Mitochondria, oxidative DNA damage, and aging

R Michael Anson; Vilhelm A Bohr

doi:10.1007/s11357-000-0020-y

. 2000 Oct;23(4):199–218. doi: 10.1007/s11357-000-0020-y

Mitochondria, oxidative DNA damage, and aging

R Michael Anson ¹, Vilhelm A Bohr ¹

PMCID: PMC3455271 PMID: 23604866

Abstract

Protection from reactive oxygen species (ROS) and from mitochondrial oxidative damage is well known to be necessary to longevity. The relevance of mitochondrial DNA (mtDNA) to aging is suggested by the fact that the two most commonly measured forms of mtDNA damage, deletions and the oxidatively induced lesion 8-oxo-dG, increase with age. The rate of increase is species-specific and correlates with maximum lifespan.

It is less clear that failure or inadequacies in the protection from reactive oxygen species (ROS) and from mitochondrial oxidative damage are sufficient to explain senescence. DNA containing 8-oxo-dG is repaired by mitochondria, and the high ratio of mitochondrial to nuclear levels of 8-oxo-dG previously reported are now suspected to be due to methodological difficulties. Furthermore, MnSOD −/+ mice incur higher than wild type levels of oxidative damage, but do not display an aging phenotype. Together, these findings suggest that oxidative damage to mitochondria is lower than previously thought, and that higher levels can be tolerated without physiological consequence.

A great deal of work remains before it will be known whether mitochondrial oxidative damage is a “clock” which controls the rate of aging. The increased level of 8-oxo-dG seen with age in isolated mitochondria needs explanation. It could be that a subset of cells lose the ability to protect or repair mitochondria, resulting in their incurring disproportionate levels of damage. Such an uneven distribution could exceed the reserve capacity of these cells and have serious physiological consequences. Measurements of damage need to focus more on distribution, both within tissues and within cells. In addition, study must be given to the incidence and repair of other DNA lesions, and to the possibility that repair varies from species to species, tissue to tissue, and young to old.

Full Text

The Full Text of this article is available as a PDF (2.0 MB).

