Reactive oxygen species regulation by AIF- and complex I-depleted brain mitochondria

Free Radical Biology and Medicine

Volumn 46, Issue 7, 2009, Pages 939-947

  Chinta, Shankar J ^a   Rane, Anand ^a   Yadava, Nagendra ^a   Andersen, Julie K ^a   Nicholls, David G ^a   Polster, Brian M ^a,b  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis inducing factor; Electron transport chain; Neurodegeneration; Oxidative stress; Protein carbonyl; Synaptosome

Indexed keywords

APOPTOSIS INDUCING FACTOR; CARBONYL DERIVATIVE; HYDROGEN PEROXIDE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE);

ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SYNAPTOSOME; WILD TYPE;

ANIMALS; APOPTOSIS INDUCING FACTOR; BRAIN; CITRATE (SI)-SYNTHASE; ELECTRON TRANSPORT COMPLEX I; HYDROGEN PEROXIDE; MALE; MICE; MITOCHONDRIA; MUTATION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PROTEIN CARBONYLATION; REACTIVE OXYGEN SPECIES; SUCCINIC ACID;

MUS;

EID: 61449250478     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2009.01.010     Document Type: Article

References (65)

1. Andersen J.K. Oxidative stress in neurodegeneration: cause or consequence?. Nat. Med. 10 Suppl. (2004) S18-S25
2. Andreyev A.Y., Kushnareva Y.E., and Starkov A.A. Mitochondrial metabolism of reactive oxygen species. Biochemistry (Mosc. ) 70 (2005) 200-214
3. Apostolova N., Cervera A.M., Victor V.M., Cadenas S., Sanjuan-Pla A., varez-Barrientos A., Esplugues J.V., and McCreath K.J. Loss of apoptosis-inducing factor leads to an increase in reactive oxygen species, and an impairment of respiration that can be reversed by antioxidants. Cell Death Differ. 13 (2006) 354-357
4. Barja G. 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 (1999) 347-366
5. Benit P., Goncalves S., Dassa E.P., Briere J.J., and Rustin P. The variability of the harlequin mouse phenotype resembles that of human mitochondrial-complex I-deficiency syndromes. PLoS ONE 3 (2008) e3208
6. Betarbet R., Sherer T.B., MacKenzie G., Garcia-Osuna M., Panov A.V., and Greenamyre J.T. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 3 (2000) 1301-1306
7. Brookes P.S. Mitochondrial H(+) leak and ROS generation: an odd couple. Free Radic. Biol. Med 38 (2005) 12-23
8. Brown D., Yu B.D., Joza N., Benit P., Meneses J., Firpo M., Rustin P., Penninger J.M., and Martin G.R. Loss of Aif function causes cell death in the mouse embryo, but the temporal progression of patterning is normal. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 9918-9923
9. Burns R.S., Chiueh C.C., Markey S.P., Ebert M.H., Jacobowitz D.M., and Kopin I.J. A primate model of parkinsonism: selective destruction of dopaminergic neurons in the pars compacta of the substantia nigra by N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Proc. Natl. Acad. Sci. U. S. A. 80 (1983) 4546-4550
10. Choi W.S., Kruse S.E., Palmiter R.D., and Xia Z. Mitochondrial complex I inhibition is not required for dopaminergic neuron death induced by rotenone, MPP+, or paraquat. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 15136-15141
11. Chu C.T., Zhu J.H., Cao G., Signore A., Wang S., and Chen J. Apoptosis inducing factor mediates caspase-independent 1-methyl-4-phenylpyridinium toxicity in dopaminergic cells. J. Neurochem. 94 (2005) 1685-1695
12. Churbanova I.Y., and Sevrioukova I.F. Redox-dependent changes in molecular properties of mitochondrial apoptosis inducing factor. J. Biol. Chem. (2007)
13. Cino M., and Del Maestro R.F. Generation of hydrogen peroxide by brain mitochondria: the effect of reoxygenation following postdecapitative ischemia. Arch. Biochem. Biophys. 269 (1989) 623-638
14. Davey G.P., and Clark J.B. Threshold effects and control of oxidative phosphorylation in nonsynaptic rat brain mitochondria. J. Neurochem. 66 (1996) 1617-1624
