Ferrostatin-1 mitigates cellular damage in a ferroptosis-like environment in Caenorhabditis elegans

Toxicol Sci. 2024 Aug 1;200(2):357-368. doi: 10.1093/toxsci/kfae066.

Abstract

Although iron (Fe) is the most biologically abundant transition metal, it is highly toxic when it accumulates as Fe2+, forming a labile Fe pool and favoring the Fenton reaction. This oxidative scenario leads to a type of caspase-independent programmed cell death, referred to as ferroptosis, where following processes take place: (i) Fe2+ overload, (ii) glutathione peroxidase 4 inactivation, (iii) lipid peroxidation, and (iv) glutathione depletion. The present study sought to evaluate the consequences of Fe2+ administration on ferroptosis induction in Caenorhabditis elegans. We demonstrated higher mortality, increased lipid peroxidation, reduced glutathione peroxidase activity, and morphological damage in dopaminergic neurons upon Fe2+ overload. Pharmacological intervention at the level of lipid peroxidation with ferrostatin-1 (250 μM) mitigated the damage and returned the biochemical parameters to basal levels, revealing the potential of this therapeutical approach. Finally, to assess the relationship between ferroptosis and dopamine in a Parkinsonian background, we evaluated the UA44 worm strain which overexpresses the alpha-synuclein protein in cherry-labeled dopaminergic neurons. We demonstrated that Fe2+ administration reduced lethality associated with similar alterations in biochemical and dopaminergic morphological parameters in wild-type animals. These experiments provide mechanistic-based evidence on the efficacy of a pharmacological approach to mitigate the physiological, biochemical, and morphological consequences of Fe2+ overload. At the same time, they encourage further research on the impact of the combined effects resulting from the genetic background and dopamine signaling in a Parkinsonian phenotype.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • Caenorhabditis elegans* / drug effects
  • Cyclohexylamines* / pharmacology
  • Dopamine / metabolism
  • Dopaminergic Neurons / drug effects
  • Dopaminergic Neurons / metabolism
  • Dopaminergic Neurons / pathology
  • Ferroptosis* / drug effects
  • Glutathione Peroxidase / metabolism
  • Iron / metabolism
  • Iron / toxicity
  • Lipid Peroxidation / drug effects
  • Phenylenediamines* / pharmacology
  • Phenylenediamines* / toxicity
  • alpha-Synuclein / metabolism

Substances

  • ferrostatin-1
  • Cyclohexylamines
  • Phenylenediamines
  • Iron
  • Dopamine
  • alpha-Synuclein
  • Caenorhabditis elegans Proteins
  • Glutathione Peroxidase