Contributor Information

R. Michael Anson, Email: Anson@jhu.edu.

Vilhelm A. Bohr, Email: BohrV@grc.nia.nih.gov

References

1.Harman D. Aging: A theory based on free radical and radiation chemistry. Journal of Gerontology. 1956;11:298–300. doi: 10.1093/geronj/11.3.298. [DOI] [PubMed] [Google Scholar]
2.Szilard L. On the nature of the aging process. Proceedings of the National Academy of Sciences of the United States of America. 1959;45:30–45. doi: 10.1073/pnas.45.1.30. [DOI] [PMC free article] [PubMed] [Google Scholar]
3.Stein G., Weiss J. Chemical effects of ionizing radiations. Nature. 1948;161:650. doi: 10.1038/161650a0. [DOI] [PubMed] [Google Scholar]
4.Commoner B., Townsend J., Pakke G.E. Free radicals in biological materials. Nature. 1954;174:689–691. doi: 10.1038/174689a0. [DOI] [PubMed] [Google Scholar]
5.Grollman A.P., Moriya M. Mutagenesis by 8-oxoguanine: an enemy within. Trends in Genetics. 1993;9:246–249. doi: 10.1016/0168-9525(93)90089-Z. [DOI] [PubMed] [Google Scholar]
6.Purmal A.A., Kow Y.W., Wallace S.S. Major oxidative products of cytosine, 5-hydroxycytosine and 5-hydroxyuracil, exhibit sequence context-dependent mispairing in vitro. Nucleic Acids Research. 1994;22:72–78. doi: 10.1093/nar/22.1.72. [DOI] [PMC free article] [PubMed] [Google Scholar]
7.Collins A.R. Oxidative DNA damage, antioxidants, and cancer. BioEssays. 1999;21(3):238–246. doi: 10.1002/(SICI)1521-1878(199903)21:3<238::AID-BIES8>3.0.CO;2-3. [DOI] [PubMed] [Google Scholar]
8.Stuart G.R., Oda Y., de Boer J.G., Glickman B.W. Mutation frequency and specificity with age in liver, bladder and brain of lacl transgenic mice. Genetics. 2000;154(3):1291–1300. doi: 10.1093/genetics/154.3.1291. [DOI] [PMC free article] [PubMed] [Google Scholar]
9.Jones O.T. The mechanism of the production of superoxide by phagocytes. Mol Chem Neuropathol. 1993;19(1–2):177–184. doi: 10.1007/BF03160177. [DOI] [PubMed] [Google Scholar]
10.Rodeberg D.A., Chaet M.S., Bass R.C., Arkovitz M.S., Garcia V.F. Nitric oxide: an overview. Am J Surg. 1995;170(3):292–303. doi: 10.1016/s0002-9610(05)80017-0. [DOI] [PubMed] [Google Scholar]
11.May J.M., de Haen C. The insulin-like effect of hydrogen peroxide on pathways of lipid synthesis in rat adipocytes. J Biol Chem. 1979;254(18):9017–9021. [PubMed] [Google Scholar]
12.May J.M., de Haen C. Insulin-stimulated intracellular hydrogen peroxide production in rat epididymal fat cells. J Biol Chem. 1979;254(7):2214–2220. [PubMed] [Google Scholar]
13.Krieger-Brauer H.I., Kather H. Human fat cells possess a plasma membrane-bound H202-generating system that is activated by insulin via a mechanism bypassing the receptor kinase. J Clin Invest. 1992;89(3):1006–1013. doi: 10.1172/JCI115641. [DOI] [PMC free article] [PubMed] [Google Scholar]
14.Krieger-Brauer HI, Medda PK, Kather H. Insulin-induced activation of NADPH-dependent H202 generation in human adipocyte plasma membranes is mediated by Galphai2. J Biol Chem. 1997; 272(15):10135–10143. [DOI] [PubMed]
15.Sasaki H., Kodama K., Yamada M. A review of forty-five years study of Hiroshima and Nagasaki atomic bomb survivors. Aging. J Radiat Res (Tokyo) 1991;32(Suppl):310–326. doi: 10.1269/jrr.32.SUPPLEMENT_310. [DOI] [PubMed] [Google Scholar]
16.Beckman K.B., Ames B.N. The free radical theory of aging matures. Physiol Rev. 1998;78(2):547–581. doi: 10.1152/physrev.1998.78.2.547. [DOI] [PubMed] [Google Scholar]
17.Harman D. The biologic clock: the mitochondria? J Am Geriatr Soc. 1972;20(4):145–147. doi: 10.1111/j.1532-5415.1972.tb00787.x. [DOI] [PubMed] [Google Scholar]
18.Miquel J., Economos A.C., Fleming J., Johnson J.E., Jr Mitochondrial role in cell aging. Exp Gerontol. 1980;15(6):575–591. doi: 10.1016/0531-5565(80)90010-8. [DOI] [PubMed] [Google Scholar]
19.Shearman C.W., Kalf G.F. DNA replication by a membrane-DNA complex from rat liver mitochondria. Arch Biochem Biophys. 1977;182(2):573–586. doi: 10.1016/0003-9861(77)90539-2. [DOI] [PubMed] [Google Scholar]
20.Singh G., Sharkey S.M., Moorehead R. Mitochondrial DNA damage by anticancer agents. Pharmacology and Therapeutics. 1992;54:217–230. doi: 10.1016/0163-7258(92)90033-V. [DOI] [PubMed] [Google Scholar]
21.Davis A.F., Clayton D.A. In situ localization of mitochondrial DNA replication in intact mammalian cells. J Cell Biol. 1996;135(4):883–893. doi: 10.1083/jcb.135.4.883. [DOI] [PMC free article] [PubMed] [Google Scholar]
22.Bandy B., Davison A.J. Mitochondrial mutations may increase oxidative stress: implications for carcinogenesis and aging? Free Radical Biology and Medicine. 1990;8:523–539. doi: 10.1016/0891-5849(90)90152-9. [DOI] [PubMed] [Google Scholar]
23.Kasai H., Nishimura S. Hydroxylation of the C-8 position of deoxyguanosine by reducing agents in the presence of oxygen. Nucleic Acids Symp Ser. 1983;12:165–167. [PubMed] [Google Scholar]
24.Kasai H., Nishimura S. Hydroxylation of deoxy guanosine at the C-8 position by polyphenols and aminophenols in the presence of hydrogen peroxide and ferric ion. Gann. 1984;75(7):565–566. [PubMed] [Google Scholar]
25.Kasai H., Nishimura S. Hydroxylation of deoxyguanosine at the C-8 position by ascorbic acid and other reducing agents. Nucleic Acids Res. 1984;12(4):2137–2145. doi: 10.1093/nar/12.4.2137. [DOI] [PMC free article] [PubMed] [Google Scholar]
26.Kasai H., Nishimura S. DNA damage induced by asbestos in the presence of hydrogen peroxide. Gann. 1984;75(10):841–844. [PubMed] [Google Scholar]
27.Kasai H., Tanooka H., Nishimura S. Formation of 8-hydroxyguanine residues in DNA by X-irradiation. Gann. 1984;75(12):1037–1039. [PubMed] [Google Scholar]
28.Floyd R.A., Watson J.J., Wong P.K., Altmiller D.H., Rickard R.C. Hydroxyl free radical adduct of deoxyguanosine: sensitive detection and mechanisms of formation. Free Radical Research Communications. 1986;1(3):163–172. doi: 10.3109/10715768609083148. [DOI] [PubMed] [Google Scholar]
29.Kouchakdjian M., Bodepudi V., Shibutani S., et al. NMR structural studies of the ionizing radiation adduct 7-hydro-8-oxodeoxyguanosine (8-oxo-7H-dG) opposite deoxyadenosine in a DNA duplex. 8-Oxo-7H-dG(syn).dA(anti) alignment at lesion site. Biochemistry. 1991;30:1403–1412. doi: 10.1021/bi00219a034. [DOI] [PubMed] [Google Scholar]
30.McAuley-Hecht KE, Leonard GA, Gibson NJ, et al. Crystal structure of a DNA duplex containing 8-hydroxydeoxyguanine-adenine base pairs. Biochemistry. 1994;33(34):10266–10270. [DOI] [PubMed]
31.Shibutani S., Takeshita M., Grollman A.P. Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature. 1991;349:431–434. doi: 10.1038/349431a0. [DOI] [PubMed] [Google Scholar]
32.Pinz K.G., Shibutani S., Bogenhagen D.F. Action of mitochondrial DNA polymerase gamma at sites of base loss or oxidative damage. Journal of Biological Chemistry. 1995;270(16):9202–9206. doi: 10.1074/jbc.270.16.9202. [DOI] [PubMed] [Google Scholar]
33.Moraes E.C., Keyse S.M., Tyrrell R.M. Mutagenesis by hydrogen peroxide treatment of mammalian cells: a molecular analysis. Carcinogenesis. 1990;11:283–293. doi: 10.1093/carcin/11.2.283. [DOI] [PubMed] [Google Scholar]
34.Tkeshelashvili L.K., McBride T., Spence K., Loeb L.A. Mutation spectrum of copper-induced DNA damage. J Biol Chem. 1991;266(10):6401–6406. [PubMed] [Google Scholar]
35.Michaels M.L., Pham L., Cruz C., Miller J.H. MutM, a protein that prevents G.C—T.A transversions, is formamidopyrimidine-DNA glycosylase. Nucleic Acids Research. 1991;19:3629–3632. doi: 10.1093/nar/19.13.3629. [DOI] [PMC free article] [PubMed] [Google Scholar]
36.Radicella J.P., Dherin C., Desmaze C., Fox M.S., Boiteux S. Cloning and characterization of hOGG1, a human homolog of the OGG1 gene of Saccharomyces cerevisiae. Proc Natl Acad Sci USA. 1997;94(15):8010–8015. doi: 10.1073/pnas.94.15.8010. [DOI] [PMC free article] [PubMed] [Google Scholar]
37.Suter M., Richter C. Fragmented mitochondrial DNA is the predominant carrier of oxidized DNA bases. Biochemistry. 1999;38(1):459–464. doi: 10.1021/bi9811922. [DOI] [PubMed] [Google Scholar]
38.Helbock H.J., Beckman K.B., Shigenaga M.K., et al. DNA oxidation matters: the HPLC-electrochemical detection assay of 8-oxo-deoxyguanosine and 8-oxo-guanine. Proc Natl Acad Sci USA. 1998;95(1):288–293. doi: 10.1073/pnas.95.1.288. [DOI] [PMC free article] [PubMed] [Google Scholar]
39.Hayakawa M., Ogawa T., Sugiyama S., Tanaka M., Ozawa T. Massive conversion of guanosine to 8-hydroxy-guanosine in mouse liver mitochondrial DNA by administration of azidothymidine. Biochemical and Biophysical Research Communications. 1991;176:87–93. doi: 10.1016/0006-291X(91)90893-C. [DOI] [PubMed] [Google Scholar]
40.Dizdaroglu M. Chemical determination of oxidative DNA damage by gas chromatography-mass spectrometry. Methods Enzymol. 1994;234:3–16. doi: 10.1016/0076-6879(94)34072-2. [DOI] [PubMed] [Google Scholar]
41.Wassermann K, Kohn KW, Bohr VA. Heterogeneity of nitrogen mustard-induced DNA damage and repair at the level of the gene in Chinese hamster ovary cells. Journal of Biological Chemistry. 1990;265:13906–13913. [PubMed]
42.Epe B., Hegler J., Wild D. Singlet oxygen as an ultimately reactive species in Salmonella typhimurium DNA damage induced by methylene blue/visible light. Carcinogenesis. 1989;10:2019–2024. doi: 10.1093/carcin/10.11.2019. [DOI] [PubMed] [Google Scholar]
43.Hegler J., Bittner D., Boiteux S., Epe B. Quantification of oxidative DNA modifications in mitochondria. Carcinogenesis. 1993;14:2309–2312. doi: 10.1093/carcin/14.11.2309. [DOI] [PubMed] [Google Scholar]
44.Bohr V.A., Smith C.A., Okumoto D.S., Hanawalt P.C. DNA repair in an active gene: removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell. 1985;40(2):359–369. doi: 10.1016/0092-8674(85)90150-3. [DOI] [PubMed] [Google Scholar]
45.Bohr V.A., Okumoto D.S. Analysis of pyrimidine dimers in defined genes. In: Friedberg E.C., Hanawalt P.C., editors. DNA Repair: A laboratory manual of research procedures, VoL III. 0 ed. New York and Basel: Marcel Dekker, Inc.; 1988. pp. 347–366. [Google Scholar]
46.Kalinowski D.P., Illenye S., Van Houten B. Analysis of DNA damage and repair in murine leukemia L1210 cells using a quantitative polymerase chain reaction assay. Nucleic Acids Research. 1992;20(13):3485–3494. doi: 10.1093/nar/20.13.3485. [DOI] [PMC free article] [PubMed] [Google Scholar]
47.Yakes F.M., Van Houten B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci USA. 1997;94(2):514–519. doi: 10.1073/pnas.94.2.514. [DOI] [PMC free article] [PubMed] [Google Scholar]
48.Drouin R., Rodriguez H., Holmquist G.P., Akman S.A. In vivo Cu-H202-and H202-induced DNA damage maps show the same oxidative damage frequency for each nucleotide position. Proceedings of the National Academy of Sciences of the United States of America. 1995;36:550. [Google Scholar]
49.Rodriguez H, Drouin R, Holmquist GP, et al. Mapping of copper hydrogen peroxide-induced DNA damage at nucleotide resolution in human genomic DNA by ligation-mediated polymerase chain reaction. Journal of Biological Chemistry. 1995;270:17633–17640. [DOI] [PubMed]
50.Driggers W.J., Holmquist G.P., LeDoux S.P., Wilson G.L. Mapping frequencies of endogenous oxidative damage and the kinetic response to oxidative stress in a region of rat mtDNA. Nucleic Acids Res. 1997;25(21):4362–4369. doi: 10.1093/nar/25.21.4362. [DOI] [PMC free article] [PubMed] [Google Scholar]
51.Mueller P.R., Wold B. In vivo footprinting of a muscle specific enhancer by Ligation Mediated PCR. Science. 1989;246:780–786. doi: 10.1126/science.2814500. [DOI] [PubMed] [Google Scholar]
52.Pfeifer G.P., Drouin R., Riggs A.D., Holmquist G.P. Binding of transcription factors creates hot spots for UV photoproducts in vivo. Mol Cell Biol. 1992;12:1798–1804. doi: 10.1128/mcb.12.4.1798. [DOI] [PMC free article] [PubMed] [Google Scholar]
53.Soultanakis R.P., Melamede R.J., Bespalov I.A., et al. Fluorescence detection of 8-oxoguanine in nuclear and mitochondrial DNA of cultured cells using a recombinant fab and confocal scanning laser microscopy. Free Radic Biol Med. 2000;28(6):987–998. doi: 10.1016/S0891-5849(00)00185-4. [DOI] [PubMed] [Google Scholar]
54.Beckman KB, Ames BN. Oxidative decay of DNA. J Biol Chem. 1997;272(32):19633–19636. [DOI] [PubMed]
55.Collins A., Cadet J., Epe B., Gedik C. Problems in the measurement of 8-oxoguanine in human DNA. Carcinogenesis. 1997;18(9):1833–1836. doi: 10.1093/carcin/18.9.1833. [DOI] [PubMed] [Google Scholar]
56.ESCODD. Comparison of different methods of measuring 8-oxoguanine as a marker of oxidative DNA damage. ESCODD (European Standards Committee on Oxidative DNA Damage) Free Radic Res. 2000;32(4):333–341. doi: 10.1080/10715760000300331. [DOI] [PubMed] [Google Scholar]
57.Hudson E.K., Hogue B.A., Souza-Pinto N.C., et al. Age-associated change in mitochondrial DNA damage. Free Radical Research. 1998;29(6):573–579. doi: 10.1080/10715769800300611. [DOI] [PubMed] [Google Scholar]
58.Anson R.M., Hudson E., Bohr V.A. Mitochondrial endogenous oxidative damage has been overestimated. Faseb J. 2000;14(2):355–360. doi: 10.1096/fasebj.14.2.355. [DOI] [PubMed] [Google Scholar]
59.Richter C., Park J.W., Ames B.N. Normal oxidative damage to mitochondrial and nuclear DNA is extensive. Proceedings of the National Academy of Sciences of the United States of America. 1988;85(17):6465–6467. doi: 10.1073/pnas.85.17.6465. [DOI] [PMC free article] [PubMed] [Google Scholar]
60.Higuchi Y., Linn 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. Journal of Biological Chemistry. 1995;270(14):7950–7956. doi: 10.1074/jbc.270.14.7950. [DOI] [PubMed] [Google Scholar]
61.Takasawa M., Hayakawa M., Sugiyama S., Hattori K., Ito T., Ozawa T. Age-associated damage in mitochondrial function in rat hearts. Exp Gerontol. 1993;28(3):269–280. doi: 10.1016/0531-5565(93)90034-B. [DOI] [PubMed] [Google Scholar]
62.Beckman K.B., Ames B.N. Detection and quantification of oxidative adducts of mitochondrial DNA. Methods in Enzymology. 1996;264:442–453. doi: 10.1016/s0076-6879(96)64040-3. [DOI] [PubMed] [Google Scholar]
