Mitochondrial DNA, base excision repair and neurodegeneration

DNA Repair

Volumn 7, Issue 7, 2008, Pages 1098-1109

  de Souza Pinto, Nadja C ^a   Wilson III, David M ^a   Stevnsner, Tinna V ^b   Bohr, Vilhelm A ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

8 oxoG; BER; DNA glycosylase; Mitochondrial DNA; Oxidative damage

Indexed keywords

DNA GLYCOSYLTRANSFERASE; MITOCHONDRIAL DNA;

ALZHEIMER DISEASE; ARTICLE; CELL DEATH; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA DAMAGE; EXCISION REPAIR; HUMAN; HUNTINGTON CHOREA; NERVE DEGENERATION; NERVOUS TISSUE; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PREMATURE AGING; PRIORITY JOURNAL;

ANIMALS; DNA DAMAGE; DNA REPAIR; DNA, MITOCHONDRIAL; HUMANS; MITOCHONDRIA; MODELS, BIOLOGICAL; NEURODEGENERATIVE DISEASES; NEURONS; OXIDATIVE STRESS;

EID: 44949168388     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2008.03.011     Document Type: Article

References (144)

1. Cummings J.L., and Jeste D.V. Alzheimer's disease and its management in the year 2010. Psychiatr. Serv. 50 (1999) 1173-1177
2. Wilson III D.M., and Mattson M.P. Neurodegeneration: nicked to death. Curr. Biol. 17 (2007) R55-R58
3. Harman D. The biologic clock: the mitochondria?. J. Am. Geriatr Soc. 20 (1972) 145-147
4. Vina J., Borras C., and Miquel J. Theories of ageing. IUBMB Life 59 (2007) 249-254
5. McFarland R., Taylor R.W., and Turnbull D.M. Mitochondrial disease - its impact, etiology, and pathology. Curr. Top. Dev. Biol. 77 (2007) 113-155
6. Wong L.J. Diagnostic challenges of mitochondrial DNA disorders. Mitochondrion 7 (2007) 45-52
7. Morava E., van den H.L., Hol F., de Vries M.C., Hogeveen M., Rodenburg R.J., and Smeitink J.A. Mitochondrial disease criteria: diagnostic applications in children. Neurology 67 (2006) 1823-1826
8. Greenamyre J.T., Sherer T.B., Betarbet R., and Panov A.V. Complex I and Parkinson's disease. IUBMB Life 52 (2001) 135-141
9. Schapira A.H. Mitochondrial dysfunction in Parkinson's disease. Cell Death Differ. 14 (2007) 1261-1266
10. Browne S.E., and Beal M.F. Toxin-induced mitochondrial dysfunction. Int. Rev. Neurobiol. 53 (2002) 243-279
11. Davis G.C., Williams A.C., Markey S.P., Ebert M.H., Caine E.D., Reichert C.M., and Kopin I.J. Chronic Parkinsonism secondary to intravenous injection of meperidine analogues. Psychiatry Res. 1 (1979) 249-254
12. Chiba K., Trevor A., and Castagnoli Jr. N. Metabolism of the neurotoxic tertiary amine, MPTP, by brain monoamine oxidase. Biochem. Biophys. Res. Commun. 120 (1984) 574-578
13. Nicklas W.J., Vyas I., and Heikkila R.E. Inhibition of NADH-linked oxidation in brain mitochondria by 1-methyl-4-phenyl-pyridine, a metabolite of the neurotoxin, 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine. Life Sci. 36 (1985) 2503-2508
14. Heikkila R.E., Nicklas W.J., Vyas I., and Duvoisin R.C. Dopaminergic toxicity of rotenone and the 1-methyl-4-phenylpyridinium ion after their stereotaxic administration to rats: implication for the mechanism of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine toxicity. Neurosci. Lett. 62 (1985) 389-394
15. Ramsay R.R., Salach J.I., Dadgar J., and Singer T.P. Inhibition of mitochondrial NADH dehydrogenase by pyridine derivatives and its possible relation to experimental and idiopathic Parkinsonism. Biochem. Biophys. Res. Commun. 135 (1986) 269-275
16. Cosi C., Colpaert F., Koek W., Degryse A., and Marien M. Poly(ADP-ribose) polymerase inhibitors protect against MPTP-induced depletions of striatal dopamine and cortical noradrenaline in C57B1/6 mice. Brain Res. 729 (1996) 264-269
17. Cosi C., and Marien M. Implication of poly (ADP-ribose) polymerase (PARP) in neurodegeneration and brain energy metabolism. Decreases in mouse brain NAD+ and ATP caused by MPTP are prevented by the PARP inhibitor benzamide. Ann. N. Y. Acad. Sci. 890 (1999) 227-239
