Complex I specific increase in superoxide formation and respiration rate by PrP-null mouse brain mitochondria

Journal of Neurochemistry

Volumn 105, Issue 1, 2008, Pages 177-191

  Paterson, Andrew W J ^a   Curtis, John C ^a   MacLeod, Nikki K ^a  

^a Centre for Integrative Physiology   (United Kingdom)

Author keywords

Electron microscopy; Electron paramagnetic resonance; Mitochondria; Neurodegeneration; PrP; Respiration; Submitochondrial particles; Superoxide; Superoxide dismutase; Tempone

Indexed keywords

MITOCHONDRIAL PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUPEROXIDE; SUPEROXIDE DISMUTASE;

ANIMAL TISSUE; ARTICLE; BRAIN MITOCHONDRION; BREATHING RATE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RESPIRATORY CHAIN; SUBMITOCHONDRIAL PARTICLE; WESTERN BLOTTING;

AGE FACTORS; ANIMALS; BRAIN; ELECTRON SPIN RESONANCE SPECTROSCOPY; ELECTRON TRANSPORT COMPLEX I; FREE RADICALS; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; OXYGEN CONSUMPTION; PRIONS; RESPIRATION; SUBMITOCHONDRIAL PARTICLES; SUPEROXIDES; VOLTAGE-DEPENDENT ANION CHANNEL 1;

MUS;

EID: 41149107987     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.05123.x     Document Type: Article

References (71)

