MeSH terms

  • Animals
  • Cell Line
  • Cell Line, Tumor
  • Citric Acid Cycle
  • Cricetinae
  • Cricetulus
  • Fumarate Hydratase / genetics
  • Humans
  • Isocitrate Dehydrogenase / metabolism
  • Ketoglutaric Acids / metabolism*
  • Mitochondria / genetics
  • Mitochondria / metabolism*
  • Mutation
  • NAD / metabolism
  • NADP Transhydrogenase, AB-Specific / metabolism
  • Neoplasms / genetics
  • Neoplasms / metabolism*
  • Oxidation-Reduction

Substances

  • Ketoglutaric Acids
  • NAD
  • Isocitrate Dehydrogenase
  • NADP Transhydrogenase, AB-Specific
  • Fumarate Hydratase