18. Browne S.E., and Beal M.F. The energetics of Huntington's disease. Neurochem. Res. 29 (2004) 531-546
19. Browne S.E., Bowling A.C., MacGarvey U., Baik M.J., Berger S.C., Muqit M.M., Bird E.D., and Beal M.F. Oxidative damage and metabolic dysfunction in Huntington's disease: selective vulnerability of the basal ganglia. Ann. Neurol. 41 (1997) 646-653
20. Browne S.E., Ferrante R.J., and Beal M.F. Oxidative stress in Huntington's disease. Brain Pathol. 9 (1999) 147-163
21. Albring M., Griffith J., and Attardi G. Association of a protein structure of probable membrane derivation with HeLa cell mitochondrial DNA near its origin of replication. Proc. Natl. Acad. Sci. U.S.A. 74 (1977) 1348-1352
22. Cadenas E., and Davies K.J. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic. Biol. Med. 29 (2000) 222-230
23. Ward J.F. Biochemistry of DNA lesions. Radiat. Res. Suppl. 8 (1985) S103-S111
24. Cadenas E. Biochemistry of oxygen toxicity. Annu. Rev. Biochem. 58 (1989) 79-110
25. Richter C., Park J.W., and Ames B.N. Normal oxidative damage to mitochondrial and nuclear DNA is extensive. Proc. Natl. Acad. Sci. U.S.A. 85 (1988) 6465-6467
26. Hudson E.K., Hogue B.A., Souza-Pinto N.C., Croteau D.L., Anson R.M., Bohr V.A., and Hansford R.G. Age-associated change in mitochondrial DNA damage. Free Radic. Res. 29 (1998) 573-579
27. Mori T., Hori Y., and Dizdaroglu M. DNA base damage generated in vivo in hepatic chromatin of mice upon whole body gamma-irradiation. Int. J. Radiat. Biol. 64 (1993) 645-650
28. Kasai H., Crain P.F., Kuchino Y., Nishimura S., Ootsuyama A., and Tanooka H. Formation of 8-hydroxyguanine moiety in cellular DNA by agents producing oxygen radicals and evidence for its repair. Carcinogenesis 7 (1986) 1849-1851
29. Kohda K., Tada M., Kasai H., Nishimura S., and Kawazoe Y. Formation of 8-hydroxyguanine residues in cellular DNA exposed to the carcinogen 4-nitroquinoline 1-oxide. Biochem. Biophys. Res. Commun. 139 (1986) 626-632
30. Grollman A.P., and Moriya M. Mutagenesis by 8-oxoguanine: an enemy within. Trends Genet. 9 (1993) 246-249
31. Pinz K.G., Shibutani S., and Bogenhagen D.F. Action of mitochondrial DNA polymerase gamma at sites of base loss or oxidative damage. J. Biol. Chem. 270 (1995) 9202-9206
32. Maga G., Villani G., Crespan E., Wimmer U., Ferrari E., Bertocci B., and Hubscher U. 8-oxo-guanine bypass by human DNA polymerases in the presence of auxiliary proteins. Nature 447 (2007) 606-608
33. Charlet-Berguerand N., Feuerhahn S., Kong S.E., Ziserman H., Conaway J.W., Conaway R., and Egly J.M. RNA polymerase II bypass of oxidative DNA damage is regulated by transcription elongation factors. EMBO J. 25 (2006) 5481-5491
34. Stuart J.A., Bourque B.M., Souza-Pinto N.C., and Bohr V.A. No evidence of mitochondrial respiratory dysfunction in OGG1-null mice deficient in removal of 8-oxodeoxyguanine from mitochondrial DNA. Free Radic. Biol. Med. 38 (2005) 737-745
35. Souza-Pinto N.C., Eide L., Hogue B.A., Thybo T., Stevnsner T., Seeberg E., Klungland A., and Bohr V.A. Repair of 8-oxodeoxyguanosine lesions in mitochondrial DNA depends on the oxoguanine DNA glycosylase (OGG1) gene and 8-oxoguanine accumulates in the mitochondrial DNA of OGG1-defective mice. Cancer Res. 61 (2001) 5378-5381
36. Wirtz M., Schumann C.A., Schellentrager M., Gab S., Vom B.J., Podeschwa M.A., Altenbach H.J., Oscier D., and Schmitz O.J. Capillary electrophoresis-laser induced fluorescence analysis of endogenous damage in mitochondrial and genomic DNA. Electrophoresis 26 (2005) 2599-2607
37. Clark J.M., and Beardsley G.P. Thymine glycol lesions terminate chain elongation by DNA polymerase I in vitro. Nucleic Acids Res. 14 (1986) 737-749