1. Albers D. S. Beal M. F. (2000) Mitochondrial dysfunction and oxidative stress in aging and neurodegenerative disease. J. Neural Transmission-Suppl. 59, 133 154.
2. Anderson M. F. Sims N. R. (2000) Improved recovery of highly enriched mitochondrial fractions from small brain tissue samples. Brain Res Brain Res Protoc 5, 95 101.
3. Baldwin M. A., Cohen F. E. Prusiner S. B. (1995) Prion protein isoforms, a convergence of biological and structural investigations. J. Biol. Chem. 270, 19197 19200.
4. Beer S. M., Taylor E. R., Brown S. E., Dahm C. C., Costa N. J., Runswick M. J. Murphy M. P. (2004) Glutaredoxin 2 catalyzes the reversible oxidation and glutathionylation of mitochondrial membrane thiol protein. J. Biol. Chem. 279, 47939 47951.
5. Bremer J. Davies E. J. (1975) Studies on the active transfer of reducing equivalents into mitochondria via the malate-aspartate shuttle. Biochim. Biophys. Acta 376, 387 397.
6. Brown D. R. (2005) Neurodegeneration and oxidative stress: prion disease results from loss of antioxidant defence. Folia Neuropathol. 43, 229 243.
7. Brown D. R. Besinger A. (1998) Prion protein expression and superoxide dismutase activity. Biochem. J. 334, 423 429.
8. Brown D. R., Schulz S., Schmidt B. Kretzschmar H. A. (1997) Prion protein-deficient cells show altered response to oxidative stress due to decreased SOD-1 activity. Exp. Neurol. 146, 104 112.
9. Brown D. R., Schmidt B. Kretzschmar H. A. (1998) Effects of copper on survival of prion protein knockout neurons and glia. J. Neurochem. 70, 1686 1693.
10. Brown D. R., Clive C. Haswell S. J. (2001) Antioxidant activity related to copper binding of native prion protein. J. Neurochem. 76, 69 76.
11. Brown D. R., Nicholas R. S. Canevari L. (2002) Lack of prion protein expression results in a neuronal phenotype sensitive to stress. J. Neurosci. Res. 67, 211 224.
12. Burns C. S., Aronoff S., Legname G., Prusiner S. B., Antholine W. E., Gerfen G. J., Peisach J. Millhauser G. L. (2003) Copper coordination in the full-length, recombinant prion protein. Biochemistry 42, 6794 6803.
13. Chance B. Williams G. R. (1955) Respiratory enzymes in oxidative phosphorylation III The steady state. J. Biol. Chem. 217, 409 427.
14. Choi S. I., Ju W. K., Choi E. K., Kim J., Lea H. Z., Carp R. I., Wisniewski H. M. Kim Y. S. (1998) Mitochondrial dysfunction induced by oxidative stress in the brains of hamsters infected with the 263 K scrapie agent. Acta Neuropathol. (Berl) 96, 279 286.
15. Clark J. B. Nicklas W. J. (1970) The Metabolism of Rat Brain Mitochondria. Preparation and characterization. J. Biol. Chem. 245, 4724 4731.
16. Curtis J., Errington M., Bliss T., Voss K. MacLeod N. (2003) Age-dependent loss of PTP and LTP in the hippocampus of PrP-null mice. Neurobiol. Dis. 13, 55 62.
17. Dikalov S., Skatchkov M. Bassenge E. (1997) Quantification of peroxynitrite, superoxide, and peroxyl radicals by a new spin trap hydroxylamine 1-hydroxy-2,2,6,6-tetramethyl-4-oxo-piperidine. Biochem. Biophys. Res. Commun. 230, 54 57.
18. Dikalov S. I., Vitek M. P., Maples K. R. Mason R. P. (1999) Amyloid beta peptides do not form peptide-derived free radicals spontaneously, but can enhance metal-catalyzed oxidation of hydroxylamines to nitroxides. J. Biol. Chem. 274, 9392 9399.
19. Forman H. J. Fridovic I. (1973) Superoxide Dismutase - Comparison of Rate Constants. Arch. Biochem. Biophys. 158, 396 400.
20. Fridovich I. (1970) Quantitative aspects of the production of superoxide anion radical by milk xanthine oxidase. J. Biol. Chem. 245, 4053 4057.
21. Hachiya N. S., Yamada M., Watanabe K., Jozuka A., Ohkubo T., Sano K., Takeuchi Y., Kozuka Y., Sakasegawa Y. Kaneko K. (2005) Mitochondrial localization of cellular prion protein (PrPC) invokes neuronal apoptosis in aged transgenic mice overexpressing PrPC. Neurosci. Lett. 374, 98 103.
22. Halestrap A. P. (1975) The mitochondrial pyruvate carrier. Kinetics and specificity for substrates and inhibitors. Biochem. J. 148, 85 96.
23. Halliwell B. (2006) Oxidative stress and neurodegeneration: where are we now? J. Neurochem. 97, 1634 1658.
24. 2+ Transport. J. Bioenerg. Biomembr. 26, 495 508.
25. Hodges G. R., Young M. J., Paul T. Ingold K. U. (2000) How should xanthine oxidase-generated superoxide yields be measured? Free Radic. Biol. Med. 29, 434 441.
26. Huang G., Lu H., Hao A., Ng D. C. H., Ponniah S., Guo K., Lufei C., Zeng Q. Cao X. (2004) GRIM-19, a Cell Death Regulatory Protein, Is Essential for Assembly and Function of Mitochondrial Complex I. Mol. Cell. Biol. 24, 8447 8456.
