Visualizing common deletion of mitochondrial DNA-augmented mitochondrial reactive oxygen species generation and apoptosis upon oxidative stress

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1762, Issue 2, 2006, Pages 241-255

  Peng, Tsung I ^a   Yu, Pei Ru ^b   Chen, Jing Yi ^b   Wang, Hung Li ^b   Wu, Hong Yeuh ^b   Wei, Yau Huei ^c   Jou, Mei Jie ^b  

^a CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

^c NATIONAL YANG MING UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; Electron transport chain; Mitochondrial DNA mutation; Mitochondrial membrane potential; Mitochondrial permeability transition pore; Mitochondrial reactive oxygen specie

Indexed keywords

CYTOCHROME C; DNA FRAGMENT; FLUORESCENT DYE; HYDROGEN PEROXIDE; MITOCHONDRIAL DNA; PHOSPHATIDYLSERINE; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; CYBRID; CYTOPATHOLOGY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME RELEASE; GENE DELETION; HUMAN; HUMAN CELL; HYPERPOLARIZATION; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL RESPIRATION; MULTIPHOTON MICROSCOPY; OXIDATIVE STRESS; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RESPIRATORY CHAIN; SIGNAL TRANSDUCTION;

APOPTOSIS; CASPASE 3; CASPASES; CELLS, CULTURED; CYTOCHROMES C; DNA, MITOCHONDRIAL; ENZYME ACTIVATION; GENE DELETION; HUMANS; HYDROGEN PEROXIDE; MITOCHONDRIA; MITOCHONDRIAL SWELLING; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SEQUENCE DELETION;

EID: 29344444706     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2005.10.008     Document Type: Article

References (54)