38. Hu J., Souza-Pinto N.C., Haraguchi K., Hogue B.A., Jaruga P., Greenberg M.M., Dizdaroglu M., and Bohr V.A. Repair of formamidopyrimidines in DNA involves different glycosylases: role of the OGG1, NTH1 and NEIL1 enzymes. J. Biol. Chem. 280 (2005) 40544-40551
39. Wiederholt C.J., and Greenberg M.M. Fapy.dG instructs Klenow exo(-) to misincorporate deoxyadenosine. J. Am. Chem. Soc. 124 (2002) 7278-7279
40. Delaney M.O., Wiederholt C.J., and Greenberg M.M. Fapy.dA induces nucleotide misincorporation translesionally by a DNA polymerase. Angew. Chem. Int. Ed. Engl. 41 (2002) 771-773
41. Shigenaga M.K., Hagen T.M., and Ames B.N. Oxidative damage and mitochondrial decay in aging. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 10771-10778
42. Higuchi Y.L.S. Purification of all forms of HeLa cell mitochondrial DNA and assessment of damage to it caused by hydrogen peroxide treatment of mitochondria or cells. J. Biol. Chem. 270 (1995) 7950-7956
43. Hamilton M.L., Guo Z., Fuller C.D., Van Remmen H., Ward W.F., Austad S.N., Troyer D.A., Thompson I., and Richardson A. A reliable assessment of 8-oxo-2-deoxyguanosine levels in nuclear and mitochondrial DNA using the sodium iodide method to isolate DNA. Nucleic Acids Res. 29 (2001) 2117-2126
44. Barja G., and Herrero A. Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. FASEB J. 14 (2000) 312-318
45. Hoeijmakers J.H. Genome maintenance mechanisms for preventing cancer. Nature 411 (2001) 366-374
46. Hashiguchi K., Bohr V.A., and Souza-Pinto N.C. Oxidative stress and mitochondrial DNA repair: implications for NRTIs induced DNA damage. Mitochondrion 4 (2004) 215-222
47. Takao M., Aburatani H., Kobayashi K., and Yasui A. Mitochondrial targeting of human DNA glycosylases for repair of oxidative DNA damage. Nucleic Acids Res. 26 (1998) 2917-2922
48. Nishioka K., Ohtsubo T., Oda H., Fujiwara T., Kang D., Sugimachi K., and Nakabeppu Y. Expression and differential intracellular localization of two major forms of human 8-oxoguanine DNA glycosylase encoded by alternatively spliced OGG1 mRNAs. Mol. Biol. Cell 10 (1999) 1637-1652
49. Hashiguchi K., Stuart J.A., Souza-Pinto N.C., and Bohr V.A. The C-terminal alphaO helix of human Ogg1 is essential for 8-oxoguanine DNA glycosylase activity: the mitochondrial beta-Ogg1 lacks this domain and does not have glycosylase activity. Nucleic Acids Res. 32 (2004) 5596-5608
50. Bjoras M., Luna L., Johnsen B., Hoff E., Haug T., Rognes T., and Seeberg E. Opposite base-dependent reactions of a human base excision repair enzyme on DNA containing 7,8-dihydro-8-oxoguanine and abasic sites. EMBO J. 16 (1997) 6314-6322
51. Dherin C., Radicella J.P., Dizdaroglu M., and Boiteux S. Excision of oxidatively damaged DNA bases by the human alpha-hOgg1 protein and the polymorphic alpha-hOgg1(Ser326Cys) protein which is frequently found in human populations. Nucleic Acids Res. 27 (1999) 4001-4007
52. Zharkov D.O., Rosenquist T.A., Gerchman S.E., and Grollman A.P. Substrate specificity and reaction mechanism of murine 8-oxoguanine-DNA glycosylase. J. Biol. Chem. 275 (2000) 28607-28617
53. Jensen A., Calvayrac G., Karahalil B., Bohr V.A., and Stevnsner T. Mammalian 8-oxoguanine DNA glycosylase 1 incises 8-oxoadenine opposite cytosine in nuclei and mitochondria, while a different glycosylase incises 8-oxoadenine opposite guanine in nuclei. J. Biol. Chem. 278 (2003) 19541-19548
54. Michaels M.L., and Miller J.H. The GO system protects organisms from the mutagenic effect of the spontaneous lesion 8-hydroxyguanine (7,8-dihydro-8-oxoguanine). J. Bacteriol. 174 (1992) 6321-6325
55. Takao M., Zhang Q.M., Yonei S., and Yasui A. Differential subcellular localization of human MutY homolog (hMYH) and the functional activity of adenine: 8-oxoguanine DNA glycosylase. Nucleic Acids Res. 27 (1999) 3638-3644
