Characteristics of α-glycerophosphate-evoked H2O 2 generation in brain mitochondria

Journal of Neurochemistry

Volumn 100, Issue 3, 2007, Pages 650-663

  Tretter, Laszlo ^a   Takacs, Katalin ^a   Hegedus, Vera ^a   Adam Vizi, Vera ^a  

^a SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

glycerophosphate; Brain mitochondria; Oxidative stress; Reactive oxygen species; Succinate

Indexed keywords

ADENOSINE DIPHOSPHATE; CITRININ; FLAVOPROTEIN; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; GLYCEROPHOSPHATE; HYDROGEN PEROXIDE; MYXOTHIAZOL; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; ROTENONE; SUCCINIC ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; CONTROLLED STUDY; ELECTRON TRANSPORT; FLUORESCENCE; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL;

ANIMALS; ANTIBIOTICS, ANTIFUNGAL; ANTIMYCIN A; BRAIN; CELL RESPIRATION; ELECTRON TRANSPORT; ELECTRON TRANSPORT COMPLEX I; ELECTRON TRANSPORT COMPLEX III; GLYCEROLPHOSPHATE DEHYDROGENASE; GLYCEROPHOSPHATES; GUINEA PIGS; HYDROGEN PEROXIDE; MEMBRANE POTENTIAL, MITOCHONDRIAL; METHACRYLATES; MITOCHONDRIA; NADP; REACTIVE OXYGEN SPECIES; SUBCELLULAR FRACTIONS; SUCCINIC ACID; THIAZOLES; UNCOUPLING AGENTS;

CAVIA; MAMMALIA;

EID: 33846188870     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04223.x     Document Type: Article

References (64)