63.Beckman K.B., Ames B.N. Endogenous oxidative damage of mtDNA. Mutat Res. 1999;424(1–2):51–58. doi: 10.1016/s0027-5107(99)00007-x. [DOI] [PubMed] [Google Scholar]
64.Hayakawa M., Sugiyama S., Hattori K., Takasawa M., Ozawa T. Age-associated damage in mitochondrial DNA in human hearts. Mol Cell Biochem. 1993;119:95–103. doi: 10.1007/BF00926859. [DOI] [PubMed] [Google Scholar]
65.Zastawny T.H., Dabrowska M., Jaskolski T., et al. Comparison of oxidative base damage in mitochondria and nuclear DNA. Free Radic Biol Med. 1998;24(5):722–725. doi: 10.1016/S0891-5849(97)00331-6. [DOI] [PubMed] [Google Scholar]
66.Anson R.M., Senturker S., Dizdaroglu M., Bohr V.A. Measurement of oxidatively induced base lesions in liver from Wistar rats of different ages. Free Radic Biol Med. 1999;27(3–4):456–462. doi: 10.1016/S0891-5849(99)00091-X. [DOI] [PubMed] [Google Scholar]
67.Chung M.H., Kasai H., Nishimura S., Yu B.P. Protection of DNA damage by dietary restriction. Free Radical Biology and Medicine. 1992;12(6):523–525. doi: 10.1016/0891-5849(92)90105-P. [DOI] [PubMed] [Google Scholar]
68.Sohal R.S., Agarwal S., Candas M., Forster M.J., Lal H. Effect of age and caloric restriction on DNA oxidative damage in different tissues of C57BL/6 mice. Mechanisms of Ageing and Development. 1994;76:215–224. doi: 10.1016/0047-6374(94)91595-4. [DOI] [PubMed] [Google Scholar]
69.Lass A., Sohal B.H., Weindruch R., Forster M.J., Sohal R.S. Caloric restriction prevents age-associated accrual of oxidative damage to mouse skeletal muscle mitochondria. Free Radic Biol Med. 1998;25(9):1089–1097. doi: 10.1016/S0891-5849(98)00144-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
70.Masoro E.J. Dietary restriction. Exp Gerontol. 1995;30(3–4):291–298. doi: 10.1016/0531-5565(94)00028-2. [DOI] [PubMed] [Google Scholar]
71.Cortopassi G.A., Arnheim N. Detection of a specific mitochondrial DNA deletion in tissues of older humans. Nucleic Acids Res. 1990;18(23):6927–6933. doi: 10.1093/nar/18.23.6927. [DOI] [PMC free article] [PubMed] [Google Scholar]
72.Linnane A.W., Baumer A., Maxwell R.J., Preston H., Zhang C.F., Marzuki S. Mitochondrial gene mutation: the ageing process and degenerative diseases. Biochemistry International. 1990;22:1067–1076. [PubMed] [Google Scholar]
73.Cortopassi G.A., Shibata D., Soong N.W., Arnheim N. A pattern of accumulation of a somatic deletion of mitochondrial DNA in aging human tissues. Proceedings of the National Academy of Science USA. 1992;89:7370–7374. doi: 10.1073/pnas.89.16.7370. [DOI] [PMC free article] [PubMed] [Google Scholar]
74.Simonetti S., Chen X., DiMauro S., Schon E.A. Accumulation of deletions in human mitochondrial DNA during normal aging: analysis by quantitative PCR. Biochim Biophys Acta. 1992;1180(2):113–122. doi: 10.1016/0925-4439(92)90059-v. [DOI] [PubMed] [Google Scholar]
75.Lee H.C., Pang C.Y., Hsu H.S., Wei Y.H. Differential accumulations of 4,977 bp deletion in mitochondrial DNA of various tissues in human ageing. Biochim Biophys Acta. 1994;1226(1):37–43. doi: 10.1016/0925-4439(94)90056-6. [DOI] [PubMed] [Google Scholar]
76.Filser N., Margue C., Richter C. Quantification of wild-type mitochondrial DNA and its 4.8-kb deletion in rat organs. Biochem Biophys Res Commun. 1997;233(1):102–107. doi: 10.1006/bbrc.1997.6409. [DOI] [PubMed] [Google Scholar]
77.Liu V.W., Zhang C., Pang C.Y., et al. Independent occurrence of somatic mutations in mitochondrial DNA of human skin from subjects of various ages. Hum Mutat. 1998;11(3):191–196. doi: 10.1002/(SICI)1098-1004(1998)11:3<191::AID-HUMU2>3.0.CO;2-L. [DOI] [PubMed] [Google Scholar]
78.Soong N.W., Hinton D.R., Cortopassi G., Arnheim N. Mosaicism for a specific somatic mitochondrial DNA mutation in adult human brain. Nat Genet. 1992;2(4):318–323. doi: 10.1038/ng1292-318. [DOI] [PubMed] [Google Scholar]
79.Corral-Debdnski M., Horton T., Lott M.T., Shoffner J.M., Beal M.F., Wallace D.C. Mitochondrial DNA deletions in human brain: regional variability and increase with advanced age. Nat Genet. 1992;2:324–329. doi: 10.1038/ng1292-324. [DOI] [PubMed] [Google Scholar]
80.Filburn C.R., Edris W., Tamatani M., Hogue B., Kudryashova I., Hansford R.G. Mitochondrial electron transport chain activities and DNA deletions in regions of the rat brain. Mech Ageing Dev. 1996;87(1):35–46. doi: 10.1016/0047-6374(96)01696-X. [DOI] [PubMed] [Google Scholar]
81.Luo Y, Roth GS. The roles of dopamine oxidative stress and dopamine receptor signaling in aging and age-related neurodegeneration. Antioxidants and Redox Signaling. 2000;In Press. [DOI] [PubMed]
82.de Grey A.D. A proposed refinement of the mitochondrial free radical theory of aging. Bioessays. 1997;19(2):161–166. doi: 10.1002/bies.950190211. [DOI] [PubMed] [Google Scholar]
83.Gershon D. The mitochondrial theory of aging: is the culprit a faulty disposal system rather than indigenous mitochondrial alterations? Exp Gerontol. 1999;34(5):613–619. doi: 10.1016/S0531-5565(99)00010-8. [DOI] [PubMed] [Google Scholar]
84.Kowald A. The mitochondrial theory of aging: do damaged mitochondria accumulate by delayed degradation? Exp Gerontol. 1999;34(5):605–612. doi: 10.1016/S0531-5565(99)00011-X. [DOI] [PubMed] [Google Scholar]
85.Wang E., Wong A., Cortopassi G. The rate of mitochondrial mutagenesis is faster in mice than humans. Mutat Res. 1997;377(2):157–166. doi: 10.1016/s0027-5107(97)00091-2. [DOI] [PubMed] [Google Scholar]
86.Hattori K., Tanaka M., Sugiyama S., et al. Age-dependent increase in deleted mitochondrial DNA in the human heart: possible contributory factor to presbycardia. American Heart Journal. 1991;121:1735–1742. doi: 10.1016/0002-8703(91)90020-I. [DOI] [PubMed] [Google Scholar]
87.Katayama M., Tanaka M., Yamamoto H., Ohbayashi T., Nimura Y., Ozawa T. Deleted mitochondrial DNA in the skeletal muscle of aged individuals. Biochem Int. 1991;25(1):47–56. [PubMed] [Google Scholar]
88.Zhang C., Baumer A., Maxwell R.J., Linnane A.W., Nagley P. Multiple mitochondrial DNA deletions in an eldedy human individual. FEBS Lett. 1992;297(1–2):34–38. doi: 10.1016/0014-5793(92)80321-7. [DOI] [PubMed] [Google Scholar]
89.Lee C.M., Chung S.S., Kaczkowski J.M., Weindruch R., Aiken J.M. Multiple mitochondrial DNA deletions associated with age in skeletal muscle of rhesus monkeys. Journal of Gerontology. 1993;48:B201–B205. doi: 10.1093/geronj/48.6.b201. [DOI] [PubMed] [Google Scholar]
90.Melov S., Shoffner J.M., Kaufman A., Wallace D.C. Marked increase in the number and variety of mitochondrial DNA rearrangements in aging human skeletal muscle. Nucleic Acids Res. 1995;23(20):4122–4126. doi: 10.1093/nar/23.20.4122. [DOI] [PMC free article] [PubMed] [Google Scholar]
91.Reynier P., Malthiery Y. Accumulation of deletions in MtDNA during tissue aging: analysis by long PCR. Biochem Biophys Res Commun. 1995;217(1):59–67. doi: 10.1006/bbrc.1995.2745. [DOI] [PubMed] [Google Scholar]
92.Eimon P.M., Chung S.S., Lee C.M., Weindruch R., Aiken J.M. Age-associated mitochondrial DNA deletions in mouse skeletal muscle: comparison of different regions of the mitochondrial genome. Dev Genet. 1996;18(2):107–113. doi: 10.1002/(SICI)1520-6408(1996)18:2<107::AID-DVG3>3.0.CO;2-D. [DOI] [PubMed] [Google Scholar]
93.Tengan C.H., Moraes C.T. Detection and analysis of mitochondrial DNA deletions by whole genome PCR. Biochem Mol Med. 1996;58(1):130–134. doi: 10.1006/bmme.1996.0040. [DOI] [PubMed] [Google Scholar]
94.Zhang C., Liu V.W., Addessi C.L., Sheffield D.A., Linnane A.W., Nagley P. Differential occurrence of mutations in mitochondrial DNA of human skeletal muscle during aging. Hum Mutat. 1998;11(5):360–371. doi: 10.1002/(SICI)1098-1004(1998)11:5<360::AID-HUMU3>3.0.CO;2-U. [DOI] [PubMed] [Google Scholar]
95.Lee H.C., Pang C.Y., Hsu H.S., Wei Y.H. Ageing-associated tandem duplications in the D-loop of mitochondrial DNA of human muscle. FEBS Lett. 1994;354(1):79–83. doi: 10.1016/0014-5793(94)01063-3. [DOI] [PubMed] [Google Scholar]
96.Wei Y.H., Pang C.Y., You B.J., Lee H.C. Tandem duplications and large-scale deletions of mitochondrial DNA are early molecular events of human aging process. Ann N Y Acad Sci. 1996;786:82–101. doi: 10.1111/j.1749-6632.1996.tb39054.x. [DOI] [PubMed] [Google Scholar]
97.Schwarze S.R., Lee C.M., Chung S.S., Roecker E.B., Weindruch R., Aiken J.M. High levels of mitochondrial DNA deletions in skeletal muscle of old rhesus monkeys. Mech Ageing Dev. 1995;83(2):91–101. doi: 10.1016/0047-6374(95)01611-3. [DOI] [PubMed] [Google Scholar]
98.Muller-Hocker J., Seibel P., Schneiderbanger K., Kadenbach B. Different in situ hybridization patterns of mitochondrial DNA in cytochrome c oxidase-deficient extraocular muscle fibres in the elderly. Virchows Arch A Pathol Anat Histopathol. 1993;422(1):7–15. doi: 10.1007/BF01605127. [DOI] [PubMed] [Google Scholar]
99.Moslemi A.R., Melberg A., Holme E., Oldfors A. Clonal expansion of mitochondrial DNA with multiple deletions in autosomal dominant progressive external ophthalmoplegia. Ann Neurol. 1996;40(5):707–713. doi: 10.1002/ana.410400506. [DOI] [PubMed] [Google Scholar]
100.Muller-Hocker J., Jacob U., Seibel P. Hashimoto thyroiditis is associated with defects of cytochrome-c oxidase in oxyphil Askanazy cells and with the common deletion (4,977) of mitochondrial DNA. Ultrastruct Pathol. 1998;22(1):91–100. doi: 10.3109/01913129809032263. [DOI] [PubMed] [Google Scholar]
101.Prelle A., Fagiolari G., Checcarelli N., et al. Mitochondrial myopathy: correlation between oxidative defect and mitochondrial DNA deletions at single fiber level. Acta Neuropathol (Berl) 1994;87(4):371–376. doi: 10.1007/BF00313606. [DOI] [PubMed] [Google Scholar]
102.Lee C.M., Lopez M.E., Weindruch R., Aiken J.M. Association of age-related mitochondrial abnormalities with skeletal muscle fiber atrophy. Free Radic Biol Med. 1998;25(8):964–972. doi: 10.1016/S0891-5849(98)00185-3. [DOI] [PubMed] [Google Scholar]
103.Hayakawa M., Torii K., Sugiyama S., Tanaka M., Ozawa T. Age-associated accumulation of 8-hydroxydeoxyguanosine in mitochondrial DNA of human diaphragm. Biochem Biophys Res Commun. 1991;179(2):1023–1029. doi: 10.1016/0006-291X(91)91921-X. [DOI] [PubMed] [Google Scholar]
104.Hayakawa M., Hattori K., Sugiyama S., Ozawa T. Age-associated oxygen damage and mutations in mitochondrial DNA in human hearts. Biochemical and Biophysical Research Communications. 1992;189:979–985. doi: 10.1016/0006-291X(92)92300-M. [DOI] [PubMed] [Google Scholar]
105.Yen T.C., King K.L., Lee H.C., Yeh S.H., Wei Y.H. Age-dependent increase of mitochondrial DNA deletions together with lipid peroxides and superoxide dismutase in human liver mitochondria. Free Radic Biol Med. 1994;16(2):207–214. doi: 10.1016/0891-5849(94)90145-7. [DOI] [PubMed] [Google Scholar]
106.Wei Y.H., Kao S.H., Lee H.C. Simultaneous increase of mitochondrial DNA deletions and lipid peroxidation in human aging. Ann N Y Acad Sci. 1996;786:24–43. doi: 10.1111/j.1749-6632.1996.tb39049.x. [DOI] [PubMed] [Google Scholar]
107.Lezza A.M., Mecocci P., Cormio A., et al. Mitochondrial DNA 4977 bp deletion and OH8dG levels correlate in the brain of aged subjects but not Alzheimer’s disease patients. Faseb J. 1999;13(9):1083–1088. doi: 10.1096/fasebj.13.9.1083. [DOI] [PubMed] [Google Scholar]
108.Muscari C., Giaccari A., Stefanelli C., et al. Presence of a DNA-4236 bp deletion and 8-hydroxy-deoxyguanosine in mouse cardiac mitochondrial DNA during aging. Aging (Milano) 1996;8(6):429–433. doi: 10.1007/BF03339606. [DOI] [PubMed] [Google Scholar]
109.Aruoma O.I., Halliwell B., Gajewski E., Dizdaroglu M. Copper-ion-dependent damage to the bases in DNA in the presence of hydrogen peroxide. Biochemical Journal. 1991;273:601–604. doi: 10.1042/bj2730601. [DOI] [PMC free article] [PubMed] [Google Scholar]
110.Yamamoto F., Kasai H., Togashi Y., Takeichi N., Hori T., Nishimura S. Elevated level of 8-hydroxydeoxyguanosine in DNA of liver, kidneys, and brain of Long-Evans Cinnamon rats. Japanese Joumal of Cancer Research. 1993;84(5):508–511. doi: 10.1111/j.1349-7006.1993.tb00168.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
111.Mansouri A., Gaou I., Fromenty B., et al. Premature oxidative aging of hepatic mitochondrial DNA in Wilson’s disease. Gastroenterology. 1997;113(2):599–605. doi: 10.1053/gast.1997.v113.pm9247482. [DOI] [PubMed] [Google Scholar]
112.Kubota N., Hayashi J., Inada T., Iwamura Y. Induction of a particular deletion in mitochondrial DNA by X rays depends on the inherent radiosensitivity of the cells. Radiat Res. 1997;148(4):395–398. [PubMed] [Google Scholar]
113.Lezza A.M., Boffoli D., Scacco S., Cantatore P., Gadaleta M.N. Correlation between mitochondrial DNA 4977-bp deletion and respiratory chain enzyme activities in aging human skeletal muscles. Biochem Biophys Res Commun. 1994;205(1):772–779. doi: 10.1006/bbrc.1994.2732. [DOI] [PubMed] [Google Scholar]
114.Tengan C.H., Gabbai A.A., Shanske S., Zeviani M., Moraes C.T. Oxidative phosphorylation dysfunction does not increase the rate of accumulation of age-related mtDNA deletions in skeletal muscle. Mutat Res. 1997;379(1):1–11. doi: 10.1016/s0027-5107(97)00076-6. [DOI] [PubMed] [Google Scholar]
115.Pacifici R.E., Davies K.J. Protein, lipid and DNA repair systems in oxidative stress: the free-radical theory of aging revisited. Gerontology. 1991;37:166–180. doi: 10.1159/000213257. [DOI] [PubMed] [Google Scholar]
116.McCord J.M., Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein) J Biol Chem. 1969;244(22):6049–6055. [PubMed] [Google Scholar]
117.Reaume A.G., Elliott J.L., Hoffman E.K., et al. Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. NatGenet. 1996;13(1):43–47. doi: 10.1038/ng0596-43. [DOI] [PubMed] [Google Scholar]
118.Kondo T., Reaume A.G., Huang T.T., et al. Reduction of CuZn-superoxide dismutase activity exacerbates neuronal cell injury and edema formation after transient focal cerebral ischemia. J Neurosci. 1997;17(11):4180–4189. doi: 10.1523/JNEUROSCI.17-11-04180.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
