Oxidative stress triggers Ca-dependent lysosome trafficking and activation of acid sphingomyelinase

Cell Physiol Biochem. 2012;30(4):815-26. doi: 10.1159/000341460. Epub 2012 Aug 10.

Abstract

Recent studies demonstrate that rapid translocation of the acid sphingomyelinase (ASM), a lysosomal hydrolase, to the outer leaflet of the cell membrane and concomitant release of ceramide constitute a common cellular signaling cascade to various stimuli including CD95 ligation, UV-irradiation, bacterial and viral infections. Reactive oxygen species (ROS) were shown to play a crucial role in regulating this signaling cascade at least for some bacterial infections and UV-irradiation. However, the precise role of ROS for regulation of ASM is unknown. Here, by confocal microscopy and flow cytometry analysis, we demonstrate that hydrogen peroxide (H(2)O(2)), a primary form of ROS in mammalian cells, induces very rapid translocation of ASM and formation of ceramide-enriched membrane platforms in the plasma membrane of Jurkat T cells. In parallel, H(2)O(2) triggers lysosome trafficking and fusion with the plasma membrane, i.e. lysosome exocytosis, as detected by exposure of a lysosome-associated protein, LAMP1. Depletion of intracellular Ca(2+) by cell permeable EGTA-AM inhibits H(2)O(2)-induced lysosome exocytosis, ASM translocation and formation of ceramide-enriched platforms. Pharmacological inhibition or genetic deficiency of ASM did not affect H(2)O(2)-induced lysosome exocytosis. These results indicate that ROS-induced membrane translocation of ASM is mediated by exocytosis of lysosomes, which is dependent on intracellular Ca(2+) release.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Calcium / metabolism
  • Ceramides / metabolism*
  • Enzyme Activation
  • Exocytosis
  • Humans
  • Hydrogen Peroxide / metabolism*
  • Jurkat Cells
  • Lysosomal Membrane Proteins / analysis
  • Lysosomal Membrane Proteins / metabolism
  • Lysosomes / metabolism*
  • Membrane Fusion
  • Oxidative Stress*
  • Protein Transport
  • Sphingomyelin Phosphodiesterase / analysis
  • Sphingomyelin Phosphodiesterase / metabolism*

Substances

  • Ceramides
  • LAMP1 protein, human
  • Lysosomal Membrane Proteins
  • Hydrogen Peroxide
  • Sphingomyelin Phosphodiesterase
  • Calcium