56. Ohtsubo T., Nishioka K., Imaiso Y., Iwai S., Shimokawa H., Oda H., Fujiwara T., and Nakabeppu Y. Identification of human MutY homolog (hMYH) as a repair enzyme for 2-hydroxyadenine in DNA and detection of multiple forms of hMYH located in nuclei and mitochondria. Nucleic Acids Res. 28 (2000) 1355-1364
57. Luna L., Bjoras M., Hoff E., Rognes T., and Seeberg E. Cell-cycle regulation, intracellular sorting and induced overexpression of the human NTH1 DNA glycosylase involved in removal of formamidopyrimidine residues from DNA. Mutat. Res. 460 (2000) 95-104
58. Ikeda S., Kohmoto T., Tabata R., and Seki Y. Differential intracellular localization of the human and mouse endonuclease III homologs and analysis of the sorting signals. DNA Repair (Amst) 1 (2002) 847-854
59. Karahalil B., Souza-Pinto N.C., Parsons J.L., Elder R.H., and Bohr V.A. Compromised incision of oxidized pyrimidines in liver mitochondria of mice deficient in NTH1 and OGG1 glycosylases. J. Biol. Chem. 278 (2003) 33701-33707
60. Hazra T.K., Izumi T., Boldogh I., Imhoff B., Kow Y.W., Jaruga P., Dizdaroglu M., and Mitra S. Identification and characterization of a human DNA glycosylase for repair of modified bases in oxidatively damaged DNA. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 3523-3528
61. Bandaru V., Sunkara S., Wallace S.S., and Bond J.P. A novel human DNA glycosylase that removes oxidative DNA damage and is homologous to Escherichia coli endonuclease VIII. DNA Repair (Amst) 1 (2002) 517-529
62. Rosenquist T.A., Zaika E., Fernandes A.S., Zharkov D.O., Miller H., and Grollman A.P. The novel DNA glycosylase, NEIL1, protects mammalian cells from radiation-mediated cell death. DNA Repair (Amst) 2 (2003) 581-591
63. Vartanian V., Lowell B., Minko I.G., Wood T.G., Ceci J.D., George S., Ballinger S.W., Corless C.L., McCullough A.K., and Lloyd R.S. The metabolic syndrome resulting from a knockout of the NEIL1 DNA glycosylase. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 1864-1869
64. Jaruga P., Birincioglu M., Rosenquist T.A., and Dizdaroglu M. Mouse NEIL1 protein is specific for excision of 2,6-diamino-4-hydroxy-5-formamidopyrimidine and 4,6-diamino-5-formamidopyrimidine from oxidatively damaged DNA. Biochemistry 43 (2004) 15909-15914
65. Nilsen H., Otterlei M., Haug T., Solum K., Nagelhus T.A., Skorpen F., and Krokan H.E. Nuclear and mitochondrial uracil-DNA glycosylases are generated by alternative splicing and transcription from different positions in the UNG gene. Nucleic Acids Res. 21 (1997) 2579-2584
66. Dizdaroglu M., Karakaya A., Jaruga P., Slupphaug G., and Krokan H.E. Novel activities of human uracil DNA N-glycosylase for cytosine-derived products of oxidative DNA damage. Nucleic Acids Res. 24 (1996) 418-422
67. Izumi T., Tatsuka M., Tano K., Asano M., and Mitra S. Molecular cloning and characterization of the promoter of the human N-methylpurine-DNA glycosylase (MPG) gene. Carcinogenesis 18 (1997) 1837-1839
68. Satoh M.S., Huh N., Rajewsky M.F., and Kuroki T. Enzymatic removal of O6-ethylguanine from mitochondrial DNA in rat tissues exposed to N-ethyl-N-nitrosourea in vivo. J. Biol. Chem. 263 (1988) 6854-6856
69. Myers K.A., Saffhill R., and O Connor P.J. Repair of alkylated purines in the hepatic DNA of mitochondria and nuclei in the rat. Carcinogenesis 9 (1988) 285-292
70. Pettepher C.C., LeDoux S.P., Bohr V.A., and Wilson G.L. Repair of alkali-labile sites within the mitochondrial DNA of RINr 38 cells after exposure to the nitrosourea streptozotocin. J. Biol. Chem. 266 (1991) 3113-3117
71. LeDoux S.P., Patton N.J., Avery L.J., and Wilson G.L. Repair of N-methylpurines in the mitochondrial DNA of xeroderma pigmentosum complementation group D cells. Carcinogenesis 14 (1993) 913-917
72. Jackson E.B., Theriot C.A., Chattopadhyay R., Mitra S., and Izumi T. Analysis of nuclear transport signals in the human apurinic/apyrimidinic endonuclease (APE1/Ref1). Nucleic Acids Res. 33 (2005) 3303-3312