119.Li Y., Huang T.T., Carlson E.J., et al. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet. 1995;11(4):376–381. doi: 10.1038/ng1295-376. [DOI] [PubMed] [Google Scholar]
120.Melov S., Schneider J.A., Day B.J., et al. A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase. Nat Genet. 1998;18(2):159–163. doi: 10.1038/ng0298-159. [DOI] [PubMed] [Google Scholar]
121.Ishii N., Fujii M., Hartman P.S., et al. A mutation in succinate dehydrogenase cytochrome b causes oxidative stress and ageing in nematodes. Nature. 1998;394(6694):694–697. doi: 10.1038/29331. [DOI] [PubMed] [Google Scholar]
122.Guidot D.M., Repine J.E., Kitlowski A.D., et al. Mitochondrial respiration scavenges extramitochondrial superoxide anion via a nonenzymatic mechanism. J Clin Invest. 1995;96(2):1131–1136. doi: 10.1172/JCI118100. [DOI] [PMC free article] [PubMed] [Google Scholar]
123.Clayton D.A., Doda J.N., Friedberg E.C. The absence of a pyrimidine dimer repair mechanismin mammalian mitochondria. Proceedings of the National Academy of Sciences of the United States of America. 1974;71(7):2777–2781. doi: 10.1073/pnas.71.7.2777. [DOI] [PMC free article] [PubMed] [Google Scholar]
124.Ryoji M., Katayama H., Fusamae H., Matsuda A., Sakai F., Utano H. Repair of DNA damage in a mitochondrial lysate of Xenopus laevis oocytes. Nucleic Acids Research. 1996;24(20):4057–4062. doi: 10.1093/nar/24.20.4057. [DOI] [PMC free article] [PubMed] [Google Scholar]
125.Lansman R.A., Clayton D.A. Selective nicking of mammalian mitochondrial DNA in vivo: photosensitization by incorporation of 5-bromodeoxyuridine. Journal of Molecular Biology. 1975;99:761–776. doi: 10.1016/s0022-2836(75)80183-5. [DOI] [PubMed] [Google Scholar]
126.Pascucci B., Versteegh A., van Hoffen A., van Zeeland A.A., Mullenders L.H., Dogliotti E. DNA repair of UV photoproducts and mutagenesis in human mitochondrial DNA. J Mol Biol. 1997;273(2):417–427. doi: 10.1006/jmbi.1997.1268. [DOI] [PubMed] [Google Scholar]
127.LeDoux S.P., Wilson G.L., Beecham E.J., Stevnsner T., Wassermann K., Bohr V.A. Repair of mitochondrial DNA after various types of DNA damage in Chinese hamster ovary cells. Carcinogenesis. 1992;13:1967–1973. doi: 10.1093/carcin/13.11.1967. [DOI] [PubMed] [Google Scholar]
128.Bohr V.A. Gene specific DNA repair. Carcinogenesis. 1991;12:1983–1992. doi: 10.1093/carcin/12.11.1983. [DOI] [PubMed] [Google Scholar]
129.Mellon I., Spivak G., Hanawalt P.C. Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell. 1987;51(2):241–249. doi: 10.1016/0092-8674(87)90151-6. [DOI] [PubMed] [Google Scholar]
130.Pfeifer G.P., Drouin R., Holmquist G.P. Detection of DNA adducts at the DNA sequence level by ligation-mediated PCR. Mutation Research. 1993;288:39–46. doi: 10.1016/0027-5107(93)90206-u. [DOI] [PubMed] [Google Scholar]
131.Hanawalt P.C., Gee P., Ho L., Hsu R.K., Kane C.J. Genomic heterogeneity of DNA repair. Role in aging? Annals of the New York Academy of Sciences. 1992;663:17–25. doi: 10.1111/j.1749-6632.1992.tb38644.x. [DOI] [PubMed] [Google Scholar]
132.Holmes G.E., Bernstein C., Bernstein H. Oxidative and other DNA damages as the basis of aging: a review. Mutation Research. 1992;275:305–315. doi: 10.1016/0921-8734(92)90034-M. [DOI] [PubMed] [Google Scholar]
133.Bohr V.A., Anson R.M. DNA damage, mutation and fine structure DNA repair in aging. Mutation Research. 1995;338(1–6):25–34. doi: 10.1016/0921-8734(95)00008-t. [DOI] [PubMed] [Google Scholar]
134.Myers K.A., Saffhill R., O’Connor P.J. Repair of alkylated purines in the hepatic DNA of mitochondria and nuclei in the rat. Carcinogenesis. 1988;9(2):285–292. doi: 10.1093/carcin/9.2.285. [DOI] [PubMed] [Google Scholar]
135.Satoh M.S., Huh N., Rajewsky M.F., Kuroki T. Enzymatic removal of O6-ethylguanine from mitochondrial DNA in rat tissues exposed to N-ethyl-N-nitrosourea in vivo. Journal of Biological Chemistry. 1988;263(14):6854–6856. [PubMed] [Google Scholar]
136.Pettepher C.C., LeDoux S.P., Bohr V.A., Wilson G.L. Repair of alkali-labile sites within the mitochondrial DNA of RINr 38 cells after exposure to the nitrosourea streptozotocin. Journal of Biological Chemistry. 1991;266:3113–3117. [PubMed] [Google Scholar]
137.Pirsel M., Bohr V.A. Methyl methanesulfonate adduct formation and repair in the DHFR gene and in mitochondrial DNA in hamster cells. Carcinogenesis. 1993;14:2105–2108. doi: 10.1093/carcin/14.10.2105. [DOI] [PubMed] [Google Scholar]
138.Cullinane C., Bohr V.A. DNA interstrand cross-links induced by psoralen are not repaired in mammalian mitochondria. Cancer Res. 1998;58(7):1400–1404. [PubMed] [Google Scholar]
139.Snyderwine E.G., Bohr V.A. Gene-and strand-specific damage and repair in Chinese hamster ovary cells treated with 4-nitroquinoline 1-oxide. Cancer Research. 1992;52:4183–4189. [PubMed] [Google Scholar]
140.Thyagarajan B, Padua RA, Campbell C. Mammalian mitochondria possess homologous DNA recombination activity. Journal of Biological Chemistry. 1996;271(44):27536–27543. [DOI] [PubMed]
141.Richter C. Reactive oxygen and DNA damage in mitochondria. Mutation Research. 1992;275:249–255. doi: 10.1016/0921-8734(92)90029-O. [DOI] [PubMed] [Google Scholar]
142.Driggers WJ, LeDoux SP, Wilson GL. Repair of oxidative damage within the mitochondrial DNA of RINr 38 cells. Journal of Biological Chemistry. 1993;268:22042–22045. [PubMed]
143.Chung M.H., Kiyosawa H., Ohtsuka E., Nishimura S., Kasai H. DNA strand cleavage at 8-hydroxyguanine residues by hot piperidine treatment. Biochemical and Biophysical Research Communications. 1992;188:1–7. doi: 10.1016/0006-291X(92)92341-T. [DOI] [PubMed] [Google Scholar]
144.Driggers W.J., Grishko V.I., LeDoux S.P., Wilson G.L. Defective repair of oxidative damage in the mitochondrial DNA of a xeroderma pigmentosum group A cell line. Cancer Research. 1996;56(6):1262–1266. [PubMed] [Google Scholar]
145.Shen C.C., Wertelecki W., Driggers W.J., LeDoux S.P., Wilson G.L. Repair of mitochondrial DNA damage induced by bleomycin in human cells. Mutation Research. 1995;337(1):19–23. doi: 10.1016/0921-8777(95)00008-8. [DOI] [PubMed] [Google Scholar]
146.Anson R.M., Croteau D.L., Stierum R.H., Filburn F., Parsell R., Bohr V.A. Homogenous repair of singlet oxygen-induced DNA damage in differentially transcribed regions and strands of human mitochondrial DNA. Nucleic Acids Research. 1998;26(2):662–668. doi: 10.1093/nar/26.2.662. [DOI] [PMC free article] [PubMed] [Google Scholar]
147.Taffe B.G., Larminat F., Laval J., Croteau D.L., Anson R.M., Bohr V.A. Gene-specific nuclear and mitochondrial repair of formamidopyrimidine DNA glycosylase-sensitive sites in Chinese hamster ovary cells. Mutation Research. 1996;364(3):183–192. doi: 10.1016/s0921-8777(96)00031-6. [DOI] [PubMed] [Google Scholar]
148.Epe B., Pflaum M., Boiteux S. DNA damage induced by photosensitizers in cellular and cell-free systems. Mutation Research. 1993;299:135–145. doi: 10.1016/0165-1218(93)90091-Q. [DOI] [PubMed] [Google Scholar]
149.Epe B., Pflaum M., Haring M., Hegler J., Rudiger H. Use of repair endonucleases to characterize DNA damage induced by reactive oxygen species in cellular and cell-free systems. Toxicol Lett. 1993;67:57–72. doi: 10.1016/0378-4274(93)90046-Z. [DOI] [PubMed] [Google Scholar]
150.Horai S., Hayasaka K. Intraspecific nucleotide sequence differences in the major noncoding region of human mitochondrial DNA. American Journal of Human Genetics. 1990;46:828–842. [PMC free article] [PubMed] [Google Scholar]
151.Crawford D.R., Wang Y., Schools G.P., Kochheiser J., Davies K.J. Down-regulation of mammalian mitochondrial RNAs during oxidative stress. Free Radic Biol Med. 1997;22(3):551–559. doi: 10.1016/S0891-5849(96)00380-2. [DOI] [PubMed] [Google Scholar]
152.Abramova N.E., Davies K.J.A., Crawford D.R. Polynucleotide degradation during early stage response to oxidative stress is specific to mitochondria. Free Radical Biology and Medicine. 2000;28(2):281–288. doi: 10.1016/S0891-5849(99)00239-7. [DOI] [PubMed] [Google Scholar]
153.Tang J.T., Yamazaki H., Inoue T., et al. Mitochondrial DNA influences radiation sensitivity and induction of apoptosis in human fibroblasts. Anticancer Research. 1999;19(6B):4959–4964. [PubMed] [Google Scholar]
154.Fung H., Kow Y.W., Van Houten B., et al. Asbestos increases mammalian AP-endonuclease gene expression, protein levels, and enzyme activity in mesothelial cells. Cancer Res. 1998;58(2):189–194. [PubMed] [Google Scholar]
155.Souza-Pinto N.C., Croteau D.L., Hudson E.K., Hansford R.G., Bohr V.A. Age-associated increase in 8-oxo-deoxyguanosine glycosylase/AP lyase activity in rat mitochondria. Nucleic Acids Research. 1999;27(8):1935–1942. doi: 10.1093/nar/27.8.1935. [DOI] [PMC free article] [PubMed] [Google Scholar]
156.Anderson C.T., Friedberg E.C. The presence of nuclear and mitochondrial uracil-DNA glycosylase in extracts of human KB cells. Nucleic Acids Research. 1980;8(4):875–888. [PMC free article] [PubMed] [Google Scholar]
157.Caradonna S., Ladner R., Hansbury M., Kosciuk M., Lynch F., Muller S. Affinity purification and comparative analysis of two distinct human uracil DNA glycosylases. Exp Cell Res. 1996;222(2):345–359. doi: 10.1006/excr.1996.0044. [DOI] [PubMed] [Google Scholar]
158.Nilsen H., Otterlei M., Haug T., et al. Nuclear and mitochondrial uracil-DNA glycosylases are generated by alternative splicing and transcription from different positions in the UNG gene. Nucleic Acids Research. 1997;25(4):750–755. doi: 10.1093/nar/25.4.750. [DOI] [PMC free article] [PubMed] [Google Scholar]
159.Tomkinson AE, Bonk RT, Linn S. Mitochondrial endonuclease activities specific for apurinic/apyrimidinic sites in DNA from mouse cells. Journal of Biological Chemistry. 1988;263(25):12532–12537. [PubMed]
160.Croteau DL, ap Rhys CM, Hudson EK, Dianov GL, Hansford RG, Bohr VA. An oxidative damage-specific endonuclease from rat liver mitochondria. J Biol Chem. 1997;272(43):27338–27344. [DOI] [PubMed]
161.Rosenquist T.A., Zharkov D.O., Grollman A.P. Cloning and characterization of a mammalian 8-oxoguanine DNA glycosylase. Proc Natl Acad Sci U S A. 1997;94(14):7429–7434. doi: 10.1073/pnas.94.14.7429. [DOI] [PMC free article] [PubMed] [Google Scholar]
162.Takao M., Aburatani H., Kobayashi K., Yasui A. Mitochondrial targeting of human DNA glycosylases for repair of oxidative DNA damage. Nucleic Acids Res. 1998;26(12):2917–2922. doi: 10.1093/nar/26.12.2917. [DOI] [PMC free article] [PubMed] [Google Scholar]
163.Vanderstraeten S, Van den Brule S, Hu J, Foury F. The role of 3′-5′ exonucleolytic proofreading and mismatch repair in yeast mitochondrial DNA error avoidance. J Biol Chem. 1998; 273(37):23690–23697. [DOI] [PubMed]
164.Pinz K.G., Bogenhagen D.F. Efficient repair of abasic sites in DNA by mitochondrial enzymes. Mol Cell Biol. 1998;18(3):1257–1265. doi: 10.1128/mcb.18.3.1257. [DOI] [PMC free article] [PubMed] [Google Scholar]
165.Reenan R.A., Kolodner R.D. Characterization of insertion mutations in the Saccharomyces cerevisiae MSH1 and MSH2 genes: evidence for separate mitochondrial and nuclear functions. Genetics. 1992;132:975–985. doi: 10.1093/genetics/132.4.975. [DOI] [PMC free article] [PubMed] [Google Scholar]
166.Shadel G.S., Clayton D.A. Mitochondrial DNA maintenance in vertebrates. Annu Rev Biochem. 1997;66:409–435. doi: 10.1146/annurev.biochem.66.1.409. [DOI] [PubMed] [Google Scholar]
167.Awadalla P., Eyre-Walker A., Smith J.M. Linkage disequilibrium and recombination in hominid mitochondrial DNA. Science. 1999;286(5449):2524–2525. doi: 10.1126/science.286.5449.2524. [DOI] [PubMed] [Google Scholar]
168.Hagelberg E., Goldman N., Lio P., et al. Evidence for mitochondrial DNA recombination in a human population of island Melanesia. Proc R Soc Lond B Biol Sci. 1999;266(1418):485–492. doi: 10.1098/rspb.1999.0663. [DOI] [PMC free article] [PubMed] [Google Scholar]
169.Ikeda S., Ozaki K. Action of mitochondrial endonuclease G on DNA damaged by L-ascorbic acid, peplomycin, and cis-diamminedichloroplatinum (II) Biochem Biophys Res Commun. 1997;235(2):291–294. doi: 10.1006/bbrc.1997.6786. [DOI] [PubMed] [Google Scholar]
170.Le X.C., Xing J.Z., Lee J., Leadon S.A., Weinfeld M. Inducible repair of thymine glycol detected by an ultrasensitive assay for DNA damage. Science. 1998;280(5366):1066–1069. doi: 10.1126/science.280.5366.1066. [DOI] [PubMed] [Google Scholar]
171.Ku H.H., Sohal R.S. Comparison of mitochondrial pro-oxidant generation and anti-oxidant defenses between rat and pigeon: possible basis of variation in longevity and metabolic potential. Mechanisms of Ageing and Development. 1993;72:67–76. doi: 10.1016/0047-6374(93)90132-B. [DOI] [PubMed] [Google Scholar]
172.Barja G., Cadenas S., Rojas C., Perez-Campo R., Lopez-Torres M. Low mitochondrial free radical production per unit O2 consumption can explain the simultaneous presence of high longevity and high aerobic metabolic rate in birds. Free Radic Res. 1994;21(5):317–327. doi: 10.3109/10715769409056584. [DOI] [PubMed] [Google Scholar]
173.Ogburn C.E., Austad S.N., Holmes D.J., et al. Cultured renal epithelial cells from birds and mice: Enhanced resistance of avian cells to oxidative stress and DNA damage. Journals of Gerontology Series A-Biological Sciences and Medical Sciences. 1998;53(4):B287–B292. doi: 10.1093/gerona/53a.4.b287. [DOI] [PubMed] [Google Scholar]
174.Herrero A., Barja G. 8-oxo-deoxyguanosine levels in heart and brain mitochondrial and nuclear DNA of two mammals and three birds in relation to their different rates of aging. Aging-Clinical And Experimental Research. 1999;11(5):294–300. doi: 10.1007/BF03339803. [DOI] [PubMed] [Google Scholar]
175.Barja G., Herrero A. Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. FASEB Journal. 2000;14(2):312–318. doi: 10.1096/fasebj.14.2.312. [DOI] [PubMed] [Google Scholar]
176.Williams MD, Van Remmen H, Conrad CC, Huang TT, Epstein CJ, Richardson A. Increased oxidative damage is correlated to altered mitochondrial function in heterozygous manganese superoxide dismutase knockout mice. J Biol Chem. 1998;273(43):28510–28515. [DOI] [PubMed]

