Ca2+-induced permeabilization promotes free radical release from rat brain mitochondria with partially inhibited complex I

Journal of Neurochemistry

Volumn 93, Issue 3, 2005, Pages 526-537

  Votyakova, Tatyana V ^a   Reynolds, Ian J ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Ca2+; Mitochondria; Oxidative stress; Respiratory chain

Indexed keywords

ADENOSINE DIPHOSPHATE; ALAMETHICIN; CYCLOSPORIN A; CYTOCHROME C; FREE RADICAL; GLUTATHIONE; OLIGOMYCIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE; RUTHENIUM RED; CALCIUM; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ANIMAL CELL; ARTICLE; BRAIN MITOCHONDRION; CALCIUM TRANSPORT; CELL PERMEABILIZATION; MEMBRANE PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; ANIMAL; BRAIN; COMPARATIVE STUDY; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; INTRACELLULAR MEMBRANE; METABOLISM; MITOCHONDRION; PERMEABILITY; SPRAGUE DAWLEY RAT;

ANIMALS; BRAIN; CALCIUM; ELECTRON TRANSPORT COMPLEX I; FREE RADICALS; INTRACELLULAR MEMBRANES; MITOCHONDRIA; NADP; PERMEABILITY; RATS; RATS, SPRAGUE-DAWLEY; ROTENONE;

EID: 18144427184     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03042.x     Document Type: Article

References (40)