73. Tomkinson A.E., Bonk R.T., and Linn S. Mitochondrial endonuclease activities specific for apurinic/apyrimidinic sites in DNA from mouse cells. J. Biol. Chem. 263 (1988) 12532-12537
74. Tell G., Crivellato E., Pines A., Paron I., Pucillo C., Manzini G., Bandiera A., Kelley M.R., Di Loreto C., and Damante G. Mitochondrial localization of APE/Ref-1 in thyroid cells. Mutat. Res. 485 (2001) 143-152
75. Frossi B., Tell G., Spessotto P., Colombatti A., Vitale G., and Pucillo C. H(2)O(2) induces translocation of APE/Ref-1 to mitochondria in the Raji B-cell line. J. Cell Physiol. 193 (2002) 180-186
76. Chattopadhyay R., Wiederhold L., Szczesny B., Boldogh I., Hazra T.K., Izumi T., and Mitra S. Identification and characterization of mitochondrial abasic (AP)-endonuclease in mammalian cells. Nucleic Acids Res. 34 (2006) 2067-2076
77. Tsuchimoto D., Sakai Y., Sakumi K., Nishioka K., Sasaki M., Fujiwara T., and Nakabeppu Y. Human APE2 protein is mostly localized in the nuclei and to some extent in the mitochondria, while nuclear APE2 is partly associated with proliferating cell nuclear antigen. Nucleic Acids Res. 29 (2001) 2349-2360
78. Hadi M.Z., Ginalski K., Nguyen L.H., and Wilson III D.M. Determinants in nuclease specificity of Ape1 and Ape2, human homologues of Escherichia coli exonuclease III. J. Mol. Biol. 316 (2002) 853-866
79. Graziewicz M.A., Longley M.J., and Copeland W.C. DNA polymerase gamma in mitochondrial DNA replication and repair. Chem. Rev. 106 (2006) 383-405
80. Lim S.E., Longley M.J., and Copeland W.C. The mitochondrial p55 accessory subunit of human DNA polymerase gamma enhances DNA binding, promotes processive DNA synthesis, and confers N-ethylmaleimide resistance. J. Biol. Chem. 274 (1999) 38197-38203
81. Johnson A.A., Tsai Y., Graves S.W., and Johnson K.A. Human mitochondrial DNA polymerase holoenzyme: reconstitution and characterization. Biochemistry 39 (2000) 1702-1708
82. Longley M.J., Prasad R., Srivastava D.K., Wilson S.H., and Copeland W.C. Identification of 5'-deoxyribose phosphate lyase activity in human DNA polymerase gamma and its role in mitochondrial base excision repair in vitro [In Process Citation]. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 12244-12248
83. Pinz K.G., and Bogenhagen D.F. The influence of the DNA polymerase gamma accessory subunit on base excision repair by the catalytic subunit. DNA Repair (Amst) 5 (2006) 121-128
84. Lakshmipathy U., and Campbell C. The human DNA ligase III gene encodes nuclear and mitochondrial proteins. Mol. Cell Biol. 19 (1999) 3869-3876
85. Lakshmipathy U., and Campbell C. Mitochondrial DNA ligase III function is independent of Xrcc1. Nucleic Acids Res. 28 (2000) 3880-3886
86. Thompson L.H., and West M.G. XRCC1 keeps DNA from getting stranded. Mutat. Res. 459 (2000) 1-18
87. Wang J., Xiong S., Xie C., Markesbery W.R., and Lovell M.A. Increased oxidative damage in nuclear and mitochondrial DNA in Alzheimer's disease. J. Neurochem. 93 (2005) 953-962
88. Wang J., Markesbery W.R., and Lovell M.A. Increased oxidative damage in nuclear and mitochondrial DNA in mild cognitive impairment. J. Neurochem. 96 (2006) 825-832
89. Weissman L., Jo D.G., Sorensen M.M., Souza-Pinto N.C., Markesbery W.R., Mattson M.P., and Bohr V.A. Defective DNA base excision repair in brain from individuals with Alzheimer's disease and amnestic mild cognitive impairment. Nucleic Acids Res. 35 (2007) 5545-5555
90. Bancher C., Braak H., Fischer P., and Jellinger K.A. Neuropathological staging of Alzheimer lesions and intellectual status in Alzheimer's and Parkinson's disease patients. Neurosci. Lett. 162 (1993) 179-182
91. Zhang J., Perry G., Smith M.A., Robertson D., Olson S.J., Graham D.G., and Montine T.J. Parkinson's disease is associated with oxidative damage to cytoplasmic DNA and RNA in substantia nigra neurons. Am. J. Pathol. 154 (1999) 1423-1429
