Oxidative stress is involved in the permeabilization of the inner membrane of brain mitochondria exposed to hypoxia/reoxygenation and low micromolar Ca2+

FEBS Journal

Volumn 272, Issue 14, 2005, Pages 3593-3601

  Schild, Lorenz ^a,b   Reiser, Georg ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

^b Inst fur Klin Chem Pathobiochemie   (Germany)

Author keywords

Brain mitochondria; Hypoxia, calcium; Membrane permeabilization; Oxidative stress

Indexed keywords

CALCIUM ION; CYTOCHROME C; GLUCOSE; GLUTATHIONE; HYDROGEN PEROXIDE; OXYGEN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; TEMPOL;

AMINO ACID BRAIN LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN METABOLISM; BRAIN MITOCHONDRION; CELL DEATH; CONTROLLED STUDY; HYPOXIA; MEMBRANE PERMEABILITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN SECRETION; RAT; REOXYGENATION;

ANIMALS; BRAIN; CALCIUM; CELL HYPOXIA; CELL MEMBRANE PERMEABILITY; CYCLIC N-OXIDES; GLUTATHIONE; HYDROGEN PEROXIDE; INTRACELLULAR MEMBRANES; MALE; MITOCHONDRIA; NAD; OXIDATIVE STRESS; OXYGEN; RATS; RATS, WISTAR; SPIN LABELS;

EID: 22544480783     PISSN: 1742464X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2005.04781.x     Document Type: Article

References (52)

