A new human pyridinium metabolite of furosemide, inhibitor of mitochondrial complex I, is a candidate inducer of neurodegeneration

Biochem Pharmacol. 2019 Feb:160:14-23. doi: 10.1016/j.bcp.2018.12.007. Epub 2018 Dec 8.

Abstract

Pharmaceuticals and their by-products are increasingly a matter of concern, because of their unknown impacts on human health and ecosystems. The lack of information on these transformation products, which toxicity may exceed that of their parent molecules, makes their detection and toxicological evaluation impossible. Recently we characterized the Pyridinium of furosemide (PoF), a new transformation product of furosemide, the most widely used diuretic and an emerging pollutant. Here, we reveal PoF toxicity in SH-SY5Y cells leading to alpha-synuclein accumulation, reactive oxygen species generation, and apoptosis. We also showed that its mechanism of action is mediated through specific inhibition of striatal respiratory chain complex I, both in vitro by direct exposure of striatum mitochondria to PoF, and in vivo, in striatal mitochondria isolated from mice exposed to PoF for 7 days in drinking water and sacrificed 30 days later. Moreover, in mice, PoF induced neurodegenerative diseases hallmarks like phospho-Serine129 alpha-synuclein, tyrosine hydroxylase decrease in striatum, Tau accumulation in hippocampus. Finally, we uncovered PoF as a new metabolite of furosemide present in urine of patients treated with this drug by LC/MS. As a physiopathologically relevant neurodegeneration inducer, this new metabolite warrants further studies in the framework of public health and environment protection.

Keywords: Alpha-synuclein; Metabolite; Mitochondrial complex I; Neurodegenerative diseases; Pharmaceutical pollutant; ROS.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aged
  • Animals
  • Apoptosis / drug effects
  • Cell Line, Tumor
  • Electron Transport Complex I / antagonists & inhibitors*
  • Electron Transport Complex I / metabolism
  • Electron Transport Complex I / physiology
  • Female
  • Furosemide / metabolism
  • Furosemide / pharmacology*
  • Furosemide / urine
  • Humans
  • Male
  • Mice
  • Middle Aged
  • Mitochondria / drug effects*
  • Mitochondria / metabolism
  • Mitochondria / physiology
  • Molecular Structure
  • Nervous System / drug effects*
  • Nervous System / metabolism
  • Nervous System / physiopathology
  • Oxygen Consumption / drug effects
  • Pyridinium Compounds / chemistry
  • Pyridinium Compounds / metabolism
  • Pyridinium Compounds / pharmacology
  • Reactive Oxygen Species / metabolism

Substances

  • Pyridinium Compounds
  • Reactive Oxygen Species
  • Furosemide
  • Electron Transport Complex I