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PMID: 14570403 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The production of reactive oxygen species in intact isolated nerve terminals is independent of the mitochondrial membrane potential.

Neurochemical research ·Vol. 28 ·No. 10 ·2003-10-00 ·Pages 1575-81

Sipos I, Tretter L, Adam-Vizi V

Abstract

Dependence on mitochondrial membrane potential (deltapsim) of hydrogen peroxide formation of in situ mitochondria in response to inhibition of complex I or III was studied in synaptosomes. Blockage of electron flow through complex I by rotenone or that through complex III by antimycin resulted in an increase in the rate of H2O2 generation as measured with the Amplex red assay. Membrane potential of mitochondria was dissipated by either FCCP (250 nM) or DNP (50 microM) and then the rate of H2O2 production was followed. Neither of the uncouplers had a significant effect on the rate of H2O2 production induced by rotenone or antimycin. Inhibition of the F0F1-ATPase by oligomycin, which also eliminates deltapsim in the presence of rotenone and antimycin, respectively, was also without effect on the ROS formation induced by rotenone and only slightly reduced the antimycin-induced H2O2 production. These results indicate that ROS generation of in situ mitochondria in nerve terminals in response to inhibition of complex I or complex III is independent of deltapsim. In addition, we detected a significant antimycin-induced H2O2 production when the flow of electrons through complex I was inhibited by rotenone, indicating that the respiratory chain of in situ mitochondria in synaptosomes has a substantial electron influx distal from the rotenone site, which could contribute to ROS generation when the complex III is inhibited.