1. Beal MF (1998) Mitochondrial dysfunction in neurodegenerative diseases. Biochim Biophys Acta 1366, 211-223.
2. Halliwell B (1992) Reactive oxygen species and the central nervous system. J Neurochem 59, 1609-1623.
3. Morita-Fujimura Y, Fujimura M, Kawase M, Chen SF & Chan PH (1999) Release of mitochondrial cytochrome c and DNA fragmentation after cold injury-induced brain trauma in mice: possible role in neuronal apoptosis. Neurosci Lett 267, 201-205.
4. Noshita N, Sugawara T, Fujimura M, Morita-Fujimura Y & Chan PH (2001) Manganese superoxide dismutase affects cytochrome c release and caspase-9 activation after transient focal cerebral ischemia in mice. J Cereb Blood Flow Metab 21, 557-567.
5. Hall ED (1995) Inhibition of lipid peroxidation in central nervous system trauma and ischemia. J Neurol Sci 134 (Suppl.), 79-83.
6. Yu ZF, Bruce-Keller AJ, Goodman Y & Mattson MP (1998) Uric acid protects neurons against excitotoxic and metabolic insults in cell culture, and against focal ischemic brain injury in vivo. J Neurosci Res 53, 613-625.
7. Anderson MF & Sims NR (1999) Mitochondrial respiratory function and cell death in focal cerebral ischemia. J Neurochem 73, 1189-1199.
8. Sims NR & Anderson MF (2002) Mitochondrial contributions to tissue damage in stroke. Neurochem Int 40, 511-526.
9. Solenski NJ, diPierro CG, Trimmer PA, Kwan AL & Helms GA (2002) Ultrastructural changes of neuronal mitochondria after transient and permanent cerebral ischemia. Stroke 33, 816-824.
10. Namura S, Nagata I, Takami S, Masayasu H & Kikuchi H (2001) Ebselen reduces cytochrome c release from mitochondria and subsequent DNA fragmentation after transient focal cerebral ischemia in mice. Stroke 32, 1906-1911.
11. Sugawara T, Noshita N, Lewen A, Gasche Y, Ferrand-Drake M, Fujimura M, Morita-Fujimura Y & Chan PH (2002) Overexpression of copper/zinc superoxide dismutase in transgenic rats protects vulnerable neurons against ischemic damage by blocking the mitochondrial pathway of caspase activation. J Neurosci 22, 209-217.
12. Wiswedel I, Hirsch D, Nourooz-Zadeh J, Flechsig A, Luck-Lambrecht A & Augustin W (2002) Analysis of monohydroxyeicosatetraenoic acids and F2-isoprostanes as markers of lipid peroxidation in rat brain mitochondria. Free Radic Res 36, 1-11.
13. Cadenas E, Boveris A, Ragan CI & Stoppani AO (1977) Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria. Arch Biochem Biophys 180, 248-257.
14. Turrens JF & Boveris A (1980) Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem J 191, 421-427.
15. Korshunov SS, Skulachev VP & Starkov AA (1997) High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416, 15-18.
16. 2 production in pigeon heart mitochondria. FEBS Lett 18, 261-264.
17. Meldrum BS (1986) Cell damage in epilepsy and the role of calcium in cytotoxicity. Adv Neurol 44, 849-855.
18. Starkov AA, Chinopoulos C & Fiskum G (2004) Mitochondrial calcium and oxidative stress as mediators of ischemic brain injury. Cell Calcium 36, 257-264.
19. Du G, Mouithys-Mickalad A & Sluse FE (1998) Generation of superoxide anion by mitochondria and impairment of their functions during anoxia and reoxygenation in vitro. Free Radic Biol Med 25, 1066-1074.
20. Schild L, Reinheckel T, Wiswedel I & Augustin W (1997) Short-term impairment of energy production in isolated rat liver mitochondria by hypoxia/reoxygenation: involvement of oxidative protein modification. Biochem J 328, 205-210.
21. 2+ rise upon hypoxia/reoxygenation for functional breakdown and morphological desintegration. J Biol Chem 278, 25454-25460.
22. Rodrigues CM, Spellman SR, Sola S, Grande AW, Linehan-Stieers C, Low WC & Steer CJ (2002) Neuroprotection by a bile acid in an acute stroke model in the rat. J Cereb Blood Flow Metab 22, 463-471.
23. Fujimura M, Morita-Fujimura Y, Kawase M, Copin JC, Calagui B, Epstein CJ & Chan PH (1999) Manganese superoxide dismutase mediates the early release of mitochondrial cytochrome C and subsequent DNA fragmentation after permanent focal cerebral ischemia in mice. J Neurosci 19, 3414-3422.
24. Matsumoto S, Friberg H, Ferrand-Drake M & Wieloch T (1999) Blockade of the mitochondrial permeability transition pore diminishes infarct size in the rat after transient middle cerebral artery occlusion. J Cereb Blood Flow Metab 19, 736-741.
25. Kim GW, Kondo T, Noshita N & Chan PH (2002) Manganese superoxide dismutase deficiency exacerbates cerebral infarction after focal cerebral ischemia/reperfusion in mice: implications for the production and role of superoxide radicals. Stroke 33, 809-815.