92. Howell N., Elson J.L., Chinnery P.F., and Turnbull D.M. mtDNA mutations and common neurodegenerative disorders. Trends Genet. 21 (2005) 583-586
93. Lin F.H., Lin R., Wisniewski H.M., Hwang Y.W., Grundke-Iqbal I., Healy-Louie G., and Iqbal K. Detection of point mutations in codon 331 of mitochondrial NADH dehydrogenase subunit 2 in Alzheimer's brains. Biochem. Biophys. Res. Commun. 182 (1992) 238-246
94. Petruzzella V., Chen X., and Schon E.A. Is a point mutation in the mitochondrial ND2 gene associated with Alzheimer's disease. Biochem. Biophys. Res. Commun. 186 (1992) 491-497
95. Kosel S., Egensperger R., Mehraein P., and Graeber M.B. No association of mutations at nucleotide 5460 of mitochondrial NADH dehydrogenase with Alzheimer's disease. Biochem. Biophys. Res. Commun. 203 (1994) 745-749
96. Chang S.W., Zhang D., Chung H.D., and Zassenhaus H.P. The frequency of point mutations in mitochondrial DNA is elevated in the Alzheimer's brain. Biochem. Biophys. Res. Commun. 273 (2000) 203-208
97. Shoffner J.M., Brown M.D., Torroni A., Lott M.T., Cabell M.F., Mirra S.S., Beal M.F., Yang C.C., Gearing M., and Salvo R. Mitochondrial DNA variants observed in Alzheimer disease and Parkinson disease patients. Genomics 17 (1993) 171-184
98. Hutchin T., and Cortopassi G. A mitochondrial DNA clone is associated with increased risk for Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 6892-6895
99. Davis R.E., Miller S., Herrnstadt C., Ghosh S.S., Fahy E., Shinobu L.A., Galasko D., Thal L.J., Beal M.F., Howell N., and Parker Jr. W.D. Mutations in mitochondrial cytochrome c oxidase genes segregate with late-onset Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 4526-4531
100. Coskun P.E., Beal M.F., and Wallace D.C. Alzheimer's brains harbor somatic mtDNA control-region mutations that suppress mitochondrial transcription and replication. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 10726-10731
101. Blanchard B.J., Park T., Fripp W.J., Lerman L.S., and Ingram V.M. A mitochondrial DNA deletion in normally aging and in Alzheimer brain tissue. Neuroreport 4 (1993) 799-802
102. Corral-Debrinski M., Horton T., Lott M.T., Shoffner J.M., Beal M.F., and Wallace D.C. Mitochondrial DNA deletions in human brain: regional variability and increase with advanced age. Nat. Genet. 2 (1992) 324-329
103. Hamblet N.S., and Castora F.J. Elevated levels of the Kearns-Sayre syndrome mitochondrial DNA deletion in temporal cortex of Alzheimer's patients. Mutat. Res. 379 (1997) 253-262
104. Lezza A.M., Mecocci P., Cormio A., Beal M.F., Cherubini A., Cantatore P., Senin U., and Gadaleta M.N. Mitochondrial DNA 4977 bp deletion and OH8dG levels correlate in the brain of aged subjects but not Alzheimer's disease patients. FASEB J. 13 (1999) 1083-1088
105. Payami H., and Hoffbuhr K. Lack of evidence for maternal effect in familial Alzheimer's disease. Genet. Epidemiol. 10 (1993) 461-464
106. Janetzky B., Schmid C., Bischof F., Frolich L., Gsell W., Kalaria R.N., Riederer P., and Reichmann H. Investigations on the point mutations at nt 5460 of the mtDNA in different neurodegenerative and neuromuscular diseases. Eur. Neurol. 36 (1996) 149-153
107. Zsurka G., Kalman J., Csaszar A., Rasko I., Janka Z., and Venetianer P. No mitochondrial haplotype was found to increase risk for Alzheimer's disease. Biol. Psychiatry 44 (1998) 371-373
108. Garcia-Lozano J.R., Mir P., Alberca R., Aguilera I., Gil N.E., Fernandez-Lopez O., Cayuela A., and Nunez-Roldan A. Mitochondrial DNA A4336G mutation in Alzheimer's and Parkinson's diseases. Eur. Neurol. 48 (2002) 34-36
109. Wallace D.C., Stugard C., Murdock D., Schurr T., and Brown M.D. Ancient mtDNA sequences in the human nuclear genome: a potential source of errors in identifying pathogenic mutations. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 14900-14905