27. Hutter G., Heppner F. L. Aguzzi A. (2003) No superoxide dismutase activity of cellular prion protein in vivo. Biol Chem 384, 1279 1285.
28. Jeffrey M., Scott J. R. Fraser H. (1991) Scrapie inoculation of mice: light and electron microscopy of the superior colliculi. Acta Neuropathol. (Berl) 81, 562 571.
29. Jha N., Jurma O., Lalli G., Liu Y., Pettus E. H., Greenamyre J. T., Liu R. M., Forman H. J. Andersen J. K. (2000) Glutathione depletion in PC12 results in selective inhibition of mitochondrial complex I activity - Implications for Parkinson's disease. J. Biol. Chem. 275, 26096 26101.
30. 2+ load, but not by mitochondrial depolarization. FEBS Lett. 529, 351 355.
31. Keeney P. M., Xie J., Capaldi R. A. Bennett Jr. J. P. (2006) Parkinson's Disease Brain Mitochondrial Complex I Has Oxidatively Damaged Subunits and Is Functionally Impaired and Misassembled. J. Neurosci. 26, 5256 5264.
32. Klamt F., Dal P., Conte d., Walz R., Andrades M. E., da S., Brentani R. R., Izquierdo I. Fonseca M. (2001) Imbalance of antioxidant defense in mice lacking cellular prion protein. Free Radic. Biol. Med. 30, 1137 1144.
33. Koopman W. J. H., Verkaart S., Visch H. J., van der Westhuizen F. H., Murphy M. P., van den Heuvel L. W., Smeitnk J. A. Willems P. H. (2005) Inhibition of complex I of the electron transport chain causes O2-.-mediated mitochondrial outgrowth. Am. J. Physiol. Cell Physiol. 288, 1440 1450.
34. Kosenko E., Venediktova N., Kaminsky Y., Montoliu C. Felipo V. (2003) Sources of oxygen radicals in brain in acute ammonia intoxication in vivo. Brain Res. 981, 193 200.
35. Kriaucionis S., Paterson A., Curtis J., Guy J., MacLeod N. Bird A. (2006) Gene expression analysis exposes mitochondrial abnormalities in a mouse model of Rett Syndrome. Mol. Cell. Biol. 26, 5033 5042.
36. Kudin A. P., Bimpong-Buta N. Y., Vielhaber S., Elger C. E. Kunz W. S. (2004) Characterization of superoxide-producing sites in isolated brain mitochondria. J. Biol. Chem. 279, 4127 4135.
37. Kussmaul L. Hirst J. (2006) The mechanism of superoxide production by NADH: ubiquinone oxidoreductase (complex I) from bovine heart mitochondria. Proc. Natl Acad. Sci. USA 103, 7607 7612.
38. Lai J. C., Walsh J. M., Dennis S. C. Clark J. B. (1977) Synaptic and non-synaptic mitochondria from rat brain: isolation and characterization. J. Neurochem. 28, 625 631.
39. Lee D. W., Sohn H. O., Lim H. B., Lee Y. G., Kim Y. S., Carp R. I. Wisniewski H. M. (1999) Alteration of free radical metabolism in the brain of mice infected with scrapie agent. Free Radic. Res. 30, 499 507.
40. Lin M. T. Beal M. F. (2006) Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443, 787 795.
41. Lobao-Soares B., Bianchin M. M., Linhares M. N. et al. (2005) Normal brain mitochondrial respiration in adult mice lacking cellular prion protein. Neurosci. Lett. 375, 203 206.
42. Manson J. C., Clarke A. R., Hooper M. L., Aitchison L., Mcconnell I. Hope J. (1994) 129/Ola Mice Carrying A Null Mutation in Prp That Abolishes Messenger-Rna Production Are Developmentally Normal. Mol. Neurobiol. 8, 121 127.
43. Miele G., Jeffrey M., Turnbull D., Manson J. Clinton M. (2002) Ablation of cellular prion protein expression affects mitochondrial numbers and morphology. Biochem. Biophys. Res. Commun. 291, 372 377.
44. Mishmar D., Ruiz-Pesini E., Mondragon-Palomino M., Procaccio V., Gaut B. Wallace D. C. (2006) Adaptive selection of mitochondrial complex I subunits during primate radiation. Gene 378, 11 18.
45. Oberley L. W. Spitz D. R. (1984) Assay of superoxide dismutase activity in tumor tissue. Methods Enzymol. 105, 457 464.
46. Palmisano G., Sardanelli A. M., Signorile A., Papa S. Larsen M. R. (2007) The phosphorylation pattern of bovine heart complex I subunits. Proteomics 7, 1575 1583.
47. Panov A., Dikalov S., Shalbuyeva N., Taylor G., Sherer T. Greenamyre J. T. (2005) Rotenone model of Parkinsons disease: multiple brain mitochondria dysfunctions after short term rotenone intoxication. J. Biol. Chem. 280, 42026 42035.
48. Pauly P. C. Harris D. A. (1998) Copper stimulates endocytosis of the prion protein. J. Biol. Chem. 273, 33107 33110.
49. Peterson G. L. (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal. Biochem. 83, 346 356.
50. Piccoli C., Scacco S., Bellomo F., Signorile A., Iuso A., Boffoli D., Scrima R., Capitanio N. Papa S. (2006) cAMP controls oxygen metabolism in mammalian cells. FEBS Lett. 580, 4539 4543.