26. Murakami K, Kondo T, Kawase M, Li Y, Sato S, Chen SF & Chan PH (1998) Mitochondrial susceptibility to oxidative stress exacerbates cerebral infarction that follows permanent focal cerebral ischemia in mutant mice with manganese superoxide dismutase deficiency. J Neurosci 18, 205-213.
27. Mackensen GB, Patel M, Sheng H, Calvi CL, Batinic-Haberle I, Day BJ, Liang LP, Fridovich I, Crapo JD, Pearlstein RD & Warner DS (2001) Neuroprotection from delayed postischemic administration of a metalloporphyrin catalytic antioxidant. J Neurosci 21, 4582-4592.
28. Forsman M, Fleischer JE, Milde JH, Steen PA & Michenfelder JD (1988) Superoxide dismutase and catalase failed to improve neurologic outcome after complete cerebral ischemia in the dog. Acta Anaesthesiol Scand 32, 152-155.
29. Matsumiya N, Koehler RC, Kirsch JR & Traystman RJ (1991) Conjugated superoxide dismutase reduces extent of caudate injury after transient focal ischemia in cats. Stroke 22, 1193-1200.
30. Muizelaar JP, Marmarou A, Young HF, Choi SC, Wolf A, Schneider RL & Kontos HA (1993) Improving the outcome of severe head injury with the oxygen radical scavenger polyethylene glycol-conjugated superoxide dismutase: a phase II trial. J Neurosurg 78, 375-382.
31. Uyama O, Matsuyama T, Michishita H, Nakamura H & Sugita M (1992) Protective effects of human recombinant superoxide dismutase on transient ischemic injury of CA1 neurons in gerbils. Stroke 23, 75-81.
32. Kim DY, Won SJ & Gwag BJ (2002) Analysis of mitochondrial free radical generation in animal models of neuronal disease. Free Radic Biol Med 33, 715-723.
33. Cino M & Del Maestro RF (1989) Generation of hydrogen peroxide by brain mitochondria: the effect of reoxygenation following postdecapitative ischemia. Arch Biochem Biophys 269, 623-638.
34. Barja G & Herrero A (1998) Localization at complex I and mechanism of the higher free radical production of brain nonsynaptic mitochondria in the short-lived rat than in the longevous pigeon. J Bioenerg Biomembr 30, 235-243.
35. Kwong LK & Sohal RS (1998) Substrate and site specificity of hydrogen peroxide generation in mouse mitochondria. Arch Biochem Biophys 350, 118-126.
36. Novgorodov SA, Gudz TI, Milgrom YM & Brierley GP (1992) The permeability transition in heart mitochondria is regulated synergistically by ADP and cyclosporin A. J Biol Chem 267, 16274-16282.
37. 2 production from mitochondrial respiratory chain. Biochem Biophys Res Commun 281, 645-650.
38. m-Dependent and -independent production of reactive oxygen species by rat brain mitochondria. J Neurochem 79, 266-277.
39. Haworth RA & Hunter DR (1980) Allosteric inhibition of the Ca2+-activated hydrophilic channel of the mitochondrial inner membrane by nucleotides. J Membr Biol 54, 231-236.
40. Zoratti M & Szabo I (1995) The mitochondrial permeability transition. Biochim Biophys Acta 1241, 139-176.
41. Chinopoulos C, Starkov AA & Fiskum G (2003) Cyclosporin A-insensitive permeability transition in brain mitochondria: inhibition by 2-aminoethoxydiphenyl borate. J Biol Chem 278, 27382-27389.
42. 2+ thresholds determine cytochrome c release or permeability transition pore opening in brain mitochondria. FASEB J 15, 565-567.
43. Brustovetsky N & Dubinsky JM (2000) Limitations of cyclosporin A inhibition of the permeability transition in CNS mitochondria. J Neurosci 20, 8229-8237.
44. 2 in brain mitochondria. J Neurochem 47, 1-8.
45. 2+ overload. Eur J Biochem 178, 489-501.
46. Schild L, Westphal S, Scheithauer S, Holfeld M, Augustin W & Sabel BA (1996) Isolation of functionally intact pig retina mitochondria. Acta Ophthalmol Scand 74, 354-357.
47. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
48. Fabiato A & Fabiato F (1979) Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells. J Physiol (Paris) 75, 463-505.
49. 2 solubility in aqueous media determined by a kinetic method. Anal Biochem 145, 406-418.
50. Ghafourifar P, Schenk U, Klein SD & Richter C (1999) Mitochondrial nitric-oxide synthase stimulation causes cytochrome c release from isolated mitochondria. Evidence for intramitochondrial peroxynitrite formation. J Biol Chem 274, 31185-31188.
51. Black MJ & Brandt RB (1974) Spectrofluorometric analysis of hydrogen peroxide. Anal Biochem 58, 246-254.
52. Baker MA, Cerniglia GJ & Zaman A (1990) Microtiter plate assay for the measurement of glutathione and glutathione disulfide in large numbers of biological samples. Anal Biochem 190, 360-365.