The mtDNA T8993G (NARP) mutation results in an impairment of oxidative phosphorylation that can be improved by antioxidants

Human Molecular Genetics

Volumn 13, Issue 8, 2004, Pages 869-879

  Mattiazzi, Marina ^a,b   Vijayvergiya, Chetan ^a,c   Gajewski, Carl D ^a   DeVivo, Darryl C ^d   Lenaz, Giorgio ^b   Wiedmann, Martin ^c   Manfredi, Giovanni ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d NEUROLOGICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATE; ANTIOXIDANT; CARBONYL CYANIDE 4 (TRIFLUOROMETHOXY)PHENYLHYDRAZONE; COPPER ZINC SUPEROXIDE DISMUTASE; CYTOCHROME C OXIDASE; DIHYDROLIPOATE; FREE RADICAL; GUANINE; LIPID; LIPID HYDROPEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL DNA; OLIGOMYCIN; OXYGEN; REACTIVE OXYGEN METABOLITE; ROTENONE; THYMINE; UBIDECARENONE;

ANIMAL CELL; ARTICLE; ATAXIA; CELL CULTURE; CONTROLLED STUDY; CYBRID; DRUG EFFICACY; EXTRACHROMOSOMAL INHERITANCE; FIBROBLAST; HUMAN; HUMAN CELL; LEIGH DISEASE; LIPID PEROXIDATION; MITOCHONDRIAL RESPIRATION; NEUROPATHY; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PATHOGENESIS; POINT MUTATION; PRIORITY JOURNAL; RESPIRATORY CHAIN; RETINITIS PIGMENTOSA; SYNTHESIS;

ADENOSINE TRIPHOSPHATE; ANTIOXIDANTS; CELL RESPIRATION; DNA, MITOCHONDRIAL; GENETIC LOAD; HUMANS; HYDROGEN-ION CONCENTRATION; LIPID PEROXIDATION; MUTATION; OXIDATIVE PHOSPHORYLATION; PROTON-TRANSLOCATING ATPASES; REACTIVE OXYGEN SPECIES;

ATAXIA;

EID: 1942453308     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddh103     Document Type: Article

References (49)