51. Poderoso J. J., Carreras M. C., Lisdero C., Riobo N., Schopfer F. Boveris A. (1996) Nitric oxide inhibits electron transfer and increases superoxide radical production in rat heart mitochondria and submitochondrial particles. Arch. Biochem. Biophys. 328, 85 92.
52. Riobo N. A., Clementi E., Melani M., Boveris A., Cadenas E., Moncada S. Poderoso J. J. (2001) Nitiric oxide inhibits mitochondrial NADH:ubiquinone reductase activity through peroxynitrite formation. Biochem. J. 359, 139 145.
53. Robinson B. H. (1998) Human Complex I deficiency: Clinical spectrum and involvement of oxygen free radicals in the pathogenicity of the defect. Biochim. Biophys. Acta-Bioenerget. 1364, 271 286.
54. Rossignol R., Letellier T., Malgat M., Rocher C. Mazat J. P. (2000) Tissue variation in the control of oxidative phosphorylation: implication for mitochondrial diseases. Biochem. J. 347, 45 53.
55. Sales N., Rodolfo K., Hassig R., Faucheux B., Di Giamberardino L. Moya K. L. (1998) Cellular prion protein localization in rodent and primate brain. Eur. J. Neurosci. 10, 2464 2471.
56. Sasaki S., Warita H., Murakami T., Abe K. Iwata M. (2004) Ultrastructural study of mitochondria in the spinal cord of transgenic mice with a G93A mutant SOD1 gene. Acta Neuropathol. 107, 461 474.
57. Scacco S., Vergari R., Scarpulla R. C., Technikova-Dobrova Z., Sardanelli A., Lambo R., Lorusso V. Papa S. (2000) cAMP-dependent Phosphorylation of the Nuclear Encoded 18-kDa (IP) Subunit of Respiratory Complex I and Activation of the Complex in Serum-starved Mouse Fibroblast Cultures. J. Biol. Chem. 275, 17578 17582.
58. Schagger H. (1995) Quantification of Oxidative-Phosphorylation Enzymes After Blue Native Electrophoresis and 2-Dimensional Resolution - Normal Complex-I Protein Amounts in Parkinsons-Disease Conflict with Reduced Catalytic Activities. Electrophoresis 16, 763 770.
59. Shalbuyeva N., Brustovetsky T., Bolshakov A. Brustovetsky N. (2006) Calcium-dependent spontaneously reversible remodeling of brain mitochondria. J. Biol. Chem. 281, 37547 37558.
60. Sipos I., Tretter L. Adam-Vizi V. (2003) Quantitative relationship between inhibition of respiratory complexes and formation of reactive oxygen species in isolated nerve terminals. J. Neurochem. 84, 112 118.
61. Spector A. (2000) Review: Oxidative stress and disease. J. Ocul. Pharmacol. Ther. 16, 193 201.
62. Starkov A. A. Fiskum G. (2003) Regulation of brain mitochondrial H2O2 production by membrane potential and NAD(P)H redox state. J. Neurochem. 86, 1101 1107.
63. Starkov A. A., Polster B. M. Fiskum G. (2002) Regulation of hydrogen peroxide production by brain mitochondria by calcium and Bax. J. Neurochem. 83, 220 228.
64. St-Pierre J., Buckingham J. A., Roebuck S. J. Brand M. D. (2002) Topology of superoxide production from different sites in the mitochondrial electron transport chain. J. Biol. Chem. 277, 44784 44790.
65. Taylor R. W. Turnbull D. M. (1997) Laboratory diagnosis of mitochondrial disease, in Organelle Diseases (Applegarth D. A., Dimmick J. E. Hall J. G., eds Chapman and Hall, London, 342 350.
66. Trimmer P. A., Swerdlow R. H., Parks J. K., Keeney P., Bennet J. P. J., Miller S. W., Davies R. E. Parker W. D. J. (2000) Abnormal mitochondria morphology in sporadic Parkinson's and Alzheimer's disease cybrid cell lines. Exp. Neurol. 162, 37 50.
67. Turrens J. F., Freeman B. A., Levitt J. G. Crapo J. D. (1982) The effect of hyperoxia on superoxide production by lung submitochondrial particles. Arch. Biochem. Biophys. 217, 401 410.
68. Waggoner D. J., Drisaldi B., Bartnikas T. B., Casareno R. L., Prohaska J. R., Gitlin J. D. Harris D. A. (2000) Brain copper content and cuproenzyme activity do not vary with prion protein expression level. J. Biol. Chem. 275, 7455 7458.
69. White A. R., Collins S. J., Maher F., Jobling M. F., Stewart L. R., Thyer J. M., Beyreuther K., Masters C. L. Cappai R. (1999) Prion protein-deficient neurons reveal lower glutathione reductase activity and increased susceptibility to hydrogen peroxide toxicity. Am. J. Pathol. 155, 1723 1730.
70. Wong B. S., Liu T., Li R. et al. (2001) Increased levels of oxidative stress markers detected in the brains of mice devoid of prion protein. J. Neurochem. 76, 565 572.
71. Yadava N., Houchens T., Potluri P. Scheffler I. E. (2004) Development and characterization of a conditional mitochondrial complex I assembly system. J. Biol. Chem. 279, 12406 12413.