[CR1] 1.Harman D. Aging: A theory based on free radical and radiation chemistry. Journal of Gerontology. 1956;11:298–300. doi: 10.1093/geronj/11.3.298. [DOI] [PubMed] [Google Scholar]

[CR2] 2.Szilard L. On the nature of the aging process. Proceedings of the National Academy of Sciences of the United States of America. 1959;45:30–45. doi: 10.1073/pnas.45.1.30. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR3] 3.Stein G., Weiss J. Chemical effects of ionizing radiations. Nature. 1948;161:650. doi: 10.1038/161650a0. [DOI] [PubMed] [Google Scholar]

[CR4] 4.Commoner B., Townsend J., Pakke G.E. Free radicals in biological materials. Nature. 1954;174:689–691. doi: 10.1038/174689a0. [DOI] [PubMed] [Google Scholar]

[CR5] 5.Grollman A.P., Moriya M. Mutagenesis by 8-oxoguanine: an enemy within. Trends in Genetics. 1993;9:246–249. doi: 10.1016/0168-9525(93)90089-Z. [DOI] [PubMed] [Google Scholar]

[CR6] 6.Purmal A.A., Kow Y.W., Wallace S.S. Major oxidative products of cytosine, 5-hydroxycytosine and 5-hydroxyuracil, exhibit sequence context-dependent mispairing in vitro. Nucleic Acids Research. 1994;22:72–78. doi: 10.1093/nar/22.1.72. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR7] 7.Collins A.R. Oxidative DNA damage, antioxidants, and cancer. BioEssays. 1999;21(3):238–246. doi: 10.1002/(SICI)1521-1878(199903)21:3<238::AID-BIES8>3.0.CO;2-3. [DOI] [PubMed] [Google Scholar]

[CR8] 8.Stuart G.R., Oda Y., de Boer J.G., Glickman B.W. Mutation frequency and specificity with age in liver, bladder and brain of lacl transgenic mice. Genetics. 2000;154(3):1291–1300. doi: 10.1093/genetics/154.3.1291. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR9] 9.Jones O.T. The mechanism of the production of superoxide by phagocytes. Mol Chem Neuropathol. 1993;19(1–2):177–184. doi: 10.1007/BF03160177. [DOI] [PubMed] [Google Scholar]

[CR10] 10.Rodeberg D.A., Chaet M.S., Bass R.C., Arkovitz M.S., Garcia V.F. Nitric oxide: an overview. Am J Surg. 1995;170(3):292–303. doi: 10.1016/s0002-9610(05)80017-0. [DOI] [PubMed] [Google Scholar]

[CR11] 11.May J.M., de Haen C. The insulin-like effect of hydrogen peroxide on pathways of lipid synthesis in rat adipocytes. J Biol Chem. 1979;254(18):9017–9021. [PubMed] [Google Scholar]

[CR12] 12.May J.M., de Haen C. Insulin-stimulated intracellular hydrogen peroxide production in rat epididymal fat cells. J Biol Chem. 1979;254(7):2214–2220. [PubMed] [Google Scholar]

[CR13] 13.Krieger-Brauer H.I., Kather H. Human fat cells possess a plasma membrane-bound H202-generating system that is activated by insulin via a mechanism bypassing the receptor kinase. J Clin Invest. 1992;89(3):1006–1013. doi: 10.1172/JCI115641. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR14] 14.Krieger-Brauer HI, Medda PK, Kather H. Insulin-induced activation of NADPH-dependent H202 generation in human adipocyte plasma membranes is mediated by Galphai2. J Biol Chem. 1997; 272(15):10135–10143. [DOI] [PubMed]

[CR15] 15.Sasaki H., Kodama K., Yamada M. A review of forty-five years study of Hiroshima and Nagasaki atomic bomb survivors. Aging. J Radiat Res (Tokyo) 1991;32(Suppl):310–326. doi: 10.1269/jrr.32.SUPPLEMENT_310. [DOI] [PubMed] [Google Scholar]

[CR16] 16.Beckman K.B., Ames B.N. The free radical theory of aging matures. Physiol Rev. 1998;78(2):547–581. doi: 10.1152/physrev.1998.78.2.547. [DOI] [PubMed] [Google Scholar]

[CR17] 17.Harman D. The biologic clock: the mitochondria? J Am Geriatr Soc. 1972;20(4):145–147. doi: 10.1111/j.1532-5415.1972.tb00787.x. [DOI] [PubMed] [Google Scholar]

[CR18] 18.Miquel J., Economos A.C., Fleming J., Johnson J.E., Jr Mitochondrial role in cell aging. Exp Gerontol. 1980;15(6):575–591. doi: 10.1016/0531-5565(80)90010-8. [DOI] [PubMed] [Google Scholar]

[CR19] 19.Shearman C.W., Kalf G.F. DNA replication by a membrane-DNA complex from rat liver mitochondria. Arch Biochem Biophys. 1977;182(2):573–586. doi: 10.1016/0003-9861(77)90539-2. [DOI] [PubMed] [Google Scholar]

[CR20] 20.Singh G., Sharkey S.M., Moorehead R. Mitochondrial DNA damage by anticancer agents. Pharmacology and Therapeutics. 1992;54:217–230. doi: 10.1016/0163-7258(92)90033-V. [DOI] [PubMed] [Google Scholar]

[CR21] 21.Davis A.F., Clayton D.A. In situ localization of mitochondrial DNA replication in intact mammalian cells. J Cell Biol. 1996;135(4):883–893. doi: 10.1083/jcb.135.4.883. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR22] 22.Bandy B., Davison A.J. Mitochondrial mutations may increase oxidative stress: implications for carcinogenesis and aging? Free Radical Biology and Medicine. 1990;8:523–539. doi: 10.1016/0891-5849(90)90152-9. [DOI] [PubMed] [Google Scholar]

[CR23] 23.Kasai H., Nishimura S. Hydroxylation of the C-8 position of deoxyguanosine by reducing agents in the presence of oxygen. Nucleic Acids Symp Ser. 1983;12:165–167. [PubMed] [Google Scholar]

[CR24] 24.Kasai H., Nishimura S. Hydroxylation of deoxy guanosine at the C-8 position by polyphenols and aminophenols in the presence of hydrogen peroxide and ferric ion. Gann. 1984;75(7):565–566. [PubMed] [Google Scholar]

[CR25] 25.Kasai H., Nishimura S. Hydroxylation of deoxyguanosine at the C-8 position by ascorbic acid and other reducing agents. Nucleic Acids Res. 1984;12(4):2137–2145. doi: 10.1093/nar/12.4.2137. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR26] 26.Kasai H., Nishimura S. DNA damage induced by asbestos in the presence of hydrogen peroxide. Gann. 1984;75(10):841–844. [PubMed] [Google Scholar]