1. Elston, T., Wang, H. and Oster, G. (1998) Energy transduction in ATP synthase. Nature, 391, 510-513.
2. Noji, H. and Yoshida, M. (2001) The rotary machine in the cell, ATP synthase. J. Biol. Chem., 276, 1665-1668.
3. Rastogi, V.K. and Girvin, M.E. (1999) Structural changes linked to proton translocation by subunit c ofthe ATP synthase. Nature, 402, 263-268.
4. Holt, I.J., Harding, A.E., Petty, R.K. and Morgan-Hughes, J.A. (1990) A new mitochondrial disease associated with mitochondrial DNA heteroplasmy. Am. J. Hum. Genet., 46, 428-433.
5. Santorelli, F.M., Shanske, S., Macaya, A., DeVivo, D.C. and DiMauro, S. (1993) The mutation at nt 8993 of mitochondrial DNA is a common cause of Leigh's syndrome. Ann. Neurol., 34, 827-834.
6. White, S.L., Collins, V.R., Wolfe, R., Cleary, M.A., Shanske, S., DiMauro, S., Dahl, H.H. and Thorburn, D.R. (1999) Genetic counseling and prenatal diagnosis for the mitochondrial DNA mutations at nucleotide 8993. Am. J. Hum. Genet., 65, 474-482.
7. Schon, E.A., Santra, S., Pallotti, F. and Girvin, M.E. (2001) Pathogenesis of primary defects in mitochondrial ATP synthesis. Semin. Cell Dev. Biol., 12, 441-448.
8. Tatuch, Y. and Robinson, B.H. (1993) The mitochondrial DNA mutation at 8993 associated with NARP slows the rate of ATP synthesis in isolated lymphoblast mitochondria. Biochem. Biophys. Res. Commun., 192, 124-128.
9. Vazquez-Memije, M.E., Shanske, S., Santorelli, F.M., Kranz-Eble, P., Davidson, E., DeVivo, D.C. and DiMauro, S. (1996) Comparative biochemical studies in fibroblasts from patients with different forms of Leigh syndrome. J. Inherit. Metab. Dis., 19, 43-50.
10. Manfredi, G., Gupta, N., Vazquez-Memije, M.E., Sadlock, J.E., Spinazzola, A., De Vivo, D.C. and Schon, E.A. (1999) Oligomycin induces a decrease in the cellular content of a pathogenic mutation in the human mitochondrial ATPase 6 gene. J. Biol. Chem., 274, 9386-9391.
11. 0 cells completely lacking mtDNA. J. Biol. Chem., 275, 11075-11081.
12. Baracca, A., Barogi, S., Carelli, V., Lenaz, G. and Solaini, G. (2000) Catalytic activities of mitochondrial ATP synthase in patients with mitochondrial DNA T8993G mutation in the ATPase 6 gene encoding subunit a. J. Biol. Chem., 275, 4177-4182.
13. Nijtmans, L.G., Henderson, N.S., Attardi, G. and Holt, I.J. (2001) Impaired ATP synthase assembly associated with a mutation in the human ATP synthase subunit 6 gene. J. Biol. Chem., 276, 6755-6762.
14. Geromel, V., Kadhom, N., Cebalos-Picot, I., Ouari, O., Polidori, A., Munnich, A., Rotig, A. and Rustin, P. (2001) Superoxide-induced massive apoptosis in cultured skin fibroblasts harboring the neurogenic ataxia retinitis pigmentosa (NARP) mutation in the ATPasc-6 gene of the mitochondrial DNA. Hum. Mol. Genet., 10, 1221-1228.
15. Tanaka, M., Kovalenko, S.A., Gong, J.S., Borgeld, H.J., Katsumata, K., Hayakawa, M., Yoneda, M. and Ozawa, T. (1996) Accumulation of deletions and point mutations in mitochondrial genome in degenerative diseases. Ann. N YAcad. Sci., 786, 102-111.
16. Pitkanen, S. and Robinson, B.H. (1996) Mitochondrial complex I deficiency leads to increased production of superoxide radicals and induction of superoxide dismutase. J. Clin. Invest., 98, 345-351.
17. 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, 1364, 271-286.
18. Barrientos, A., Kenyon, L. and Moraes, C.T. (1998) Human xenomitochondrial cybrids. Cellular models of mitochondrial complex I deficiency. J. Biol. Chem., 273, 14210-14217.
19. King, M.P. and Attardi, G. (1989) Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation. Science, 246, 500-503.
20. Robinson, B.H. (1996) Use of fibroblast and lymphoblast cultures for detection of respiratory chain defects. Meth. Enzymol., 264, 454-464.
21. Villani, G. and Attardi, G. (1997) In vivo control of respiration by cytochrome c oxidase in wild-type and mitochondrial DNA mutation-carrying human cells. Proc. Natl Acad. Sci. USA, 94, 1166-1171.
22. Hurt, E.C., Pesold-Hurt, B., Suda, K., Oppliger, W. and Schatz, G. (1985) The first twelve amino acids (less than half of the pre-sequence) of an imported mitochondrial protein can direct mouse cytosolic dihydrofolate reductase into the yeast mitochondrial matrix. EMBO J., 4, 2061-2068.
23. Miesenbock, G., De Angelis, D.A. and Rothman, J.E. (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature, 394, 192-195.
24. Llopis, J., McCaffery, J.M., Miyawaki, A., Farquhar, M.G. and Tsien, R.Y. (1998) Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins. Proc. Natl Acad. Sci. USA, 95, 6803-6808.
25. Seaton, T.A., Cooper, J.M. and Schapira, A.H. (1997) Free radical scavengers protect dopaminergic cell lines from apoptosis induced by complex I inhibitors. Brain Res., 777, 110-118.
26. Pich, M.M., Castagnoli, A., Biondi, A., Bernacchia, A., Tazzari, P.L., D'Aurelio, M., Castelli, G.P., Formiggini, G., Conte, R., Bovina, C. et al. (2002) Ubiquinol and a coenzyme Q reducing system protect platelet mitochondrial function of transfusional buffy coats from oxidative stress. Free Radic. Res., 36, 429-436.