MeSH Terms
Animals Antimycin A/analogs & derivatives,pharmacology Electron Transport Complex I/antagonists & inhibitors Electron Transport Complex III/antagonists & inhibitors Guinea Pigs Hydrogen Peroxide/metabolism In Vitro Techniques Membrane Potentials Mitochondria/physiology Mitochondrial Proton-Translocating ATPases/antagonists & inhibitors Oligomycins/pharmacology Reactive Oxygen Species/metabolism Rotenone/pharmacology Synaptosomes/metabolism
Chemicals
Oligomycins Reactive Oxygen Species Rotenone antimycin Antimycin A Hydrogen Peroxide Mitochondrial Proton-Translocating ATPases Electron Transport Complex I Electron Transport Complex III
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Sipos Ildiko
Neurochemical Group of MTA-SOTE EKSZ, Budapest, Hungary.
Tretter Laszlo
Adam-Vizi Vera
References (36)
36 references, click to expand
  1. Failure to maintain glycolysis in anoxic nerve terminals.
    J Neurochem. 1986 Dec;47(6):1864-9 PMID: 3095495
  2. Mitochondria, calcium regulation, and acute glutamate excitotoxicity in cultured cerebellar granule cells.
    J Neurochem. 1996 Dec;67(6):2282-91 PMID: 8931459
  3. Mechanisms of oxidant-mediated cell injury. The glycolytic and mitochondrial pathways of ADP phosphorylation are major intracellular targets inactivated by hydrogen peroxide.
    J Biol Chem. 1988 Feb 5;263(4):1665-75 PMID: 3338986
  4. Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria.
    Arch Biochem Biophys. 1985 Mar;237(2):408-14 PMID: 2983613
  5. Dependence of H2O2 formation by rat heart mitochondria on substrate availability and donor age.
    J Bioenerg Biomembr. 1997 Feb;29(1):89-95 PMID: 9067806
  6. Glutamate-induced destabilization of intracellular calcium concentration homeostasis in cultured cerebellar granule cells: role of mitochondria in calcium buffering.
    Mol Pharmacol. 1995 Jan;47(1):140-7 PMID: 7838122
  7. Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure.
    J Neurosci. 1996 Sep 15;16(18):5688-97 PMID: 8795624
  8. Role of desensitization of AMPA receptors on the neuronal viability and on the [Ca2+]i changes in cultured rat hippocampal neurons.
    Eur J Neurosci. 2000 Jun;12(6):2021-31 PMID: 10886341
  9. Depolarization of in situ mitochondria due to hydrogen peroxide-induced oxidative stress in nerve terminals: inhibition of alpha-ketoglutarate dehydrogenase.
    J Neurochem. 1999 Jul;73(1):220-8 PMID: 10386974
  10. NMDA-dependent superoxide production and neurotoxicity.
    Nature. 1993 Aug 5;364(6437):535-7 PMID: 7687749
  11. Brain cytochrome oxidase in Alzheimer's disease.
    J Neurochem. 1992 Aug;59(2):776-9 PMID: 1321237
  12. Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria.
    Arch Biochem Biophys. 1977 Apr 30;180(2):248-57 PMID: 195520
  13. A highly sensitive fluorescent micro-assay of H2O2 release from activated human leukocytes using a dihydroxyphenoxazine derivative.
    J Immunol Methods. 1997 Mar 28;202(2):133-41 PMID: 9107302
  14. Superoxide radical and iron modulate aconitase activity in mammalian cells.
    J Biol Chem. 1995 Jun 2;270(22):13399-405 PMID: 7768942
  15. Generation of reactive oxygen species by the mitochondrial electron transport chain.
    J Neurochem. 2002 Mar;80(5):780-7 PMID: 11948241
  16. Mitochondria deficient in complex I activity are depolarized by hydrogen peroxide in nerve terminals: relevance to Parkinson's disease.
    J Neurochem. 2001 Jan;76(1):302-6 PMID: 11146003
  17. Requirement for superoxide in excitotoxic cell death.
    Neuron. 1996 Feb;16(2):345-55 PMID: 8789949
  18. Mitochondrial dysfunction in neurodegenerative diseases.
    Biochim Biophys Acta. 1998 Aug 10;1366(1-2):211-23 PMID: 9714810
  19. High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria.
    FEBS Lett. 1997 Oct 13;416(1):15-8 PMID: 9369223
  20. Regulation of hydrogen peroxide production by brain mitochondria by calcium and Bax.
    J Neurochem. 2002 Oct;83(1):220-8 PMID: 12358746
  21. The cellular production of hydrogen peroxide.
    Biochem J. 1972 Jul;128(3):617-30 PMID: 4404507
  22. Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation.
    J Neurosci. 1995 May;15(5 Pt 1):3318-27 PMID: 7751912
  23. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen.
    Biochem J. 1973 Jul;134(3):707-16 PMID: 4749271
  24. Energy transduction in intact synaptosomes. Influence of plasma-membrane depolarization on the respiration and membrane potential of internal mitochondria determined in situ.
    Biochem J. 1980 Jan 15;186(1):21-33 PMID: 7370008
  25. Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate.
    J Neurosci. 1995 Oct;15(10):6377-88 PMID: 7472402
  26. Mitochondrial complex I deficiency in Parkinson's disease.
    J Neurochem. 1990 Mar;54(3):823-7 PMID: 2154550
  27. Mitochondrial H2O2 formation: relationship with energy conservation.
    FEBS Lett. 1973 Jun 15;33(1):84-7 PMID: 4737333
  28. Inhibition of Krebs cycle enzymes by hydrogen peroxide: A key role of [alpha]-ketoglutarate dehydrogenase in limiting NADH production under oxidative stress.
    J Neurosci. 2000 Dec 15;20(24):8972-9 PMID: 11124972
  29. Differential postreceptor signaling events triggered by excitotoxic stimulation of different ionotropic glutamate receptors in retinal neurons.
    J Neurosci Res. 2001 Nov 15;66(4):643-55 PMID: 11746384
  30. Mitochondria in the life and death of neurons.
    Essays Biochem. 1998;33:43-52 PMID: 10488440
  31. Quantitative relationship between inhibition of respiratory complexes and formation of reactive oxygen species in isolated nerve terminals.
    J Neurochem. 2003 Jan;84(1):112-8 PMID: 12485407
  32. Metabolic impairment induces oxidative stress, compromises inflammatory responses, and inactivates a key mitochondrial enzyme in microglia.
    J Neurochem. 1999 May;72(5):1948-58 PMID: 10217272
  33. Cyclosporin A delays mitochondrial depolarization induced by N-methyl-D-aspartate in cortical neurons: evidence of the mitochondrial permeability transition.
    Neuroscience. 1996 Dec;75(4):993-7 PMID: 8938735
  34. DeltaPsi(m)-Dependent and -independent production of reactive oxygen species by rat brain mitochondria.
    J Neurochem. 2001 Oct;79(2):266-77 PMID: 11677254
  35. The oxidative inactivation of mitochondrial electron transport chain components and ATPase.
    J Biol Chem. 1990 Sep 25;265(27):16330-6 PMID: 2168888
  36. Role of ubiquinone in the mitochondrial generation of hydrogen peroxide.
    Biochem J. 1976 May 15;156(2):435-44 PMID: 182149
Article Info
Journal
Neurochemical research
Abbr.
Neurochem Res
ISSN
0364-3190
Published
2003-10-00
Pages
1575-81
Language
English
Region
United States
NLM ID
7613461
Subset
IM
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