Neurotoxic nitric oxide rapidly depolarizes and permeabilizes mitochondria by dynamically opening the mitochondrial transition pore

Mol Cell Neurosci. 2003 Aug;23(4):559-73. doi: 10.1016/s1044-7431(03)00074-5.

Abstract

Exposure of SH-SY5Y neuroblastoma or rat cortical neurons to diethylenetriamine-NO (DETA-NO) rapidly depolarized mitochondria. In SH-SY5Y DETA-NO activated caspase 3 and produced cell death. Mitochondrial depolarization in SH-SY5Y was visualized both with JC-1 accumulation and as dequenching of calcein fluorescence in mitochondria initially loaded with calcein-AM and tetramethylrhodamine methyl ester (TMRM). Calcein/TMRM-visualized mitochondrial depolarization was prevented by cyclosporin A (CsA) or approximately two-fold increased levels of BclXL protein. Dynamic imaging of mitochondrial potential (Deltapsi M) with TMRM showed that DETA-NO induced cycles of mitochondrial depolarization/repolarization ("flickering"). Fifteen-30 min of DETA-NO exposure caused high-frequency flickering with small peak size; 2 h of DETA-NO produced large peaks with prolonged depolarization. NO-induced flickering but not that from Bax was blocked by the calcium uniporter antagonist Ru360. Our findings show rapid-onset, dynamic regulation of Deltapsi M by NO, implying that neuroprotective therapies for brain ischemia target cell death processes downstream of effects of NO on mitochondria.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Brain Ischemia / drug therapy
  • Brain Ischemia / metabolism*
  • Brain Ischemia / physiopathology
  • Calcium Channels
  • Calcium-Binding Proteins / antagonists & inhibitors
  • Calcium-Binding Proteins / metabolism
  • Caspase 3
  • Caspases / drug effects
  • Caspases / metabolism
  • Cell Death / drug effects
  • Cell Death / physiology*
  • Cell Membrane Permeability / drug effects
  • Cell Membrane Permeability / physiology
  • Cyclosporine / pharmacology
  • Dose-Response Relationship, Drug
  • Fluorescent Dyes
  • Humans
  • Intracellular Membranes / drug effects
  • Intracellular Membranes / metabolism
  • Ion Channels / drug effects
  • Ion Channels / metabolism*
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Mitochondria / drug effects
  • Mitochondria / metabolism*
  • Nerve Degeneration / drug therapy
  • Nerve Degeneration / metabolism*
  • Nerve Degeneration / physiopathology
  • Neurons / drug effects
  • Neurons / metabolism*
  • Nitric Oxide / metabolism*
  • Nitric Oxide / toxicity
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Rats
  • Rhodamines / pharmacology
  • Ruthenium Compounds / pharmacology
  • Triazenes / pharmacology
  • Tumor Cells, Cultured
  • bcl-X Protein

Substances

  • 1-hydroxy-2-oxo-3,3-bis(2-aminoethyl)-1-triazene
  • BCL2L1 protein, human
  • Bcl2l1 protein, rat
  • Calcium Channels
  • Calcium-Binding Proteins
  • Fluorescent Dyes
  • Ion Channels
  • Proto-Oncogene Proteins c-bcl-2
  • Rhodamines
  • Ru 360
  • Ruthenium Compounds
  • Triazenes
  • bcl-X Protein
  • mitochondrial calcium uniporter
  • tetramethylrhodamine methyl ester
  • Nitric Oxide
  • Cyclosporine
  • CASP3 protein, human
  • Casp3 protein, rat
  • Caspase 3
  • Caspases