1. Adam-Vizi V. (2005) Production of reactive oxygen species in brain mitochondria: contribution by electron transport chain and non-electron transport chain sources. Antiox. Redox Signal 7, 1140-1149.
2. Andreyev A. Y., Kushnareva Y. E. and Starkov A. A. (2005) Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc.) 70, 200-214.
3. Atlante A., Calissano P., Bobba A., Giannattasio S., Marra E. and Passarella S. (2001) Glutamate neurotoxicity, oxidative stress and mitochondria. FEBS Lett. 497, 1-5.
4. Atlante A., de Bari L., Bobba A., Marra E., Calissano P. and Passarella S. (2003) Cytochrome c, released from cerebellar granule cells undergoing apoptosis or excytotoxic death, can generate proton-motive force and drive ATP synthesis in isolated mitochondria. J. Neurochem. 86, 591-604.
5. Barja G. (1999) Mitochondrial oxygen radical generation and leak: sites of production in states 4 and 3, organ specificity, and relation to aging and longevity. J. Bioenerg. Biomembr. 31, 347-366.
6. Beal M. F. (2005) Mitochondria take center stage in aging and neurodegeneration. Ann. Neurol. 58, 495-505.
7. Bolter C. J. and Chefurka W. (1990) Extramitochondrial release of hydrogen peroxide from insect and mouse liver mitochondria using the respiratory inhibitors phosphine, myxothiazol, and antimycin and spectral analysis of inhibited cytochromes. Arch. Biochem. Biophys. 278, 65-72.
8. Boveris A. and Chance B. (1973) The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem. J. 134, 707-716.
9. Brookes P. S. (2005) Mitochondrial H (+) leak and ROS generation: an odd couple. Free Radic. Biol. Med. 38, 12-23.
10. Bunik V. I. and Sievers C. (2002) Inactivation of the 2-oxo acid dehydrogenase complexes upon generation of intrinsic radical species. Eur. J. Biochem. 269, 5004-5015.
11. Cadenas E. and Boveris A. (1980) Enhancement of hydrogen peroxide formation by protophores and ionophores in antimycin-supplemented mitochondria. Biochem. J. 188, 31-37.
12. Cadenas E., Boveris A., Ragan C. I. and Stoppani A. O. (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.
13. Chinopoulos C. and Adam-Vizi V. (2006) Calcium, mitochondria and oxidative stress in neuronal pathology. Novel aspects of an enduring theme. FEBS J. 273, 433-450.
14. Chowdhury S. K., Gemin A. and Singh G. (2005) High activity of mitochondrial glycerophosphate dehydrogenase and glycerophosphate-dependent ROS production in prostate cancer cell lines. Biochem. Biophys. Res. Commun. 333, 1139-1145.
15. 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.
16. Crofts A. R., Barquera B., Gennis R. B., Kuras R., Guergova-Kuras M. and Berry E. A. (1999) Mechanism of ubiquinol oxidation by the bc (1) complex: different domains of the quinol binding pocket and their role in the mechanism and binding of inhibitors. Biochemistry 38, 15 807-15 826.
17. Davey G. P., Peuchen S. and Clark J. B. (1998) Energy thresholds in brain mitochondria. Potential involvement in neurodegeneration. J. Biol. Chem. 273, 12 753-12 757.
18. Drahota Z., Chowdhury S. K., Floryk D., Mracek T., Wilhelm J., Rauchova H., Lenaz G. and Houstek J. (2002) Glycerophosphate-dependent hydrogen peroxide production by brown adipose tissue mitochondria and its activation by ferricyanide. J. Bioenerg. Biomembr. 34, 105-113.
19. Fiskum G. (2000) Mitochondrial participation in ischemic and traumatic neural cell death. J. Neurotrauma 17, 843-855.
20. Gyulkhandanyan A. V. and Pennefather P. S. (2004) Shift in the localization of sites of hydrogen peroxide production in brain mitochondria by mitochondrial stress. J. Neurochem. 90, 405-421.
21. Halliwell B. and Gutteridge J. M. C. (1998) Ch. 9. Free radicals, other reactive species and disease, in Free Radicals in Biology and Medicine (Halliwell B. and Gutteridge J. M. C., eds.), pp. 617-784. Oxford Science Publications, Oxford.
22. Hansford R. G., Hogue B. A. and Mildaziene V. (1997) Dependence of H2O2 formation by rat heart mitochondria on substrate availability and donor age. J. Bioenerg. Biomembr. 29, 89-95.
23. Herrero A. and Barja G. (1999) 8-oxo-deoxyguanosine levels in heart and brain mitochondrial and nuclear DNA of two mammals and three birds in relation to their different rates of aging. Aging (Milano) 11, 294-300.
24. Hinkle P. C., Butow R. A., Racker E. and Chance B. (1967) Partial resolution of the enzymes catalyzing oxidative phosphorylation. XV. Reverse electron transfer in the flavin-cytochrome beta region of the respiratory chain of beef heart submitochondrial particles. J. Biol. Chem. 242, 5169-5173.
25. Kamo N., Demura M. and Kobatake Y. (1989) Linear-Equation for Calibration of the Mitochondrial-Membrane Potential. Bioelectrochem. Bioenergetics 21, 33-46.
26. Kamo N., Muratsugu M., Hongoh R. and Kobatake Y. (1979) Membrane potential of mitochondria measured with an electrode sensitive to tetraphenyl phosphonium and relationship between proton electrochemical potential and phosphorylation potential in steady state. J. Membr. Biol. 49, 105-121.
27. Klingenberg M. and Buecher T. (1961) [Glycerin-1-phosphate and flight muscle mitochondria.]. Biochem. Z. 334, 1-17.
28. 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.
29. 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.
30. Kwong L. K. and Sohal R. S. (1998) Substrate and site specificity of hydrogen peroxide generation in mouse mitochondria. Arch. Biochem. Biophys. 350, 118-126.
31. Liu Y., Fiskum G. and Schubert D. (2002) Generation of reactive oxygen species by the mitochondrial electron transport chain. J. Neurochem. 80, 780-787.
32. Lu A., Tang Y., Ran R., Clark J. F., Aronow B. J. and Sharp F. R. (2003) Genomics of the periinfarction cortex after focal cerebral ischemia. J. Cereb. Blood Flow Metab. 23, 786-810.