1. Akerman K. E. O. and Wikstrom M. K. F. (1976) Safranine as a probe of the mitochondrial membrane potential. FEBS Lett. 68, 191-197.
2. Beal M. F. (1996) Mitochondria, free radicals, and neurodegeneration. Curr. Opin. Neurobiol. 6, 661-666.
3. Bernardi P., Vassanelli S., Veronese P., Colonna R., Szabo I. and Zoratti M. (1992) Modulation of the mitochondrial permeability transition pore. Effect of protons and divalent cations. J. Biol. Chem. 267, 2934-2939.
4. Betarbet R., Sherer T. B., MacKenzie G., Garcia-Osuna M., Panov A. V. and Greenamyre J. T. (2000) Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 3, 1301-1306.
5. Bindokas V. P., Jordan J., Lee C. C. and Miller R. J. (1996) Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine. J. Neurosci. 16, 1324-1336.
6. Boveris A. and Chance B. (1973) The mitochondrial generation of hydrogen peroxide: general properties and effect of hyperbaric oxygen. Biochem. J. 134, 707-716.
7. Boveris A., Oshino N. and Chance B. (1972) The cellular production of hydrogen peroxide. Biochem. J. 128, 617-630.
8. Brustovetsky N. and Dubinsky J. M. (2000a) Dual responses of CNS mitochondria to elevated calcium. J. Neurosci. 20, 103-113.
9. Brustovetsky N. and Dubinsky J. M. (2000b) Limitations of cyclosporin A inhibition of the permeability transition in CNS mitochondria. J. Neurosci. 20, 8229-8237.
10. Brustovetsky N., Brustovetsky T., Jemmerson R. and Dubinsky J. M. (2002) Calcium-induced cytochrome c release from CNS mitochondria is associated with the permeability transition and rupture of the outer membrane. J. Neurochem. 80, 207-218.
11. Budd S. L. and Nicholls D. G. (1996) Mitochondria, calcium regulation and acute glutamate excitotoxicity in cultured cerebellar granule cells. J. Neurochem. 67, 2282-2291.
12. Canton M., Caffieri S., Dall'Acqua F. and Di Lisa F. (2002) PUVA-induced apoptosis involves mitochondrial dysfunction caused by the opening of the permeability transition pore. FEBS Lett. 522, 168-172.
13. Cino M. and Del Maestro R. F. (1989) Generation of hydrogen peroxide by brain mitochondria: the effect of reoxygenation following postdecapitative ischemia. Arch. Biochem. Biophys. 269, 623-638.
14. Dugan L. L., Sensi S. L., Canzoniero L. M. T., Handran S. D., Rothman S. M., Lin T.-S., Goldberg M. P. and Choi D. W. (1995) Mitochondrial production of reactive oxygen species in cortical neurons following exposure to N-methyl-D-aspartate. J. Neurosci. 15, 6377-6388.
15. +: implications for neurodegeneration. J. Neurochem. 63, 584-591.
16. Esposito L. A., Melov S., Panov A., Cottrell B. A. and Wallace D. C. (1999) Mitochondrial disease in mouse results in increased oxidative stress. Proc. Natl Acad. Sci. USA 96, 4820-4825.
17. Halliwell B. and Gutteridge J. M. C. (2000) Free radicals in biology and medicine, 3rd Edition. Oxford University Press, Oxford.
18. Korshunov S. S., Skulachev V. P. and Starkov A. A. (1997) High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett. 416, 15-18.
19. Korshunov S. S., Krasnikov B. F., Pereverzev M. O. and Skulachev V. P. (1999) The antioxidant functions of cytochrome c. FEBS Lett. 462, 192-198.
20. Kushnareva Y., Murphy A. N. and Andreyev A. (2002) Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P)+ oxidation-reduction state. Biochem. J. 368, 545-553.
21. Lafon-Cazal M., Pietri S., Culcasi M. and Bockaert J. (1993) NMDA-dependent superoxide production and neurotoxicity. Nature 364, 535-537.
22. 2+-induced membrane permeability transition in brain mitochondria. J. Neurochem. 79, 1237-1245.
23. McNaught K. S. and Jenner P. (2000) Extracellular accumulation of nitric oxide, hydrogen peroxide, and glutamate in astrocytic cultures following glutathione depletion, complex I inhibition, and/or lipopolysaccharide-induced activation. Biochem. Pharmacol. 60, 979-988.
24. Nieminen A.-L., Petrie T. G., Lemasters J. J. and Selman W. R. (1996) Cyclosporin A delays mitochondrial depolarization induced by N-methyl-D-aspartate in cortical neurons: evidence of the mitochondrial permeability transition. Neuroscience 75, 993-997.
25. Novgorodov S. A., Gudz T. I., Milgrom Y. M. and Brierley G. P. (1992) The permeability transition in heart mitochondria is regulated synergistically by ADP and cyclosporin A. J. Biol. Chem. 267, 16 274-16 282.
26. Novgorodov S. A., Gudz T. I., Brierley G. P. and Pfeiffer D. R. (1994) Magnesium ion modulates the sensitivity of the mitochondrial permeability transition pore to cyclosporin A and ADP. Arch. Biochem. Biophys. 311, 219-228.
27. Petronilli V., Nicolli A., Constanti P., Colonna R. and Bernardi P. (1994) Regulation of the permeability transition pore, a voltage dependent mitochondrial channel inhibited by cyclosporin A. Biochim. Biophys. Acta 1187, 255-259.
28. Petronilli V., Penzo D., Scorrano L., Bernardi P. and Di Lisa F. (2001) The mitochondrial permeability transition, release of cytochrome c and cell death. Correlation with the duration of pore openings in situ. J. Biol. Chem. 276, 12 030-12 034.
29. Reynolds I. J. and Hastings T. G. (1995) Glutamate induces the production of reactive oxygen species in cultured forebrain neurons following NMDA receptor activation. J. Neurosci. 15, 3318-3327.
30. Schinder A. F., Olson E. C., Spitzer N. C. and Montal M. (1996) Mitochondrial dysfunction is a primary event in glutamate neurotoxicity. J. Neurosci. 16, 6125-6133.
31. Sims N. R. (1991) Selective impairment of respiration in mitochondria isolated from brain subregions following transient forebrain ischemia in the rat. J. Neurochem. 56, 1836-1844.
32. 2+-induced oxidative stress in brain mitochondria treated with the respiratory chain inhibitor rotenone. FEBS Lett. 543, 179-183.
33. Starkov A. A., Polster B. M. and Fiskum G. (2002) Regulation of hydrogen peroxide production by brain mitochondria by calcium and Bax. J. Neurochem. 83, 220-228.
34. Stout A. K., Raphael H. M., Kanterewicz B. I., Klann E. and Reynolds I. J. (1998) Glutamate-induced neuron death requires mitochondrial calcium uptake. Nat. Neurosci. 1, 366-373.
35. Votyakova T. V. and Reynolds I. J. (2001) Δψm-dependent and independent production of reactive oxygen species by brain mitochondria. J. Neurochem. 79, 266-277.
36. 2+ in brain mitochondria free radical generation. Biophys. J. 82, 287a.
37. Votyakova T. V. and Reynolds I. J. (2004) Detection of hydrogen peroxide with Amplex Red: interference by NADH and reduced glutathione auto-oxidation. Arch. Biochem. Biophys. 431, 138-144.
38. White R. J. and Reynolds I. J. (1996) Mitochondrial depolarization in glutamate-stimulated neurons: an early signal specific to excitotoxin exposure. J. Neurosci. 16, 5688-5697.
39. 2+. J. Biol. Chem. 279, 4166-4174.
40. Zoratti M. and Szabo I. (1995) The mitochondrial permeability transition. Biochim. Biophys. Acta 1241, 139-176.