[CR27] 27.Kasai H., Tanooka H., Nishimura S. Formation of 8-hydroxyguanine residues in DNA by X-irradiation. Gann. 1984;75(12):1037–1039. [PubMed] [Google Scholar]

[CR28] 28.Floyd R.A., Watson J.J., Wong P.K., Altmiller D.H., Rickard R.C. Hydroxyl free radical adduct of deoxyguanosine: sensitive detection and mechanisms of formation. Free Radical Research Communications. 1986;1(3):163–172. doi: 10.3109/10715768609083148. [DOI] [PubMed] [Google Scholar]

[CR29] 29.Kouchakdjian M., Bodepudi V., Shibutani S., et al. NMR structural studies of the ionizing radiation adduct 7-hydro-8-oxodeoxyguanosine (8-oxo-7H-dG) opposite deoxyadenosine in a DNA duplex. 8-Oxo-7H-dG(syn).dA(anti) alignment at lesion site. Biochemistry. 1991;30:1403–1412. doi: 10.1021/bi00219a034. [DOI] [PubMed] [Google Scholar]

[CR30] 30.McAuley-Hecht KE, Leonard GA, Gibson NJ, et al. Crystal structure of a DNA duplex containing 8-hydroxydeoxyguanine-adenine base pairs. Biochemistry. 1994;33(34):10266–10270. [DOI] [PubMed]

[CR31] 31.Shibutani S., Takeshita M., Grollman A.P. Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature. 1991;349:431–434. doi: 10.1038/349431a0. [DOI] [PubMed] [Google Scholar]

[CR32] 32.Pinz K.G., Shibutani S., Bogenhagen D.F. Action of mitochondrial DNA polymerase gamma at sites of base loss or oxidative damage. Journal of Biological Chemistry. 1995;270(16):9202–9206. doi: 10.1074/jbc.270.16.9202. [DOI] [PubMed] [Google Scholar]

[CR33] 33.Moraes E.C., Keyse S.M., Tyrrell R.M. Mutagenesis by hydrogen peroxide treatment of mammalian cells: a molecular analysis. Carcinogenesis. 1990;11:283–293. doi: 10.1093/carcin/11.2.283. [DOI] [PubMed] [Google Scholar]

[CR34] 34.Tkeshelashvili L.K., McBride T., Spence K., Loeb L.A. Mutation spectrum of copper-induced DNA damage. J Biol Chem. 1991;266(10):6401–6406. [PubMed] [Google Scholar]

[CR35] 35.Michaels M.L., Pham L., Cruz C., Miller J.H. MutM, a protein that prevents G.C—T.A transversions, is formamidopyrimidine-DNA glycosylase. Nucleic Acids Research. 1991;19:3629–3632. doi: 10.1093/nar/19.13.3629. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR36] 36.Radicella J.P., Dherin C., Desmaze C., Fox M.S., Boiteux S. Cloning and characterization of hOGG1, a human homolog of the OGG1 gene of Saccharomyces cerevisiae. Proc Natl Acad Sci USA. 1997;94(15):8010–8015. doi: 10.1073/pnas.94.15.8010. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR37] 37.Suter M., Richter C. Fragmented mitochondrial DNA is the predominant carrier of oxidized DNA bases. Biochemistry. 1999;38(1):459–464. doi: 10.1021/bi9811922. [DOI] [PubMed] [Google Scholar]

[CR38] 38.Helbock H.J., Beckman K.B., Shigenaga M.K., et al. DNA oxidation matters: the HPLC-electrochemical detection assay of 8-oxo-deoxyguanosine and 8-oxo-guanine. Proc Natl Acad Sci USA. 1998;95(1):288–293. doi: 10.1073/pnas.95.1.288. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR39] 39.Hayakawa M., Ogawa T., Sugiyama S., Tanaka M., Ozawa T. Massive conversion of guanosine to 8-hydroxy-guanosine in mouse liver mitochondrial DNA by administration of azidothymidine. Biochemical and Biophysical Research Communications. 1991;176:87–93. doi: 10.1016/0006-291X(91)90893-C. [DOI] [PubMed] [Google Scholar]

[CR40] 40.Dizdaroglu M. Chemical determination of oxidative DNA damage by gas chromatography-mass spectrometry. Methods Enzymol. 1994;234:3–16. doi: 10.1016/0076-6879(94)34072-2. [DOI] [PubMed] [Google Scholar]

[CR41] 41.Wassermann K, Kohn KW, Bohr VA. Heterogeneity of nitrogen mustard-induced DNA damage and repair at the level of the gene in Chinese hamster ovary cells. Journal of Biological Chemistry. 1990;265:13906–13913. [PubMed]

[CR42] 42.Epe B., Hegler J., Wild D. Singlet oxygen as an ultimately reactive species in Salmonella typhimurium DNA damage induced by methylene blue/visible light. Carcinogenesis. 1989;10:2019–2024. doi: 10.1093/carcin/10.11.2019. [DOI] [PubMed] [Google Scholar]

[CR43] 43.Hegler J., Bittner D., Boiteux S., Epe B. Quantification of oxidative DNA modifications in mitochondria. Carcinogenesis. 1993;14:2309–2312. doi: 10.1093/carcin/14.11.2309. [DOI] [PubMed] [Google Scholar]

[CR44] 44.Bohr V.A., Smith C.A., Okumoto D.S., Hanawalt P.C. DNA repair in an active gene: removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell. 1985;40(2):359–369. doi: 10.1016/0092-8674(85)90150-3. [DOI] [PubMed] [Google Scholar]

[CR45] 45.Bohr V.A., Okumoto D.S. Analysis of pyrimidine dimers in defined genes. In: Friedberg E.C., Hanawalt P.C., editors. DNA Repair: A laboratory manual of research procedures, VoL III. 0 ed. New York and Basel: Marcel Dekker, Inc.; 1988. pp. 347–366. [Google Scholar]

[CR46] 46.Kalinowski D.P., Illenye S., Van Houten B. Analysis of DNA damage and repair in murine leukemia L1210 cells using a quantitative polymerase chain reaction assay. Nucleic Acids Research. 1992;20(13):3485–3494. doi: 10.1093/nar/20.13.3485. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR47] 47.Yakes F.M., Van Houten B. Mitochondrial DNA damage is more extensive and persists longer than nuclear DNA damage in human cells following oxidative stress. Proc Natl Acad Sci USA. 1997;94(2):514–519. doi: 10.1073/pnas.94.2.514. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR48] 48.Drouin R., Rodriguez H., Holmquist G.P., Akman S.A. In vivo Cu-H202-and H202-induced DNA damage maps show the same oxidative damage frequency for each nucleotide position. Proceedings of the National Academy of Sciences of the United States of America. 1995;36:550. [Google Scholar]

[CR49] 49.Rodriguez H, Drouin R, Holmquist GP, et al. Mapping of copper hydrogen peroxide-induced DNA damage at nucleotide resolution in human genomic DNA by ligation-mediated polymerase chain reaction. Journal of Biological Chemistry. 1995;270:17633–17640. [DOI] [PubMed]

[CR50] 50.Driggers W.J., Holmquist G.P., LeDoux S.P., Wilson G.L. Mapping frequencies of endogenous oxidative damage and the kinetic response to oxidative stress in a region of rat mtDNA. Nucleic Acids Res. 1997;25(21):4362–4369. doi: 10.1093/nar/25.21.4362. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR51] 51.Mueller P.R., Wold B. In vivo footprinting of a muscle specific enhancer by Ligation Mediated PCR. Science. 1989;246:780–786. doi: 10.1126/science.2814500. [DOI] [PubMed] [Google Scholar]

[CR52] 52.Pfeifer G.P., Drouin R., Riggs A.D., Holmquist G.P. Binding of transcription factors creates hot spots for UV photoproducts in vivo. Mol Cell Biol. 1992;12:1798–1804. doi: 10.1128/mcb.12.4.1798. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR53] 53.Soultanakis R.P., Melamede R.J., Bespalov I.A., et al. Fluorescence detection of 8-oxoguanine in nuclear and mitochondrial DNA of cultured cells using a recombinant fab and confocal scanning laser microscopy. Free Radic Biol Med. 2000;28(6):987–998. doi: 10.1016/S0891-5849(00)00185-4. [DOI] [PubMed] [Google Scholar]

[CR54] 54.Beckman KB, Ames BN. Oxidative decay of DNA. J Biol Chem. 1997;272(32):19633–19636. [DOI] [PubMed]

[CR55] 55.Collins A., Cadet J., Epe B., Gedik C. Problems in the measurement of 8-oxoguanine in human DNA. Carcinogenesis. 1997;18(9):1833–1836. doi: 10.1093/carcin/18.9.1833. [DOI] [PubMed] [Google Scholar]

[CR56] 56.ESCODD. Comparison of different methods of measuring 8-oxoguanine as a marker of oxidative DNA damage. ESCODD (European Standards Committee on Oxidative DNA Damage) Free Radic Res. 2000;32(4):333–341. doi: 10.1080/10715760000300331. [DOI] [PubMed] [Google Scholar]

[CR57] 57.Hudson E.K., Hogue B.A., Souza-Pinto N.C., et al. Age-associated change in mitochondrial DNA damage. Free Radical Research. 1998;29(6):573–579. doi: 10.1080/10715769800300611. [DOI] [PubMed] [Google Scholar]

[CR58] 58.Anson R.M., Hudson E., Bohr V.A. Mitochondrial endogenous oxidative damage has been overestimated. Faseb J. 2000;14(2):355–360. doi: 10.1096/fasebj.14.2.355. [DOI] [PubMed] [Google Scholar]

[CR59] 59.Richter C., Park J.W., Ames B.N. Normal oxidative damage to mitochondrial and nuclear DNA is extensive. Proceedings of the National Academy of Sciences of the United States of America. 1988;85(17):6465–6467. doi: 10.1073/pnas.85.17.6465. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR60] 60.Higuchi Y., Linn 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. Journal of Biological Chemistry. 1995;270(14):7950–7956. doi: 10.1074/jbc.270.14.7950. [DOI] [PubMed] [Google Scholar]

[CR61] 61.Takasawa M., Hayakawa M., Sugiyama S., Hattori K., Ito T., Ozawa T. Age-associated damage in mitochondrial function in rat hearts. Exp Gerontol. 1993;28(3):269–280. doi: 10.1016/0531-5565(93)90034-B. [DOI] [PubMed] [Google Scholar]

[CR62] 62.Beckman K.B., Ames B.N. Detection and quantification of oxidative adducts of mitochondrial DNA. Methods in Enzymology. 1996;264:442–453. doi: 10.1016/s0076-6879(96)64040-3. [DOI] [PubMed] [Google Scholar]

[CR63] 63.Beckman K.B., Ames B.N. Endogenous oxidative damage of mtDNA. Mutat Res. 1999;424(1–2):51–58. doi: 10.1016/s0027-5107(99)00007-x. [DOI] [PubMed] [Google Scholar]

[CR64] 64.Hayakawa M., Sugiyama S., Hattori K., Takasawa M., Ozawa T. Age-associated damage in mitochondrial DNA in human hearts. Mol Cell Biochem. 1993;119:95–103. doi: 10.1007/BF00926859. [DOI] [PubMed] [Google Scholar]

[CR65] 65.Zastawny T.H., Dabrowska M., Jaskolski T., et al. Comparison of oxidative base damage in mitochondria and nuclear DNA. Free Radic Biol Med. 1998;24(5):722–725. doi: 10.1016/S0891-5849(97)00331-6. [DOI] [PubMed] [Google Scholar]

[CR66] 66.Anson R.M., Senturker S., Dizdaroglu M., Bohr V.A. Measurement of oxidatively induced base lesions in liver from Wistar rats of different ages. Free Radic Biol Med. 1999;27(3–4):456–462. doi: 10.1016/S0891-5849(99)00091-X. [DOI] [PubMed] [Google Scholar]

[CR67] 67.Chung M.H., Kasai H., Nishimura S., Yu B.P. Protection of DNA damage by dietary restriction. Free Radical Biology and Medicine. 1992;12(6):523–525. doi: 10.1016/0891-5849(92)90105-P. [DOI] [PubMed] [Google Scholar]

