Stimulation of cholesterol biosynthesis in mitochondrial complex I-deficiency lowers reductive stress and improves motor function and survival in mice

Biochim Biophys Acta Mol Basis Dis. 2021 Apr 1;1867(4):166062. doi: 10.1016/j.bbadis.2020.166062. Epub 2021 Jan 13.

Abstract

The majority of cellular energy is produced by the mitochondrial oxidative phosphorylation (OXPHOS) system. Failure of the first OXPHOS enzyme complex, NADH:ubiquinone oxidoreductase or complex I (CI), is associated with multiple signs and symptoms presenting at variable ages of onset. There is no approved drug treatment yet to slow or reverse the progression of CI-deficient disorders. Here, we present a comprehensive human metabolic network model of genetically characterized CI-deficient patient-derived fibroblasts. Model calculations predicted that increased cholesterol production, export, and utilization can counterbalance the surplus of reducing equivalents in patient-derived fibroblasts, as these pathways consume considerable amounts of NAD(P)H. We show that fibrates attenuated increased NAD(P)H levels and improved CI-deficient fibroblast growth by stimulating the production of cholesterol via enhancement of its cellular efflux. In CI-deficient (Ndufs4-/-) mice, fibrate treatment resulted in prolonged survival and improved motor function, which was accompanied by an increased cholesterol efflux from peritoneal macrophages. Our results shine a new light on the use of compensatory biological pathways in mitochondrial dysfunction, which may lead to novel therapeutic interventions for mitochondrial diseases for which currently no cure exists.

Keywords: Cholesterol biosynthesis; Complex I deficiency; Leigh syndrome; Metabolic network modeling; NAD(P)H; Ndufs4(−/−) mice.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biosynthetic Pathways / drug effects*
  • Cholesterol / genetics
  • Cholesterol / metabolism*
  • Electron Transport Complex I / deficiency*
  • Electron Transport Complex I / drug effects
  • Electron Transport Complex I / genetics
  • Electron Transport Complex I / metabolism
  • Female
  • Fibric Acids / therapeutic use*
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mitochondrial Diseases / genetics
  • Mitochondrial Diseases / metabolism*
  • Mitochondrial Diseases / physiopathology
  • Motor Activity / drug effects
  • NADP / metabolism
  • Oxidation-Reduction / drug effects

Substances

  • Fibric Acids
  • NADP
  • Cholesterol
  • Electron Transport Complex I

Supplementary concepts

  • Mitochondrial complex I deficiency