Inhibition of the p62-Nrf2-GPX4 Pathway Confers Sensitivity to Butachlor-Induced Splenic Macrophage Ferroptosis

J Agric Food Chem. 2024 Jul 31;72(30):16998-17007. doi: 10.1021/acs.jafc.4c01086. Epub 2024 Jul 17.

Abstract

Butachlor is widely used in agriculture around the world and therefore poses environmental and public health hazards due to persistent and poor biodegradability. Ferroptosis is a type of iron-mediated cell death controlled by glutathione (GSH) and GPX4 inhibition. P62 is an essential autophagy adaptor that regulates Keap1 to activate nuclear factor erythroid 2-related factor 2 (Nrf2), which effectively suppresses lipid peroxidation, thereby relieving ferroptosis. Here, we found that butachlor caused changes in splenic macrophage structure, especially impaired mitochondrial morphology with disordered structure, which is suggestive of the occurrence of ferroptosis. This was further confirmed by the detection of iron metabolism, the GSH system, and lipid peroxidation. Mechanistically, butachlor suppressed the protein level of p62 and promoted Keap1-mediated degradation of Nrf2, which results in decreased GPX4 expression and accelerated splenic macrophage ferroptosis. These findings suggest that targeting the p62-Nrf2-GPX4 signaling axis may be a promising strategy for treating inflammatory diseases.

Keywords: Nrf2; P62; butachlor; ferroptosis; splenic macrophages.

MeSH terms

  • Animals
  • Ferroptosis* / drug effects
  • Humans
  • Kelch-Like ECH-Associated Protein 1 / genetics
  • Kelch-Like ECH-Associated Protein 1 / metabolism
  • Lipid Peroxidation / drug effects
  • Macrophages* / drug effects
  • Macrophages* / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL*
  • NF-E2-Related Factor 2* / genetics
  • NF-E2-Related Factor 2* / metabolism
  • Phospholipid Hydroperoxide Glutathione Peroxidase* / genetics
  • Phospholipid Hydroperoxide Glutathione Peroxidase* / metabolism
  • Sequestosome-1 Protein / genetics
  • Sequestosome-1 Protein / metabolism
  • Signal Transduction* / drug effects
  • Spleen* / cytology
  • Spleen* / drug effects
  • Spleen* / metabolism

Substances

  • glutathione peroxidase 4, mouse
  • Kelch-Like ECH-Associated Protein 1
  • NF-E2-Related Factor 2
  • Nfe2l2 protein, mouse
  • Phospholipid Hydroperoxide Glutathione Peroxidase
  • Sequestosome-1 Protein
  • Sqstm1 protein, mouse
  • butachlor