[CR68] 68.Sohal R.S., Agarwal S., Candas M., Forster M.J., Lal H. Effect of age and caloric restriction on DNA oxidative damage in different tissues of C57BL/6 mice. Mechanisms of Ageing and Development. 1994;76:215–224. doi: 10.1016/0047-6374(94)91595-4. [DOI] [PubMed] [Google Scholar]

[CR69] 69.Lass A., Sohal B.H., Weindruch R., Forster M.J., Sohal R.S. Caloric restriction prevents age-associated accrual of oxidative damage to mouse skeletal muscle mitochondria. Free Radic Biol Med. 1998;25(9):1089–1097. doi: 10.1016/S0891-5849(98)00144-0. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR70] 70.Masoro E.J. Dietary restriction. Exp Gerontol. 1995;30(3–4):291–298. doi: 10.1016/0531-5565(94)00028-2. [DOI] [PubMed] [Google Scholar]

[CR71] 71.Cortopassi G.A., Arnheim N. Detection of a specific mitochondrial DNA deletion in tissues of older humans. Nucleic Acids Res. 1990;18(23):6927–6933. doi: 10.1093/nar/18.23.6927. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR72] 72.Linnane A.W., Baumer A., Maxwell R.J., Preston H., Zhang C.F., Marzuki S. Mitochondrial gene mutation: the ageing process and degenerative diseases. Biochemistry International. 1990;22:1067–1076. [PubMed] [Google Scholar]

[CR73] 73.Cortopassi G.A., Shibata D., Soong N.W., Arnheim N. A pattern of accumulation of a somatic deletion of mitochondrial DNA in aging human tissues. Proceedings of the National Academy of Science USA. 1992;89:7370–7374. doi: 10.1073/pnas.89.16.7370. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR74] 74.Simonetti S., Chen X., DiMauro S., Schon E.A. Accumulation of deletions in human mitochondrial DNA during normal aging: analysis by quantitative PCR. Biochim Biophys Acta. 1992;1180(2):113–122. doi: 10.1016/0925-4439(92)90059-v. [DOI] [PubMed] [Google Scholar]

[CR75] 75.Lee H.C., Pang C.Y., Hsu H.S., Wei Y.H. Differential accumulations of 4,977 bp deletion in mitochondrial DNA of various tissues in human ageing. Biochim Biophys Acta. 1994;1226(1):37–43. doi: 10.1016/0925-4439(94)90056-6. [DOI] [PubMed] [Google Scholar]

[CR76] 76.Filser N., Margue C., Richter C. Quantification of wild-type mitochondrial DNA and its 4.8-kb deletion in rat organs. Biochem Biophys Res Commun. 1997;233(1):102–107. doi: 10.1006/bbrc.1997.6409. [DOI] [PubMed] [Google Scholar]

[CR77] 77.Liu V.W., Zhang C., Pang C.Y., et al. Independent occurrence of somatic mutations in mitochondrial DNA of human skin from subjects of various ages. Hum Mutat. 1998;11(3):191–196. doi: 10.1002/(SICI)1098-1004(1998)11:3<191::AID-HUMU2>3.0.CO;2-L. [DOI] [PubMed] [Google Scholar]

[CR78] 78.Soong N.W., Hinton D.R., Cortopassi G., Arnheim N. Mosaicism for a specific somatic mitochondrial DNA mutation in adult human brain. Nat Genet. 1992;2(4):318–323. doi: 10.1038/ng1292-318. [DOI] [PubMed] [Google Scholar]

[CR79] 79.Corral-Debdnski M., Horton T., Lott M.T., Shoffner J.M., Beal M.F., Wallace D.C. Mitochondrial DNA deletions in human brain: regional variability and increase with advanced age. Nat Genet. 1992;2:324–329. doi: 10.1038/ng1292-324. [DOI] [PubMed] [Google Scholar]

[CR80] 80.Filburn C.R., Edris W., Tamatani M., Hogue B., Kudryashova I., Hansford R.G. Mitochondrial electron transport chain activities and DNA deletions in regions of the rat brain. Mech Ageing Dev. 1996;87(1):35–46. doi: 10.1016/0047-6374(96)01696-X. [DOI] [PubMed] [Google Scholar]

[CR81] 81.Luo Y, Roth GS. The roles of dopamine oxidative stress and dopamine receptor signaling in aging and age-related neurodegeneration. Antioxidants and Redox Signaling. 2000;In Press. [DOI] [PubMed]

[CR82] 82.de Grey A.D. A proposed refinement of the mitochondrial free radical theory of aging. Bioessays. 1997;19(2):161–166. doi: 10.1002/bies.950190211. [DOI] [PubMed] [Google Scholar]

[CR83] 83.Gershon D. The mitochondrial theory of aging: is the culprit a faulty disposal system rather than indigenous mitochondrial alterations? Exp Gerontol. 1999;34(5):613–619. doi: 10.1016/S0531-5565(99)00010-8. [DOI] [PubMed] [Google Scholar]

[CR84] 84.Kowald A. The mitochondrial theory of aging: do damaged mitochondria accumulate by delayed degradation? Exp Gerontol. 1999;34(5):605–612. doi: 10.1016/S0531-5565(99)00011-X. [DOI] [PubMed] [Google Scholar]

[CR85] 85.Wang E., Wong A., Cortopassi G. The rate of mitochondrial mutagenesis is faster in mice than humans. Mutat Res. 1997;377(2):157–166. doi: 10.1016/s0027-5107(97)00091-2. [DOI] [PubMed] [Google Scholar]

[CR86] 86.Hattori K., Tanaka M., Sugiyama S., et al. Age-dependent increase in deleted mitochondrial DNA in the human heart: possible contributory factor to presbycardia. American Heart Journal. 1991;121:1735–1742. doi: 10.1016/0002-8703(91)90020-I. [DOI] [PubMed] [Google Scholar]

[CR87] 87.Katayama M., Tanaka M., Yamamoto H., Ohbayashi T., Nimura Y., Ozawa T. Deleted mitochondrial DNA in the skeletal muscle of aged individuals. Biochem Int. 1991;25(1):47–56. [PubMed] [Google Scholar]

[CR88] 88.Zhang C., Baumer A., Maxwell R.J., Linnane A.W., Nagley P. Multiple mitochondrial DNA deletions in an eldedy human individual. FEBS Lett. 1992;297(1–2):34–38. doi: 10.1016/0014-5793(92)80321-7. [DOI] [PubMed] [Google Scholar]

[CR89] 89.Lee C.M., Chung S.S., Kaczkowski J.M., Weindruch R., Aiken J.M. Multiple mitochondrial DNA deletions associated with age in skeletal muscle of rhesus monkeys. Journal of Gerontology. 1993;48:B201–B205. doi: 10.1093/geronj/48.6.b201. [DOI] [PubMed] [Google Scholar]

[CR90] 90.Melov S., Shoffner J.M., Kaufman A., Wallace D.C. Marked increase in the number and variety of mitochondrial DNA rearrangements in aging human skeletal muscle. Nucleic Acids Res. 1995;23(20):4122–4126. doi: 10.1093/nar/23.20.4122. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR91] 91.Reynier P., Malthiery Y. Accumulation of deletions in MtDNA during tissue aging: analysis by long PCR. Biochem Biophys Res Commun. 1995;217(1):59–67. doi: 10.1006/bbrc.1995.2745. [DOI] [PubMed] [Google Scholar]

[CR92] 92.Eimon P.M., Chung S.S., Lee C.M., Weindruch R., Aiken J.M. Age-associated mitochondrial DNA deletions in mouse skeletal muscle: comparison of different regions of the mitochondrial genome. Dev Genet. 1996;18(2):107–113. doi: 10.1002/(SICI)1520-6408(1996)18:2<107::AID-DVG3>3.0.CO;2-D. [DOI] [PubMed] [Google Scholar]

[CR93] 93.Tengan C.H., Moraes C.T. Detection and analysis of mitochondrial DNA deletions by whole genome PCR. Biochem Mol Med. 1996;58(1):130–134. doi: 10.1006/bmme.1996.0040. [DOI] [PubMed] [Google Scholar]

[CR94] 94.Zhang C., Liu V.W., Addessi C.L., Sheffield D.A., Linnane A.W., Nagley P. Differential occurrence of mutations in mitochondrial DNA of human skeletal muscle during aging. Hum Mutat. 1998;11(5):360–371. doi: 10.1002/(SICI)1098-1004(1998)11:5<360::AID-HUMU3>3.0.CO;2-U. [DOI] [PubMed] [Google Scholar]

[CR95] 95.Lee H.C., Pang C.Y., Hsu H.S., Wei Y.H. Ageing-associated tandem duplications in the D-loop of mitochondrial DNA of human muscle. FEBS Lett. 1994;354(1):79–83. doi: 10.1016/0014-5793(94)01063-3. [DOI] [PubMed] [Google Scholar]

[CR96] 96.Wei Y.H., Pang C.Y., You B.J., Lee H.C. Tandem duplications and large-scale deletions of mitochondrial DNA are early molecular events of human aging process. Ann N Y Acad Sci. 1996;786:82–101. doi: 10.1111/j.1749-6632.1996.tb39054.x. [DOI] [PubMed] [Google Scholar]

[CR97] 97.Schwarze S.R., Lee C.M., Chung S.S., Roecker E.B., Weindruch R., Aiken J.M. High levels of mitochondrial DNA deletions in skeletal muscle of old rhesus monkeys. Mech Ageing Dev. 1995;83(2):91–101. doi: 10.1016/0047-6374(95)01611-3. [DOI] [PubMed] [Google Scholar]

[CR98] 98.Muller-Hocker J., Seibel P., Schneiderbanger K., Kadenbach B. Different in situ hybridization patterns of mitochondrial DNA in cytochrome c oxidase-deficient extraocular muscle fibres in the elderly. Virchows Arch A Pathol Anat Histopathol. 1993;422(1):7–15. doi: 10.1007/BF01605127. [DOI] [PubMed] [Google Scholar]

[CR99] 99.Moslemi A.R., Melberg A., Holme E., Oldfors A. Clonal expansion of mitochondrial DNA with multiple deletions in autosomal dominant progressive external ophthalmoplegia. Ann Neurol. 1996;40(5):707–713. doi: 10.1002/ana.410400506. [DOI] [PubMed] [Google Scholar]

[CR100] 100.Muller-Hocker J., Jacob U., Seibel P. Hashimoto thyroiditis is associated with defects of cytochrome-c oxidase in oxyphil Askanazy cells and with the common deletion (4,977) of mitochondrial DNA. Ultrastruct Pathol. 1998;22(1):91–100. doi: 10.3109/01913129809032263. [DOI] [PubMed] [Google Scholar]

[CR101] 101.Prelle A., Fagiolari G., Checcarelli N., et al. Mitochondrial myopathy: correlation between oxidative defect and mitochondrial DNA deletions at single fiber level. Acta Neuropathol (Berl) 1994;87(4):371–376. doi: 10.1007/BF00313606. [DOI] [PubMed] [Google Scholar]

[CR102] 102.Lee C.M., Lopez M.E., Weindruch R., Aiken J.M. Association of age-related mitochondrial abnormalities with skeletal muscle fiber atrophy. Free Radic Biol Med. 1998;25(8):964–972. doi: 10.1016/S0891-5849(98)00185-3. [DOI] [PubMed] [Google Scholar]

[CR103] 103.Hayakawa M., Torii K., Sugiyama S., Tanaka M., Ozawa T. Age-associated accumulation of 8-hydroxydeoxyguanosine in mitochondrial DNA of human diaphragm. Biochem Biophys Res Commun. 1991;179(2):1023–1029. doi: 10.1016/0006-291X(91)91921-X. [DOI] [PubMed] [Google Scholar]

[CR104] 104.Hayakawa M., Hattori K., Sugiyama S., Ozawa T. Age-associated oxygen damage and mutations in mitochondrial DNA in human hearts. Biochemical and Biophysical Research Communications. 1992;189:979–985. doi: 10.1016/0006-291X(92)92300-M. [DOI] [PubMed] [Google Scholar]