110. Cantuti-Castelvetri I., Lin M.T., Zheng K., Keller-McGandy C.E., Betensky R.A., Johns D.R., Beal M.F., Standaert D.G., and Simon D.K. Somatic mitochondrial DNA mutations in single neurons and glia. Neurobiol. Aging 26 (2005) 1343-1355
111. Thomas B., and Beal M.F. Parkinson's disease. Hum. Mol. Genet. 16 Spec. no. 2 (2007) R183-R194
112. Ikebe S., Tanaka M., and Ozawa T. Point mutations of mitochondrial genome in Parkinson's disease. Brain Res. Mol. Brain Res. 28 (1995) 281-295
113. Ozawa T., Tanaka M., Ino H., Ohno K., Sano T., Wada Y., Yoneda M., Tanno Y., Miyatake T., and Tanaka T. Distinct clustering of point mutations in mitochondrial DNA among patients with mitochondrial encephalomyopathies and with Parkinson's disease. Biochem. Biophys. Res. Commun. 176 (1991) 938-946
114. Mayr-Wohlfart U., Rodel G., and Henneberg A. Mitochondrial tRNA(Gln) and tRNA(Thr) gene variants in Parkinson's disease. Eur. J. Med. Res. 2 (1997) 111-113
115. Autere J., Moilanen J.S., Finnila S., Soininen H., Mannermaa A., Hartikainen P., Hallikainen M., and Majamaa K. Mitochondrial DNA polymorphisms as risk factors for Parkinson's disease and Parkinson's disease dementia. Hum. Genet. 115 (2004) 29-35
116. Smigrodzki R., Parks J., and Parker W.D. High frequency of mitochondrial complex I mutations in Parkinson's disease and aging. Neurobiol. Aging 25 (2004) 1273-1281
117. Manfredi G. mtDNA clock runs out for dopaminergic neurons. Nat. Genet. 38 (2006) 507-508
118. Kraytsberg Y., Kudryavtseva E., McKee A.C., Geula C., Kowall N.W., and Khrapko K. Mitochondrial DNA deletions are abundant and cause functional impairment in aged human substantia nigra neurons. Nat. Genet. 38 (2006) 518-520
119. Bender A., Krishnan K.J., Morris C.M., Taylor G.A., Reeve A.K., Perry R.H., Jaros E., Hersheson J.S., Betts J., Klopstock T., Taylor R.W., and Turnbull D.M. High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease. Nat. Genet. 38 (2006) 515-517
120. Ferman T.J., and Boeve B.F. Dementia with Lewy bodies. Neurol. Clin. 25 (2007) 741-760 (vii)
121. Martin L.J. Transgenic mice with human mutant genes causing Parkinson's disease and amyotrophic lateral sclerosis provide common insight into mechanisms of motor neuron selective vulnerability to degeneration. Rev. Neurosci. 18 (2007) 115-136
122. Martin L.J., Pan Y., Price A.C., Sterling W., Copeland N.G., Jenkins N.A., Price D.L., and Lee M.K. Parkinson's disease alpha-synuclein transgenic mice develop neuronal mitochondrial degeneration and cell death. J. Neurosci. 26 (2006) 41-50
123. Ekstrand M.I., Terzioglu M., Galter D., Zhu S., Hofstetter C., Lindqvist E., Thams S., Bergstrand A., Hansson F.S., Trifunovic A., Hoffer B., Cullheim S., Mohammed A.H., Olson L., and Larsson N.G. Progressive Parkinsonism in mice with respiratory-chain-deficient dopamine neurons. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 1325-1330
124. Trifunovic A., Wredenberg A., Falkenberg M., Spelbrink J.N., Rovio A.T., Bruder C.E., Bohlooly Y., Gidlof S., Oldfors A., Wibom R., Tornell J., Jacobs H.T., and Larsson N.G. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429 (2004) 417-423
125. Kujoth G.C., Hiona A., Pugh T.D., Someya S., Panzer K., Wohlgemuth S.E., Hofer T., Seo A.Y., Sullivan R., Jobling W.A., Morrow J.D., Van Remmen H., Sedivy J.M., Yamasoba T., Tanokura M., Weindruch R., Leeuwenburgh C., and Prolla T.A. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309 (2005) 481-484
126. Vermulst M., Bielas J.H., Kujoth G.C., Ladiges W.C., Rabinovitch P.S., Prolla T.A., and Loeb L.A. Mitochondrial point mutations do not limit the natural lifespan of mice. Nat. Genet. 39 (2007) 540-543
127. Orrenius S., Gogvadze V., and Zhivotovsky B. Mitochondrial oxidative stress: implications for cell death. Annu. Rev. Pharmacol. Toxicol. 47 (2007) 143-183
