DDIT3 Directs a Dual Mechanism to Balance Glycolysis and Oxidative Phosphorylation during Glutamine Deprivation

Adv Sci (Weinh). 2021 Jun;8(11):e2003732. doi: 10.1002/advs.202003732. Epub 2021 Mar 27.

Abstract

Extracellular glutamine represents an important energy source for many cancer cells and its metabolism is intimately involved in maintaining redox homeostasis. The heightened metabolic activity within tumor tissues can result in glutamine deficiency, necessitating metabolic reprogramming responses. Here, dual mechanisms involving the stress-responsive transcription factor DDIT3 (DNA damage induced transcript 3) that establishes an interrelationship between glycolysis and mitochondrial respiration are revealed. DDIT3 is induced during glutamine deprivation to promote glycolysis and adenosine triphosphate production via suppression of the negative glycolytic regulator TIGAR. In concert, a proportion of the DDIT3 pool translocates to the mitochondria and suppresses oxidative phosphorylation through LONP1-mediated down-regulation of COQ9 and COX4. This in turn dampens the sustained levels of reactive oxygen species that follow glutamine withdrawal. Together these mechanisms constitute an adaptive survival mechanism permitting tumor cells to survive metabolic stress induced by glutamine starvation.

Keywords: COQ9; COX4; DDIT3/CHOP; electron transfer chain; glutamine deprivation; glycolysis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis Regulatory Proteins / genetics
  • Electron Transport Complex IV
  • Energy Metabolism / genetics
  • Gene Expression Regulation, Neoplastic / genetics
  • Glutamine / genetics*
  • Glutamine / metabolism
  • Glycolysis / genetics
  • HCT116 Cells
  • Humans
  • Mice
  • Mice, Knockout
  • Neoplasms / genetics*
  • Neoplasms / metabolism
  • Neoplasms / pathology
  • Oxidative Phosphorylation
  • Phosphoric Monoester Hydrolases / genetics
  • Transcription Factor CHOP / genetics*
  • Ubiquinone / genetics*

Substances

  • Apoptosis Regulatory Proteins
  • Glutamine
  • Ubiquinone
  • Transcription Factor CHOP
  • Cox4i1 protein, mouse
  • Electron Transport Complex IV
  • Phosphoric Monoester Hydrolases
  • TIGAR protein, mouse
  • ubiquinone 9