27. Houstek, J., Klement, P., Hermanska, J., Houstkova, H., Hansikova, H., Van den Bogert, C. and Zeman, J. (1995) Altered properties of mitochondrial ATP-synthase in patients with a T→G mutation in the ATPase 6 (subunit a) gene at position 8993 of mtDNA. Biochim. Biophys. Acta, 1271, 349-357.
28. Hartzog, P. E. and Cain, B.D. (1993) The aleu207→arg mutation in F1F0-ATP synthase from Escherichia coli. A model for human mitochondrial disease. J. Biol. Chem., 268, 12250-12252.
29. Ogilvie, I. and Capaldi, R.A. (1999) Mutation of the mitochrondrially encoded ATPase 6 gene modeled in the ATP synthase of Escherichia coli. FEBS Lett., 453, 179-182.
30. Carrozzo, R., Murray, J., Santorelli, F.M. and Capaldi, R.A. (2000) The T9176G mutation of human mtDNA gives a fully assembled but inactive ATP synthase when modeled in Escherichia coli. FEBS Lett., 486, 297-299.
31. Carelli, V., Baracca, A., Barogi, S., Pallotti, F., Valentino, M.L., Montagna, P., Zeviani, M., Pini, A., Lenaz, G., Baruzzi, A. et al. (2002) Biochemical-clinical correlation in patients with different loads of the mitochondrial DNA T8993G mutation. Arch. Neurol., 59, 264-270.
32. Trounce, I., Neill, S. and Wallace, D.C. (1994) Cytoplasmic transfer of the mtDNA nt 8993 T→G (ATP6) point mutation associated with Leigh syndrome into mtDNA-less cells demonstrates cosegregation with a decrease in state III respiration and ADP/O ratio. Proc. Natl Acad. Sci. USA, 91, 8334-8338.
33. Nicholls, D., Bernardi, P., Brand, M., Halestrap, A., Lemasters, J. and Reynolds, I. (2000) Apoptosis and the laws of thermodynamics. Nat. Cell Biol., 2, E172-173.
34. 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.
35. Nicholls, D.G., Budd, S.L., Castilho, R.F. and Ward, M.W. (1999) Glutamate excitotoxicity and neuronal energy metabolism. Ann. N Y Acad. Sci., 893, 1-12.
36. Carriere, A., Fernandez, Y., Rigoulet, M., Penicaud, L. and Casteilla, L. (2003) Inhibition of preadipocyte proliferation by mitochondrial reactive oxygen species. FEBS Lett., 550, 163-167.
37. Chantrel-Groussard, K., Geromel, V., Puccio, H., Koenig, M., Munnich, A., Rotig, A. and Rustin, P. (2001) Disabled early recruitment of antioxidant defenses in Friedreich's ataxia. Hum. Mol. Genet., 10, 2061-2067.
38. Manfredi, G., Fu, J., Ojaimi, J., Sadlock, J.E., Kwong, J.Q., Guy, J. and Schon, E.A. (2002) Rescue of a deficiency in ATP synthesis by transfer of MTATP6, a mitochondrial DNA-encoded gene, to the nucleus. Nat. Genet., 30, 394-399.
39. Guy, J., Qi, X., Pallotti, F., Schon, E.A., Manfredi, G., Carelli, V., Martinuzzi, A., Hauswirth, W.W. and Lewin, A.S. (2002) Rescue of a mitochondrial deficiency causing Leber hereditary optic neuropathy. Ann. Neurol., 52, 534-542.
40. Ojaimi, J., Pan, J., Santra, S., Snell, W.J. and Schon, E.A. (2002) An algal nucleus-encoded subunit of mitochondrial ATP synthase rescues a defect in the analogous human mitochondrial-encoded subunit. Mol. Biol. Cell, 13, 3836-3844.
41. Chinnery, P.F. and Turnbull, D.M. (1997) Clinical features, investigation, and management of patients with defects of mitochondrial DNA. J. Neurol. Neurosurg. Psychiat., 63, 559-563.
42. D'Aurelio, M., Pallotti, F., Barrientos, A., Gajewski, C.D., Kwong, J.Q., Bruno, C., Beal, M.F. and Manfredi, G. (2001) In vivo regulation of oxidative phosphorylation in cells harboring a stop-codon mutation in mitochondrial DNA-encoded cytochrome c oxidase subunit I. J. Biol. Chem., 276, 46925-46932.
43. Megli, F.M., Mattiazzi, M., Di Tullio, T. and Quagliariello, E. (2000) Annexin V binding perturbs the cardiolipin fluidity gradient in isolated mitochondria. Can it affect mitochondrial function? Biochemistry, 39, 5534-5542.
44. Manfredi, G., Yang, L., Gajewski, C.D. and Mattiazzi, M. (2002) Measurements of ATP in mammalian cells. Methods, 26, 317-326.
45. Morrison, J.E (1954) The activation of aconitase by ferrous ion and reducing agents. Biochem. J., 58, 685-692.
46. Marusich, M.F., Robinson, B.H., Taanman, J.W., Kim, S.J., Schillace, R., Smith, J.L. and Capaldi, R.A. (1997) Expression of mtDNA and nDNA encoded respiratory chain proteins in chemically and genetically-derived Rho0 human fibroblasts: a comparison of subunit proteins in normal fibroblasts treated with ethidium bromide and fibroblasts from a patient with mtDNA depletion syndrome. Biochim. Biophys. Acta, 1362, 145-159.
47. Gottlieb, R.A. and Granville, D.J. (2002) Analyzing mitochondrial changes during apoptosis. Methods, 26, 341-347.
48. Panickar, K.S., Jayakumar, A.R. and Norenberg, M.D. (2002) Differential response of neural cells to trauma-induced free radical production in vitro. Neurochem. Res., 27, 161-166.
49. Beauchamp, C. and Fridovich, I. (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal. Biochem., 44, 276-287.