Activation of lysosomal Ca2+ channels mitigates mitochondrial damage and oxidative stress

J Cell Biol. 2025 Jan 6;224(1):e202403104. doi: 10.1083/jcb.202403104. Epub 2024 Nov 5.

Abstract

Elevated levels of plasma-free fatty acids and oxidative stress have been identified as putative primary pathogenic factors in endothelial dysfunction etiology, though their roles are unclear. In human endothelial cells, we found that saturated fatty acids (SFAs)-including the plasma-predominant palmitic acid (PA)-cause mitochondrial fragmentation and elevation of intracellular reactive oxygen species (ROS) levels. TRPML1 is a lysosomal ROS-sensitive Ca2+ channel that regulates lysosomal trafficking and biogenesis. Small-molecule agonists of TRPML1 prevented PA-induced mitochondrial damage and ROS elevation through activation of transcriptional factor EB (TFEB), which boosts lysosome biogenesis and mitophagy. Whereas genetically silencing TRPML1 abolished the protective effects of TRPML1 agonism, TRPML1 overexpression conferred a full resistance to PA-induced oxidative damage. Pharmacologically activating the TRPML1-TFEB pathway was sufficient to restore mitochondrial and redox homeostasis in SFA-damaged endothelial cells. The present results suggest that lysosome activation represents a viable strategy for alleviating oxidative damage, a common pathogenic mechanism of metabolic and age-related diseases.

MeSH terms

  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors* / genetics
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors* / metabolism
  • Calcium / metabolism
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism
  • Endothelial Cells / pathology
  • Human Umbilical Vein Endothelial Cells / metabolism
  • Humans
  • Lysosomes* / drug effects
  • Lysosomes* / metabolism
  • Mitochondria* / drug effects
  • Mitochondria* / metabolism
  • Mitochondria* / pathology
  • Mitophagy / drug effects
  • Oxidative Stress* / drug effects
  • Palmitic Acid* / pharmacology
  • Reactive Oxygen Species* / metabolism
  • Transient Receptor Potential Channels* / genetics
  • Transient Receptor Potential Channels* / metabolism

Substances

  • Reactive Oxygen Species
  • MCOLN1 protein, human
  • Transient Receptor Potential Channels
  • Palmitic Acid
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • TFEB protein, human
  • Calcium