1. S. Anderson, A.T. Bankier, B.G. Barrell, M.H. de Bruijn, A.R. Coulson, J. Drouin, I.C. Eperon, D.P. Nierlich, B.A. Roe, F. Sanger, P.H. Schreier, A.J. Smith, R. Staden, and I.G. Young Sequence and organization of the human mitochondrial genome Nature 290 1981 457 465
2. D.C. Wallace Mitochondrial DNA sequence variation in human evolution and disease Proc. Natl. Acad. Sci. U. S. A. 91 1994 8739 8746
3. W.M. Brown, M. George Jr., and A.C. Wilson Rapid evolution of animal mitochondrial DNA Proc. Natl. Acad. Sci. U. S. A. 76 1979 1967 1971
4. D.C. Wallace 1994 William Allan Award Address. Mitochondrial DNA variation in human evolution, degenerative disease, and aging Am. J. Hum. Genet. 57 1995 201 223
5. I.J. Holt, J.M. Cooper, J.A. Morgan-Hughes, and A.E. Harding Deletions of muscle mitochondrial DNA Lancet 1 1988 1462
6. D.C. Wallace, G. Singh, M.T. Lott, J.A. Hodge, T.G. Schurr, A.M. Lezza, L.J. Elsas, and E.K. Nikoskelainen Mitochondrial DNA mutation associated with Leber's hereditary optic neuropathy Science 242 1988 1427 1430
7. D.C. Wallace Diseases of the mitochondrial DNA Annu. Rev. Biochem. 61 1992 1175 1212
8. D.C. Wallace Mitochondrial genetics: a paradigm for aging and degenerative diseases? Science 256 1992 628 632
9. G.A. Cortopassi, D. Shibata, N.W. Soong, and N. Arnheim A pattern of accumulation of a somatic deletion of mitochondrial DNA in aging human tissues Proc. Natl. Acad. Sci. U. S. A. 89 1992 7370 7374
10. J.M. Shoffner, M.T. Lott, A.S. Voljavec, S.A. Soueidan, D.A. Costigan, and D.C. Wallace Spontaneous Kearns-Sayre/chronic external ophthalmoplegia plus syndrome associated with a mitochondrial DNA deletion: a slip-replication model and metabolic therapy Proc. Natl. Acad. Sci. U. S. A. 86 1989 7952 7956
11. E.A. Schon, R. Rizzuto, C.T. Moraes, H. Nakase, M. Zeviani, and S. DiMauro A direct repeat is a hotspot for large-scale deletion of human mitochondrial DNA Science 244 1989 346 349
12. E.A. Schon, Y. Koga, M. Davidson, C.T. Moraes, and M.P. King The mitochondrial tRNA(Leu)(UUR)) mutation in MELAS: a model for pathogenesis Biochim. Biophys. Acta 1101 1992 206 209
13. I.J. Holt, A.E. Harding, J.M. Cooper, A.H. Schapira, A. Toscano, J.B. Clark, and J.A. Morgan-Hughes Mitochondrial myopathies: clinical and biochemical features of 30 patients with major deletions of muscle mitochondrial DNA Ann. Neurol. 26 1989 699 708
14. M. Corral-Debrinski, T. Horton, M.T. Lott, J.M. Shoffner, M.F. Beal, and D.C. Wallace Mitochondrial DNA deletions in human brain: regional variability and increase with advanced age Nat. Genet. 2 1992 324 329
15. J. Bereiter-Hahn, and M. Voth Dynamics of mitochondria in living cells: shape changes, dislocations, fusion, and fission of mitochondria Microsc. Res. Tech. 27 1994 198 219
16. R.N. Lightowlers, P.F. Chinnery, D.M. Turnbull, and N. Howell Mammalian mitochondrial genetics: heredity, heteroplasmy and disease Trends Genet. 13 1997 450 455
17. S. DiMauro Mitochondrial diseases Biochim. Biophys. Acta 1658 2004 80 88
18. W.K. Porteous, A.M. James, P.W. Sheard, C.M. Porteous, M.A. Packer, S.J. Hyslop, J.V. Melton, C.Y. Pang, Y.H. Wei, and M.P. Murphy Bioenergetic consequences of accumulating the common 4977-bp mitochondrial DNA deletion Eur. J. Biochem. 257 1998 192 201
19. L.A. Esposito, S. Melov, A. Panov, B.A. Cottrell, and D.C. Wallace Mitochondrial disease in mouse results in increased oxidative stress Proc. Natl. Acad. Sci. U. S. A. 96 1999 4820 4825
20. A. Boveris, and B. Chance The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen Biochem. J. 134 1973 707 716
21. J.F. Turrens Mitochondrial formation of reactive oxygen species J. Physiol. 552 2003 335 344
22. J.F. Turrens Superoxide production by the mitochondrial respiratory chain Biosci. Rep. 17 1997 3 8
23. M.J. Jou, S.B. Jou, H.M. Chen, C.H. Lin, and T.I. Peng Critical role of mitochondrial reactive oxygen species formation in visible laser irradiation-induced apoptosis in rat brain astrocytes (RBA-1) J. Biomed. Sci. 9 2002 507 516
24. S. Goldstein, D. Meyerstein, and G. Czapski The Fenton reagents Free Radic. Biol. Med. 15 1993 435 445
25. M.J. Jou, T.I. Peng, R.J. Reiter, S.B. Jou, H.Y. Wu, and S.T. Wen Visualization of the antioxidative effects of melatonin at the mitochondrial level during oxidative stress-induced apoptosis of rat brain astrocytes J. Pineal Res. 37 2004 55 70
26. 2 production in pigeon heart mitochondria FEBS Lett. 18 1971 261 264
27. M.J. Jou, S.B. Jou, M.J. Guo, H.Y. Wu, and T.I. Peng Mitochondrial reactive oxygen species generation and calcium increase induced by visible light in astrocytes Ann. N. Y. Acad. Sci. 1011 2004 45 56
28. T.I. Peng, and M.J. Jou Mitochondrial swelling and generation of reactive oxygen species induced by photoirradiation are heterogeneously distributed Ann. N. Y. Acad. Sci. 1011 2004 112 122
29. M.J. Jou, T.I. Peng, Y.H. Wang, Mechanistic investigation of visible laser irradiation-induced mitochondrial dysfunction in NARP cybrids harboring mitochondrial DNA 8993T > G point mutation, Biophys. J. (in press).
