Coenzyme Q biosynthesis inhibition induces HIF-1α stabilization and metabolic switch toward glycolysis

FEBS J. 2021 Mar;288(6):1956-1974. doi: 10.1111/febs.15561. Epub 2020 Sep 20.

Abstract

Coenzyme Q10 (CoQ, ubiquinone) is a redox-active lipid endogenously synthesized by the cells. The final stage of CoQ biosynthesis is performed at the mitochondrial level by the 'complex Q', where coq2 is responsible for the prenylation of the benzoquinone ring of the molecule. We report that the competitive coq2 inhibitor 4-nitrobenzoate (4-NB) decreased the cellular CoQ content and caused severe impairment of mitochondrial function in the T67 human glioma cell line. In parallel with the reduction in CoQ biosynthesis, the cholesterol level increased, leading to significant perturbation of the plasma membrane physicochemical properties. We show that 4-NB treatment did not significantly affect the cell viability, because of an adaptive metabolic rewiring toward glycolysis. Hypoxia-inducible factor 1α (HIF-1α) stabilization was detected in 4-NB-treated cells, possibly due to the contribution of both reduction in intracellular oxygen tension and ROS overproduction. Exogenous CoQ supplementation partially recovered cholesterol content, HIF-1α degradation, and ROS production, whereas only weakly improved the bioenergetic impairment induced by the CoQ depletion. Our data provide new insights on the effect of CoQ depletion and contribute to shed light on the pathogenic mechanisms of ubiquinone deficiency syndrome.

Keywords: 4-nitrobenzoate; HIF-1α; cholesterol content; coenzyme Q deficiency; coq2 inhibition; respiratory chain.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alkyl and Aryl Transferases / antagonists & inhibitors
  • Alkyl and Aryl Transferases / metabolism
  • Ataxia / metabolism
  • Cell Line, Tumor
  • Cholesterol / metabolism
  • Energy Metabolism*
  • Glycolysis*
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism*
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Mitochondrial Diseases / metabolism
  • Muscle Weakness / metabolism
  • Nitrobenzoates / pharmacology
  • Protein Stability / drug effects
  • Ubiquinone / analogs & derivatives*
  • Ubiquinone / antagonists & inhibitors
  • Ubiquinone / biosynthesis
  • Ubiquinone / deficiency
  • Ubiquinone / metabolism

Substances

  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Nitrobenzoates
  • Ubiquinone
  • Cholesterol
  • Alkyl and Aryl Transferases
  • 4-hydroxybenzoate polyprenyltransferase
  • coenzyme Q10

Supplementary concepts

  • Coenzyme Q10 Deficiency