15. Davey G.P., Peuchen S., and Clark J.B. Energy thresholds in brain mitochondria. Potential involvement in neurodegeneration. J. Biol. Chem. 273 (1998) 12753-12757
16. El V G., Csaba Z., Olivier P., Lelouvier B., Schwendimann L., Dournaud P., Verney C., Rustin P., and Gressens P. Apoptosis-inducing factor deficiency induces early mitochondrial degeneration in brain followed by progressive multifocal neuropathology. J. Neuropathol. Exp. Neurol. 66 (2007) 838-847
17. Fiskum G., Starkov A., Polster B.M., and Chinopoulos C. Mitochondrial mechanisms of neural cell death and neuroprotective interventions in Parkinson's disease. Ann. N. Y. Acad. Sci. 991 (2003) 111-119
18. Gazaryan I.G., Krasnikov B.F., Ashby G.A., Thorneley R.N., Kristal B.S., and Brown A.M. Zinc is a potent inhibitor of thiol oxidoreductase activity and stimulates reactive oxygen species production by lipoamide dehydrogenase. J. Biol. Chem. 277 (2002) 10064-10072
19. Herrero A., and Barja G. Localization of the site of oxygen radical generation inside the complex I of heart and nonsynaptic brain mammalian mitochondria. J. Bioenerg. Biomembr. 32 (2000) 609-615
20. Hinkle P.C., Butow R.A., Racker E., and Chance B. 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 (1967) 5169-5173
21. Johnson-Cadwell L.I., Jekabsons M.B., Wang A., Polster B.M., and Nicholls D.G. 'Mild uncoupling' does not decrease mitochondrial superoxide levels in cultured cerebellar granule neurons but decreases spare respiratory capacity and increases toxicity to glutamate and oxidative stress. J. Neurochem. 101 (2007) 1619-1631
22. Joza N., Oudit G.Y., Brown D., Benit P., Kassiri Z., Vahsen N., Benoit L., Patel M.M., Nowikovsky K., Vassault A., Backx P.H., Wada T., Kroemer G., Rustin P., and Penninger J.M. Muscle-specific loss of apoptosis-inducing factor leads to mitochondrial dysfunction, skeletal muscle atrophy, and dilated cardiomyopathy. Mol. Cell. Biol. 25 (2005) 10261-10272
23. Klein J.A., Longo-Guess C.M., Rossmann M.P., Seburn K.L., Hurd R.E., Frankel W.N., Bronson R.T., and Ackerman S.L. The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature 419 (2002) 367-374
24. Krantic S., Mechawar N., Reix S., and Quirion R. Apoptosis-inducing factor: a matter of neuron life and death. Prog. Neurobiol. 81 (2007) 179-196
25. Kristian T., and Fiskum G. A fluorescence-based technique for screening compounds that protect against damage to brain mitochondria. Brain Res. Brain Res. Protoc. 13 (2004) 176-182
26. Kroemer G., Galluzzi L., and Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol. Rev. 87 (2007) 99-163
27. Kushnareva Y., Murphy A.N., and Andreyev A. Complex I-mediated reactive oxygen species generation: modulation by cytochrome c and NAD(P)+ oxidation-reduction state. Biochem. J. 368 (2002) 545-553
28. Kussmaul L., and Hirst J. The mechanism of superoxide production by NADH:ubiquinone oxidoreductase (complex I) from bovine heart mitochondria. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 7607-7612
29. Lambert A.J., and Brand M.D. Inhibitors of the quinone-binding site allow rapid superoxide production from mitochondrial NADH:ubiquinone oxidoreductase (complex I). J. Biol. Chem. 279 (2004) 39414-39420
30. Lapidus R.G., and Sokolove P.M. Spermine inhibition of the permeability transition of isolated rat liver mitochondria: an investigation of mechanism. Arch. Biochem. Biophys. 306 (1993) 246-253
31. Lim M.L., Mercer L.D., Nagley P., and Beart P.M. Rotenone and MPP+ preferentially redistribute apoptosis-inducing factor in apoptotic dopamine neurons. Neuroreport 18 (2007) 307-312