33. McKenna M. C., Tildon J. T., Stevenson J. H., Boatright R. and Huang S. (1993) Regulation of energy metabolism in synaptic terminals and cultured rat brain astrocytes: differences revealed using aminooxyacetate. Dev. Neurosci. 15, 320-329.
34. McKenna M. C., Waagepetersen H. S., Schousboe A. and Sonnewald U. (2006) Neuronal and astrocytic shuttle mechanisms for cytosolic-mitochondrial transfer of reducing equivalents: Current evidence and pharmacological tools. Biochem. Pharmacol. 71, 399-407.
35. Miwa S. and Brand M. D. (2005) The topology of superoxide production by complex III and glycerol 3-phosphate dehydrogenase in Drosophila mitochondria. Biochim. Biophys. Acta 1709, 214-219.
36. Miwa S., St Pierre J., Partridge L. and Brand M. D. (2003) Superoxide and hydrogen peroxide production by Drosophila mitochondria. Free Radic. Biol. Med. 35, 938-948.
37. 2 release from activated human leukocytes using a dihydroxyphenoxazine derivative. J. Immunol. Meth. 202, 133-141.
38. Nguyen N. H., Brathe A. and Hassel B. (2003) Neuronal uptake and metabolism of glycerol and the neuronal expression of mitochondrial glycerol-3-phosphate dehydrogenase. J. Neurochem. 85, 831-842.
39. Nicholls D. G. and Budd S. L. (2000) Mitochondria and neuronal survival. Physiol. Rev. 80, 315-360.
40. Nishida M., Maruyama Y., Tanaka R., Kontani K., Nagao T. and Kurose H. (2000) G alpha (i) and G alpha (o) are target proteins of reactive oxygen species. Nature 408, 492-495.
41. Nohl H., Gille L. and Staniek K. (2005) Intracellular generation of reactive oxygen species by mitochondria. Biochem. Pharmacol. 69, 719-723.
42. Patole M. S., Swaroop A. and Ramasarma T. (1986) Generation of H2O2 in brain mitochondria. J. Neurochem. 47, 1-8.
43. Ramos M., del Arco A., Pardo B. et al. (2003) Developmental changes in the Ca2+-regulated mitochondrial aspartate-glutamate carrier aralar1 in brain and prominent expression in the spinal cord. Brain Res. Dev. Brain Res. 143, 33-46.
44. Rosenthal R. E., Hamud F., Fiskum G., Varghese P. J. and Sharpe S. (1987) Cerebral ischemia and reperfusion: prevention of brain mitochondrial injury by lidoflazine. J. Cereb. Blood Flow Metab. 7, 752-758.
45. Rutter G. A., Pralong W. F. and Wollheim C. B. (1992) Regulation of mitochondrial glycerol-phosphate dehydrogenase by Ca2+ within electropermeabilized insulin-secreting cells (INS-1). Biochim. Biophys. Acta 1175, 107-113.
46. Ryter S. W. and Tyrrell R. M. (1998) Singlet molecular oxygen 1, O2): a possible effector of eukaryotic gene expression. Free Radic. Biol. Med. 24, 1520-1534.
47. Scaduto R. C. Jr and Grotyohann L. W. (1999) Measurement of mitochondrial membrane potential using fluorescent rhodamine derivatives. Biophys. J. 76, 469-477.
48. Shaw M. A., Edwards Y. H. and Hopkinson D. A. (1982) Human mitochondrial glycerol phosphate dehydrogenase (GPDm) isozymes. Ann. Hum. Genet. 46, 11-23.
49. Sohal R. S. (1993) Aging, cytochrome oxidase activity, and hydrogen peroxide release by mitochondria. Free Radic. Biol. Med. 14, 583-588.
50. St Pierre J., Buckingham J. A., Roebuck S. J. and Brand M. D. (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 277, 44 784-44 790.
51. Starkov A. A. and Fiskum G. (2001) Myxothiazol induces H (2) O (2) production from mitochondrial respiratory chain. Biochem. Biophys. Res. Commun. 281, 645-650.
52. Starkov A. A. and Fiskum G. (2003) Regulation of brain mitochondrial H2O2 production by membrane potential and NAD (P) H redox state. J. Neurochem. 86, 1101-1107.
53. Starkov A. A., Chinopoulos C. and Fiskum G. (2004a) Mitochondrial calcium and oxidative stress as mediators of ischemic brain injury. Cell Calcium 36, 257-264.
54. Starkov A. A., Fiskum G., Chinopoulos C., Lorenzo B. J., Browne S. E., Patel M. S. and Beal M. F. (2004b) Mitochondrial alpha-keto-glutarate dehydrogenase complex generates reactive oxygen species. J. Neurosci. 24, 7779-7788.
55. Tatla S., Woodhead V., Foreman J. C. and Chain B. M. (1999) The role of reactive oxygen species in triggering proliferation and IL-2 secretion in T cells. Free Radic. Biol. Med. 26, 14-24.
56. Thierbach G. and Reichenbach H. (1981) Myxothiazol, a new inhibitor of the cytochrome b-c1 segment of th respiratory chain. Biochim. Biophys. Acta 638, 282-289.
57. Tretter L. and Adam-Vizi V. (2004) Generation of reactive oxygen species in the reaction catalyzed by alpha-ketoglutarate dehydrogenase. J. Neurosci. 24, 7771-7778.
58. Tretter L., Chinopoulos C. and Adam-Vizi V. (1998) Plasma membrane depolarization and disturbed Na+ homeostasis induced by the protonophore carbonyl cyanide-p-trifluoromethoxyphenyl-hydrazon in isolated nerve terminals. Mol. Pharmacol. 53, 734-741.
59. Tretter L., Mayer-Takacs D. and Adam-Vizi V. (2006) BSA critically influences the membrane potential and the mechanism of ROS generation in succinate-supported isolated brain mitochondria. Neurochem. Int. Epub ahead of print: PMID: 16965838.
60. Trumpower B. L. (1990) The protonmotive Q cycle. Energy transduction by coupling of proton translocation to electron transfer by the cytochrome bc1 complex. J. Biol. Chem 265, 11 409-11 412.
61. Turrens J. F. and Boveris A. (1980) Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem. J. 191, 421-427.
62. Votyakova T. V. and Reynolds I. J. (2001) DeltaPsi (m)-Dependent and - independent production of reactive oxygen species by rat brain mitochondria. J. Neurochem. 79, 266-277.
63. Waagepetersen H. S., Qu H., Schousboe A. and Sonnewald U. (2001) Elucidation of the quantitative significance of pyruvate carboxylation in cultured cerebellar neurons and astrocytes. J. Neurosci. Res. 66, 763-770.
64. Zoccarato F., Cavallini L., Deana R. and Alexandre A. (1988) Pathways of hydrogen peroxide generation in guinea pig cerebral cortex mitochondria. Biochem. Biophys. Res. Commun. 154, 727-734.