Singlet oxygen treatment of tumor cells triggers extracellular singlet oxygen generation, catalase inactivation and reactivation of intercellular apoptosis-inducing signaling

Redox Biol. 2015 Dec:6:157-168. doi: 10.1016/j.redox.2015.07.006. Epub 2015 Jul 17.

Abstract

Intracellular singlet oxygen generation in photofrin-loaded cells caused cell death without discrimination between nonmalignant and malignant cells. In contrast, extracellular singlet oxygen generation caused apoptosis induction selectively in tumor cells through singlet oxygen-mediated inactivation of tumor cell protective catalase and subsequent reactivation of intercellular ROS-mediated apoptosis signaling through the HOCl and the NO/peroxynitrite signaling pathway. Singlet oxygen generation by extracellular photofrin alone was, however, not sufficient for optimal direct inactivation of catalase, but needed to trigger the generation of cell-derived extracellular singlet oxygen through the interaction between H2O2 and peroxynitrite. Thereby, formation of peroxynitrous acid, generation of hydroxyl radicals and formation of perhydroxyl radicals (HO2(.)) through hydroxyl radical/H2O2 interaction seemed to be required as intermediate steps. This amplificatory mechanism led to the formation of singlet oxygen at a sufficiently high concentration for optimal inactivation of membrane-associated catalase. At low initial concentrations of singlet oxygen, an additional amplification step needed to be activated. It depended on singlet oxygen-dependent activation of the FAS receptor and caspase-8, followed by caspase-8-mediated enhancement of NOX activity. The biochemical mechanisms described here might be considered as promising principle for the development of novel approaches in tumor therapy that specifically direct membrane-associated catalase of tumor cells and thus utilize tumor cell-specific apoptosis-inducing ROS signaling.

Keywords: Catalase; Intercellular apoptosis-inducing signaling; Nitric oxide; Peroxnitrite; Photodynamic therapy; Singlet oxygen.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Apoptosis / genetics
  • Caspase 8 / genetics
  • Caspase 8 / metabolism
  • Catalase / antagonists & inhibitors*
  • Catalase / metabolism
  • Cell Line
  • Cell Line, Tumor
  • Dihematoporphyrin Ether / pharmacology*
  • Enzyme Inhibitors / pharmacology
  • Fibroblasts / cytology
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Gene Expression Regulation, Neoplastic*
  • Humans
  • Hydrogen Peroxide / pharmacology
  • Hypochlorous Acid / metabolism
  • Light
  • Metalloporphyrins / pharmacology
  • Mice
  • NADPH Oxidases / genetics
  • NADPH Oxidases / metabolism
  • Nitric Oxide / metabolism
  • Peroxynitrous Acid / metabolism
  • Photosensitizing Agents / pharmacology*
  • Signal Transduction*
  • Singlet Oxygen / metabolism
  • Singlet Oxygen / pharmacology*
  • Sulfones / pharmacology
  • Taurine / pharmacology
  • fas Receptor / genetics
  • fas Receptor / metabolism

Substances

  • 5,10,15,20-tetrakis(4-sulfonatophenyl)porphyrinato iron(III) chloride
  • Enzyme Inhibitors
  • Metalloporphyrins
  • Photosensitizing Agents
  • Sulfones
  • fas Receptor
  • Peroxynitrous Acid
  • Singlet Oxygen
  • Taurine
  • Nitric Oxide
  • 4-(2-aminoethyl)benzenesulfonylfluoride
  • Hypochlorous Acid
  • Dihematoporphyrin Ether
  • Hydrogen Peroxide
  • Catalase
  • NADPH Oxidases
  • CASP8 protein, human
  • Caspase 8