32. Liou A.K., Zhou Z., Pei W., Lim T.M., Yin X.M., and Chen J. BimEL up-regulation potentiates AIF translocation and cell death in response to MPTP. FASEB J. 19 (2005) 1350-1352
33. Lipton S.A., and Bossy-Wetzel E. Dueling activities of AIF in cell death versus survival: DNA binding and redox activity. Cell 111 (2002) 147-150
34. Mate M.J., Ortiz-Lombardia M., Boitel B., Haouz A., Tello D., Susin S.A., Penninger J., Kroemer G., and Alzari P.M. The crystal structure of the mouse apoptosis-inducing factor AIF. Nat. Struct. Biol. 9 (2002) 442-446
35. Miramar M.D., Costantini P., Ravagnan L., Saraiva L.M., Haouzi D., Brothers G., Penninger J.M., Peleato M.L., Kroemer G., and Susin S.A. NADH oxidase activity of mitochondrial apoptosis-inducing factor. J. Biol. Chem. 276 (2001) 16391-16398
36. Murphy M.P., Krueger M.J., Sablin S.O., Ramsay R.R., and Singer T.P. Inhibition of complex I by hydrophobic analogues of N-methyl-4-phenylpyridinium (MPP+) and the use of an ion-selective electrode to measure their accumulation by mitochondria and electron-transport particles. Biochem. J. 306 Pt 2 (1995) 359-365
37. Nicholls D.G. Bioenergetics and transmitter release in the isolated nerve terminal. Neurochem. Res. 28 (2003) 1433-1441
38. Panov A., Dikalov S., Shalbuyeva N., Taylor G., Sherer T., and Greenamyre J.T. Rotenone model of Parkinson disease: multiple brain mitochondria dysfunctions after short term systemic rotenone intoxication. J. Biol. Chem. 280 (2005) 42026-42035
39. Perier C., Tieu K., Guegan C., Caspersen C., Jackson-Lewis V., Carelli V., Martinuzzi A., Hirano M., Przedborski S., and Vila M. Complex I deficiency primes Bax-dependent neuronal apoptosis through mitochondrial oxidative damage. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 19126-19131
40. Polster B.M., Basanez G., Etxebarria A., Hardwick J.M., and Nicholls D.G. Calpain I induces cleavage and release of apoptosis-inducing factor from isolated mitochondria. J. Biol. Chem. 280 (2005) 6447-6454
41. Pospisilik J.A., Knauf C., Joza N., Benit P., Orthofer M., Cani P.D., Ebersberger I., Nakashima T., Sarao R., Neely G., Esterbauer H., Kozlov A., Kahn C.R., Kroemer G., Rustin P., Burcelin R., and Penninger J.M. Targeted deletion of AIF decreases mitochondrial oxidative phosphorylation and protects from obesity and diabetes. Cell 131 (2007) 476-491
42. Schilling B., Bharath M.M.S., Row R.H., Murray J., Cusack M.P., Capaldi R.A., Freed C.R., Prasad K.N., Andersen J.K., and Gibson B.W. Rapid purification and mass spectrometric characterization of mitochondrial NADH dehydrogenase (Complex I) from rodent brain and a dopaminergic neuronal cell line. Mol. Cell. Proteomics 4 (2005) 84-96
43. Seiler A., Schneider M., Forster H., Roth S., Wirth E.K., Culmsee C., Plesnila N., Kremmer E., Radmark O., Wurst W., Bornkamm G.W., Schweizer U., and Conrad M. Glutathione peroxidase 4 senses and translates oxidative stress into 12/15-lipoxygenase dependent- and AIF-mediated cell death. Cell Metab. 8 (2008) 237-248
44. Shepherd D., and Garland P.B. Citrate synthase from rat liver. Methods Enzymol. 13 (1969) 11-16
45. Sherer T.B., Betarbet R., Testa C.M., Seo B.B., Richardson J.R., Kim J.H., Miller G.W., Yagi T., Matsuno-Yagi A., and Greenamyre J.T. Mechanism of toxicity in rotenone models of Parkinson's disease. J. Neurosci. 23 (2003) 10756-10764
46. Sims N.R. Rapid isolation of metabolically active mitochondria from rat brain and subregions using Percoll density gradient centrifugation. J. Neurochem. 55 (1990) 698-707
47. Sipos I., Tretter L., and dam-Vizi V. Quantitative relationship between inhibition of respiratory complexes and formation of reactive oxygen species in isolated nerve terminals. J. Neurochem. 84 (2003) 112-118
48. Srere P.A. Citrate synthase. Methods Enzymol. 13 (2008) 3-11