128. Trifunovic A., Hansson A., Wredenberg A., Rovio A.T., Dufour E., Khvorostov I., Spelbrink J.N., Wibom R., Jacobs H.T., and Larsson N.G. Somatic mtDNA mutations cause aging phenotypes without affecting reactive oxygen species production. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 17993-17998
129. Maclean M.J., Aamodt R., Harris N., Alseth I., Seeberg E., Bjoras M., and Piper P.W. Base excision repair activities required for yeast to attain a full chronological life span. Aging Cell 2 (2003) 93-104
130. Hart R.W., and Setlow R.B. Correlation between deoxyribonucleic acid excision repair and life span in a number of mammalian species. Proceedings of the National Academy of Sciences of the United States of America J1 - Proceedings of the National Academy of Sciences USA J2 - PNAS. Proc. Natl. Acad. Sci. U.S.A. 71 (1974) 2169-2173
131. Souza-Pinto N.C., Croteau D.L., Hudson E.K., Hansford R.G., and Bohr V.A. Age-associated increase in 8-oxo-deoxyguanosine glycosylase/AP lyase activity in rat mitochondria. Nucleic Acids. Res 27 (1999) 1935-1942
132. Souza-Pinto N.C., Hogue B.A., and Bohr V.A. DNA repair and aging in mouse liver: 8-oxodG glycosylase activity increase in mitochondrial but not in nuclear extracts. Free Radic. Biol. Med. 30 (2001) 916-923
133. Szczesny B., and Mitra S. Effect of aging on intracellular distribution of abasic (AP) endonuclease 1 in the mouse liver. Mech. Ageing Dev. 126 (2005) 1071-1078
134. Imam S.Z., Karahalil B., Hogue B.A., Souza-Pinto N.C., and Bohr V.A. Mitochondrial and nuclear DNA-repair capacity of various brain regions in mouse is altered in an age-dependent manner. Neurobiol. Aging (2005)
135. Chen D., Cao G., Hastings T., Feng Y., Pei W., O'Horo C., and Chen J. Age-dependent decline of DNA repair activity for oxidative lesions in rat brain mitochondria. J. Neurochem. 81 (2002) 1273-1284
136. Atamna H., Cheung I., and Ames B.N. A method for detecting abasic sites in living cells: age-dependent changes in base excision repair. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 686-691
137. Shen G.P., Galick H., Inoue M., and Wallace S.S. Decline of nuclear and mitochondrial oxidative base excision repair activity in late passage human diploid fibroblasts. DNA Repair (Amst) 2 (2003) 673-693
138. Dianov G., Bischoff C., Sunesen M., and Bohr V.A. Repair of 8-oxoguanine in DNA is deficient in Cockayne syndrome group B cells. Nucleic Acids Res. 27 (1999) 1365-1368
139. Sunesen M., Stevnsner T., Brosh Jr. R.M., Dianov G.L., and Bohr V.A. Global genome repair of 8-oxoG in hamster cells requires a functional CSB gene product. Oncogene 21 (2002) 3571-3578
140. Stevnsner T., Nyaga S., Souza-Pinto N.C., van der Horst G.T., Gorgels T.G., Hogue B.A., Thorslund T., and Bohr V.A. Mitochondrial repair of 8-oxoguanine is deficient in Cockayne syndrome group B. Oncogene 21 (2002) 8675-8682
141. Wong H.K., Muftuoglu M., Beck G., Imam S.Z., Bohr V.A., and Wilson III D.M. Cockayne syndrome B protein stimulates apurinic endonuclease 1 activity and protects against agents that introduce base excision repair intermediates. Nucleic Acids Res. 35 (2007) 4103-4113
142. Iida T., Furuta A., Nishioka K., Nakabeppu Y., and Iwaki T. Expression of 8-oxoguanine DNA glycosylase is reduced and associated with neurofibrillary tangles in Alzheimer's disease brain. Acta Neuropathol. (Berl) 103 (2002) 20-25
143. Lovell M.A., Xie C., and Markesbery W.R. Decreased base excision repair and increased helicase activity in Alzheimer's disease brain. Brain Res. 855 (2000) 116-123
144. Mao G., Pan X., Zhu B.B., Zhang Y., Yuan F., Huang J., Lovell M.A., Lee M.P., Markesbery W.R., Li G.M., and Gu L. Identification and characterization of OGG1 mutations in patients with Alzheimer's disease. Nucleic Acids Res. 35 (2007) 2759-2766