30. M.J. Jou, T.I. Peng, H.Y. Wu, and Y.H. Wei Enhanced generation of mitochondrial reactive oxygen species in cybrids containing 4977-bp mitochondrial DNA deletion Ann. N. Y. Acad. Sci. 1042 2005 221 228
31. J. Sastre, F.V. Pallardo, d.l.A. Garcia, and J. Vina Mitochondria, oxidative stress and aging Free Radic. Res. 32 2000 189 198
32. N. Li, K. Ragheb, G. Lawler, J. Sturgis, B. Rajwa, J.A. Melendez, and J.P. Robinson Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production J. Biol. Chem. 278 2003 8516 8525
33. M. Lai, H. Griffiths, H. Pall, A. Williams, and J. Lunec An investigation into the role of reactive oxygen species in the mechanism of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine toxicity using neuronal cell lines Biochem. Pharmacol. 45 1993 927 933
34. Q. Chen, E.J. Vazquez, S. Moghaddas, C.L. Hoppel, and E.J. Lesnefsky Production of reactive oxygen species by mitochondria: central role of complex III J. Biol. Chem. 278 2003 36027 36031
35. V. Geromel, N. Kadhom, I. Cebalos-Picot, O. Ouari, A. Polidori, A. Munnich, A. Rotig, and P. Rustin Superoxide-induced massive apoptosis in cultured skin fibroblasts harboring the neurogenic ataxia retinitis pigmentosa (NARP) mutation in the ATPase-6 gene of the mitochondrial DNA Hum. Mol Genet. 10 2001 1221 1228
36. S. Jiang, J. Cai, D.C. Wallace, and D.P. Jones Cytochrome c-mediated apoptosis in cells lacking mitochondrial DNA. Signaling pathway involving release and caspase 3 activation is conserved J. Biol. Chem. 274 1999 29905 29911
37. S.Y. Park, I. Chang, J.Y. Kim, S.W. Kang, S.H. Park, K. Singh, and M.S. Lee Resistance of mitochondrial DNA-depleted cells against cell death: role of mitochondrial superoxide dismutase J. Biol. Chem. 279 2004 7512 7520
38. D. Davermann, M. Martinez, J. McKoy, N. Patel, D. Averbeck, and C.W. Moore Impaired mitochondrial function protects against free radical-mediated cell death Free Radic. Biol. Med. 33 2002 1209 1220
39. J.L. Mott, D. Zhang, M. Stevens, S. Chang, G. Denniger, and H.P. Zassenhaus Oxidative stress is not an obligate mediator of disease provoked by mitochondrial DNA mutations Mutat. Res. 474 2001 35 45
40. M.P. King, and G. Attardi Injection of mitochondria into human cells leads to a rapid replacement of the endogenous mitochondrial DNA Cell 52 1988 811 819
41. M.P. King, and G. Attardi Human cells lacking mtDNA: repopulation with exogenous mitochondria by complementation Science 246 1989 500 503
42. M.J. Jou, T.I. Peng, Y.H. Wang, T.S. Chan, Subcellular investigation on the bioavailability of C60 derivatives, C3 and DF1, in protecting mitochondrial DNA point mutant-induced apoptosis. Nanomedicine (in press).
43. T.I. Peng, M.J. Jou, H.Y. Wu, Y.H. Wei, M.P. Murphy, and T. Ho Mitochondrial calcium and ROS mediated apoptosis plays a potential pathogenic role in diseases associated with mitochondrial DNA 4977 bp deletion Mitochondrion 4 2004 63
44. T.I. Peng, C.J. Chang, M.J. Jou, Photosensitizer Targeting: Mitochondrion-Targeted Photosensitizer Enhances Mitochondrial Reactive Oxygen Species and Mitochondrial Calcium-Mediated Apoptosis, Opt. Quantum Electron. (in press).
45. T.I. Peng, C.J. Chang, M.J. Guo, Y.H. Wang, J.S. Yu, H.Y. Wu, and M.J. Jou Mitochondrion-targeted photosensitizer enhances the photodynamic effect-induced mitochondrial dysfunction and apoptosis Ann. N.Y. Acad. Sci. 1042 2005 419 428
46. T.I. Peng, M.J. Jou, P.Z. Yu, Reverse mutant mitochondrial DNA to normal by photodynamic effect of mitochondria-targeted photosensitizer in common deletion of human mtDNA cybrids, Biophys. J. (in press).
47. S.S. Korshunov, V.P. Skulachev, and A.A. Starkov High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria FEBS Lett. 416 1997 15 18
48. J.J. Briere, D. Chretien, P. Benit, and P. Rustin Respiratory chain defects: what do we know for sure about their consequences in vivo? Biochim. Biophys. Acta 1659 2004 172 177
49. A.M. Lezza, D. Boffoli, S. Scacco, P. Cantatore, and M.N. Gadaleta Correlation between mitochondrial DNA 4977-bp deletion and respiratory chain enzyme activities in aging human skeletal muscles Biochem. Biophys. Res. Commun. 205 1994 772 779
50. R. Schroder, S. Vielhaber, F.R. Wiedemann, C. Kornblum, A. Papassotiropoulos, P. Broich, S. Zierz, C.E. Elger, H. Reichmann, P. Seibel, T. Klockgether, and W.S. Kunz New insights into the metabolic consequences of large-scale mtDNA deletions: a quantitative analysis of biochemical, morphological, and genetic findings in human skeletal muscle J. Neuropathol. Exp. Neurol. 59 2000 353 360
51. S.M. Cardoso, A.C. Rego, N. Penacho, and C.R. Oliveira Apoptotic cell death induced by hydrogen peroxide in NT2 parental and mitochondrial DNA depleted cells Neurochem. Int. 45 2004 693 698
52. 2+ cycling and membrane damage during tert-butyl hydroperoxide metabolism by rat-liver mitochondria Eur. J. Biochem. 140 1984 1 6
53. B. Frei, and C. Richter Mono(ADP-ribosylation) in rat liver mitochondria Biochemistry 27 1988 529 535
54. H.R. Lotscher, K.H. Winterhalter, E. Carafoli, and C. Richter Hydroperoxides can modulate the redox state of pyridine nucleotides and the calcium balance in rat liver mitochondria Proc. Natl. Acad. Sci. U. S. A. 76 1979 4340 4344