49. 2 production by membrane potential and NAD(P)H redox state. J. Neurochem. 86 (2003) 1101-1107
50. Starkov A.A., Fiskum G., Chinopoulos C., Lorenzo B.J., Browne S.E., Patel M.S., and Beal M.F. Mitochondrial alpha-ketoglutarate dehydrogenase complex generates reactive oxygen species. J. Neurosci. 24 (2004) 7779-7788
51. Starkov A.A., Polster B.M., and Fiskum G. Regulation of hydrogen peroxide production by brain mitochondria by calcium and Bax. J. Neurochem. 83 (2002) 220-228
52. Tretter L., and dam-Vizi V. Generation of reactive oxygen species in the reaction catalyzed by alpha-ketoglutarate dehydrogenase. J. Neurosci. 24 (2004) 7771-7778
53. Tretter L., and dam-Vizi V. Uncoupling is without an effect on the production of reactive oxygen species by in situ synaptic mitochondria. J. Neurochem. 103 (2007) 1864-1871
54. Tretter L., Mayer-Takacs D., and dam-Vizi V. The effect of bovine serum albumin on the membrane potential and reactive oxygen species generation in succinate-supported isolated brain mitochondria. Neurochem. Int. 50 (2007) 139-147
55. Urbano A., Lakshmanan U., Choo P.H., Kwan J.C., Ng P.Y., Guo K., Dhakshinamoorthy S., and Porter A. AIF suppresses chemical stress-induced apoptosis and maintains the transformed state of tumor cells. EMBO J. 24 (2005) 2815-2826
56. Vahsen N., Cande C., Briere J.J., Benit P., Joza N., Larochette N., Mastroberardino P.G., Pequignot M.O., Casares N., Lazar V., Feraud O., Debili N., Wissing S., Engelhardt S., Madeo F., Piacentini M., Penninger J.M., Schagger H., Rustin P., and Kroemer G. AIF deficiency compromises oxidative phosphorylation. EMBO J. 23 (2004) 4679-4689
57. van V E., Bertrand A.T., van der N.R., Kostin S., Doevendans P.A., Crijns H.J., de W.E., Sluiter W., Ackerman S.L., and De Windt L.J. Downregulation of apoptosis-inducing factor in harlequin mutant mice sensitizes the myocardium to oxidative stress-related cell death and pressure overload-induced decompensation. Circ. Res. 96 (2005) e92-e101
58. van V E., Bertrand A.T., van Oort R.J., van der N.R., Engelen M., van Rijen H.V., Doevendans P.A., Crijns H.J., Ackerman S.L., Sluiter W., and De Windt L.J. EUK-8, a superoxide dismutase and catalase mimetic, reduces cardiac oxidative stress and ameliorates pressure overload-induced heart failure in the harlequin mouse mutant. J. Am. Coll. Cardiol. 48 (2006) 824-832
59. Votyakova T.V., and Reynolds I.J. DeltaPsi(m)-Dependent and -independent production of reactive oxygen species by rat brain mitochondria. J. Neurochem. 79 (2001) 266-277
60. Yadava N., and Nicholls D.G. Spare respiratory capacity rather than oxidative stress regulates glutamate excitotoxicity after partial respiratory inhibition of mitochondrial complex I with rotenone. J. Neurosci. 27 (2007) 7310-7317
61. Yadava N., Potluri P., Smith E.N., Bisevac A., and Scheffler I.E. Species-specific and mutant MWFE proteins. Their effect on the assembly of a functional mammalian mitochondrial complex I. J. Biol. Chem. 277 (2002) 21221-21230
62. Ye H., Cande C., Stephanou N.C., Jiang S., Gurbuxani S., Larochette N., Daugas E., Garrido C., Kroemer G., and Wu H. DNA binding is required for the apoptogenic action of apoptosis inducing factor. Nat. Struct. Biol. 9 (2002) 680-684
63. Zhu C., Wang X., Huang Z., Qiu L., Xu F., Vahsen N., Nilsson M., Eriksson P.S., Hagberg H., Culmsee C., Plesnila N., Kroemer G., and Blomgren K. Apoptosis-inducing factor is a major contributor to neuronal loss induced by neonatal cerebral hypoxia-ischemia. Cell Death. Differ. 14 (2007) 775-784
64. 2 in brain mitochondria: inhibition by Ca2+. J. Biol. Chem. 279 (2004) 4166-4174
65. 2 release at NADH:ubiquinone oxidoreductase (complex I) in brain mitochondria. Biochem. J. 406 (2007) 125-129