[CR105] 105.Yen T.C., King K.L., Lee H.C., Yeh S.H., Wei Y.H. Age-dependent increase of mitochondrial DNA deletions together with lipid peroxides and superoxide dismutase in human liver mitochondria. Free Radic Biol Med. 1994;16(2):207–214. doi: 10.1016/0891-5849(94)90145-7. [DOI] [PubMed] [Google Scholar]

[CR106] 106.Wei Y.H., Kao S.H., Lee H.C. Simultaneous increase of mitochondrial DNA deletions and lipid peroxidation in human aging. Ann N Y Acad Sci. 1996;786:24–43. doi: 10.1111/j.1749-6632.1996.tb39049.x. [DOI] [PubMed] [Google Scholar]

[CR107] 107.Lezza A.M., Mecocci P., Cormio A., et al. Mitochondrial DNA 4977 bp deletion and OH8dG levels correlate in the brain of aged subjects but not Alzheimer’s disease patients. Faseb J. 1999;13(9):1083–1088. doi: 10.1096/fasebj.13.9.1083. [DOI] [PubMed] [Google Scholar]

[CR108] 108.Muscari C., Giaccari A., Stefanelli C., et al. Presence of a DNA-4236 bp deletion and 8-hydroxy-deoxyguanosine in mouse cardiac mitochondrial DNA during aging. Aging (Milano) 1996;8(6):429–433. doi: 10.1007/BF03339606. [DOI] [PubMed] [Google Scholar]

[CR109] 109.Aruoma O.I., Halliwell B., Gajewski E., Dizdaroglu M. Copper-ion-dependent damage to the bases in DNA in the presence of hydrogen peroxide. Biochemical Journal. 1991;273:601–604. doi: 10.1042/bj2730601. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR110] 110.Yamamoto F., Kasai H., Togashi Y., Takeichi N., Hori T., Nishimura S. Elevated level of 8-hydroxydeoxyguanosine in DNA of liver, kidneys, and brain of Long-Evans Cinnamon rats. Japanese Joumal of Cancer Research. 1993;84(5):508–511. doi: 10.1111/j.1349-7006.1993.tb00168.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR111] 111.Mansouri A., Gaou I., Fromenty B., et al. Premature oxidative aging of hepatic mitochondrial DNA in Wilson’s disease. Gastroenterology. 1997;113(2):599–605. doi: 10.1053/gast.1997.v113.pm9247482. [DOI] [PubMed] [Google Scholar]

[CR112] 112.Kubota N., Hayashi J., Inada T., Iwamura Y. Induction of a particular deletion in mitochondrial DNA by X rays depends on the inherent radiosensitivity of the cells. Radiat Res. 1997;148(4):395–398. [PubMed] [Google Scholar]

[CR113] 113.Lezza A.M., Boffoli D., Scacco S., Cantatore P., Gadaleta M.N. Correlation between mitochondrial DNA 4977-bp deletion and respiratory chain enzyme activities in aging human skeletal muscles. Biochem Biophys Res Commun. 1994;205(1):772–779. doi: 10.1006/bbrc.1994.2732. [DOI] [PubMed] [Google Scholar]

[CR114] 114.Tengan C.H., Gabbai A.A., Shanske S., Zeviani M., Moraes C.T. Oxidative phosphorylation dysfunction does not increase the rate of accumulation of age-related mtDNA deletions in skeletal muscle. Mutat Res. 1997;379(1):1–11. doi: 10.1016/s0027-5107(97)00076-6. [DOI] [PubMed] [Google Scholar]

[CR115] 115.Pacifici R.E., Davies K.J. Protein, lipid and DNA repair systems in oxidative stress: the free-radical theory of aging revisited. Gerontology. 1991;37:166–180. doi: 10.1159/000213257. [DOI] [PubMed] [Google Scholar]

[CR116] 116.McCord J.M., Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein) J Biol Chem. 1969;244(22):6049–6055. [PubMed] [Google Scholar]

[CR117] 117.Reaume A.G., Elliott J.L., Hoffman E.K., et al. Motor neurons in Cu/Zn superoxide dismutase-deficient mice develop normally but exhibit enhanced cell death after axonal injury. NatGenet. 1996;13(1):43–47. doi: 10.1038/ng0596-43. [DOI] [PubMed] [Google Scholar]

[CR118] 118.Kondo T., Reaume A.G., Huang T.T., et al. Reduction of CuZn-superoxide dismutase activity exacerbates neuronal cell injury and edema formation after transient focal cerebral ischemia. J Neurosci. 1997;17(11):4180–4189. doi: 10.1523/JNEUROSCI.17-11-04180.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR119] 119.Li Y., Huang T.T., Carlson E.J., et al. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet. 1995;11(4):376–381. doi: 10.1038/ng1295-376. [DOI] [PubMed] [Google Scholar]

[CR120] 120.Melov S., Schneider J.A., Day B.J., et al. A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase. Nat Genet. 1998;18(2):159–163. doi: 10.1038/ng0298-159. [DOI] [PubMed] [Google Scholar]

[CR121] 121.Ishii N., Fujii M., Hartman P.S., et al. A mutation in succinate dehydrogenase cytochrome b causes oxidative stress and ageing in nematodes. Nature. 1998;394(6694):694–697. doi: 10.1038/29331. [DOI] [PubMed] [Google Scholar]

[CR122] 122.Guidot D.M., Repine J.E., Kitlowski A.D., et al. Mitochondrial respiration scavenges extramitochondrial superoxide anion via a nonenzymatic mechanism. J Clin Invest. 1995;96(2):1131–1136. doi: 10.1172/JCI118100. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR123] 123.Clayton D.A., Doda J.N., Friedberg E.C. The absence of a pyrimidine dimer repair mechanismin mammalian mitochondria. Proceedings of the National Academy of Sciences of the United States of America. 1974;71(7):2777–2781. doi: 10.1073/pnas.71.7.2777. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR124] 124.Ryoji M., Katayama H., Fusamae H., Matsuda A., Sakai F., Utano H. Repair of DNA damage in a mitochondrial lysate of Xenopus laevis oocytes. Nucleic Acids Research. 1996;24(20):4057–4062. doi: 10.1093/nar/24.20.4057. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR125] 125.Lansman R.A., Clayton D.A. Selective nicking of mammalian mitochondrial DNA in vivo: photosensitization by incorporation of 5-bromodeoxyuridine. Journal of Molecular Biology. 1975;99:761–776. doi: 10.1016/s0022-2836(75)80183-5. [DOI] [PubMed] [Google Scholar]

[CR126] 126.Pascucci B., Versteegh A., van Hoffen A., van Zeeland A.A., Mullenders L.H., Dogliotti E. DNA repair of UV photoproducts and mutagenesis in human mitochondrial DNA. J Mol Biol. 1997;273(2):417–427. doi: 10.1006/jmbi.1997.1268. [DOI] [PubMed] [Google Scholar]

[CR127] 127.LeDoux S.P., Wilson G.L., Beecham E.J., Stevnsner T., Wassermann K., Bohr V.A. Repair of mitochondrial DNA after various types of DNA damage in Chinese hamster ovary cells. Carcinogenesis. 1992;13:1967–1973. doi: 10.1093/carcin/13.11.1967. [DOI] [PubMed] [Google Scholar]

[CR128] 128.Bohr V.A. Gene specific DNA repair. Carcinogenesis. 1991;12:1983–1992. doi: 10.1093/carcin/12.11.1983. [DOI] [PubMed] [Google Scholar]

[CR129] 129.Mellon I., Spivak G., Hanawalt P.C. Selective removal of transcription-blocking DNA damage from the transcribed strand of the mammalian DHFR gene. Cell. 1987;51(2):241–249. doi: 10.1016/0092-8674(87)90151-6. [DOI] [PubMed] [Google Scholar]

[CR130] 130.Pfeifer G.P., Drouin R., Holmquist G.P. Detection of DNA adducts at the DNA sequence level by ligation-mediated PCR. Mutation Research. 1993;288:39–46. doi: 10.1016/0027-5107(93)90206-u. [DOI] [PubMed] [Google Scholar]

[CR131] 131.Hanawalt P.C., Gee P., Ho L., Hsu R.K., Kane C.J. Genomic heterogeneity of DNA repair. Role in aging? Annals of the New York Academy of Sciences. 1992;663:17–25. doi: 10.1111/j.1749-6632.1992.tb38644.x. [DOI] [PubMed] [Google Scholar]

[CR132] 132.Holmes G.E., Bernstein C., Bernstein H. Oxidative and other DNA damages as the basis of aging: a review. Mutation Research. 1992;275:305–315. doi: 10.1016/0921-8734(92)90034-M. [DOI] [PubMed] [Google Scholar]

[CR133] 133.Bohr V.A., Anson R.M. DNA damage, mutation and fine structure DNA repair in aging. Mutation Research. 1995;338(1–6):25–34. doi: 10.1016/0921-8734(95)00008-t. [DOI] [PubMed] [Google Scholar]

[CR134] 134.Myers K.A., Saffhill R., O’Connor P.J. Repair of alkylated purines in the hepatic DNA of mitochondria and nuclei in the rat. Carcinogenesis. 1988;9(2):285–292. doi: 10.1093/carcin/9.2.285. [DOI] [PubMed] [Google Scholar]

[CR135] 135.Satoh M.S., Huh N., Rajewsky M.F., Kuroki T. Enzymatic removal of O6-ethylguanine from mitochondrial DNA in rat tissues exposed to N-ethyl-N-nitrosourea in vivo. Journal of Biological Chemistry. 1988;263(14):6854–6856. [PubMed] [Google Scholar]

[CR136] 136.Pettepher C.C., LeDoux S.P., Bohr V.A., Wilson G.L. Repair of alkali-labile sites within the mitochondrial DNA of RINr 38 cells after exposure to the nitrosourea streptozotocin. Journal of Biological Chemistry. 1991;266:3113–3117. [PubMed] [Google Scholar]

[CR137] 137.Pirsel M., Bohr V.A. Methyl methanesulfonate adduct formation and repair in the DHFR gene and in mitochondrial DNA in hamster cells. Carcinogenesis. 1993;14:2105–2108. doi: 10.1093/carcin/14.10.2105. [DOI] [PubMed] [Google Scholar]

[CR138] 138.Cullinane C., Bohr V.A. DNA interstrand cross-links induced by psoralen are not repaired in mammalian mitochondria. Cancer Res. 1998;58(7):1400–1404. [PubMed] [Google Scholar]

[CR139] 139.Snyderwine E.G., Bohr V.A. Gene-and strand-specific damage and repair in Chinese hamster ovary cells treated with 4-nitroquinoline 1-oxide. Cancer Research. 1992;52:4183–4189. [PubMed] [Google Scholar]

[CR140] 140.Thyagarajan B, Padua RA, Campbell C. Mammalian mitochondria possess homologous DNA recombination activity. Journal of Biological Chemistry. 1996;271(44):27536–27543. [DOI] [PubMed]

[CR141] 141.Richter C. Reactive oxygen and DNA damage in mitochondria. Mutation Research. 1992;275:249–255. doi: 10.1016/0921-8734(92)90029-O. [DOI] [PubMed] [Google Scholar]

[CR142] 142.Driggers WJ, LeDoux SP, Wilson GL. Repair of oxidative damage within the mitochondrial DNA of RINr 38 cells. Journal of Biological Chemistry. 1993;268:22042–22045. [PubMed]

[CR143] 143.Chung M.H., Kiyosawa H., Ohtsuka E., Nishimura S., Kasai H. DNA strand cleavage at 8-hydroxyguanine residues by hot piperidine treatment. Biochemical and Biophysical Research Communications. 1992;188:1–7. doi: 10.1016/0006-291X(92)92341-T. [DOI] [PubMed] [Google Scholar]

[CR144] 144.Driggers W.J., Grishko V.I., LeDoux S.P., Wilson G.L. Defective repair of oxidative damage in the mitochondrial DNA of a xeroderma pigmentosum group A cell line. Cancer Research. 1996;56(6):1262–1266. [PubMed] [Google Scholar]

[CR145] 145.Shen C.C., Wertelecki W., Driggers W.J., LeDoux S.P., Wilson G.L. Repair of mitochondrial DNA damage induced by bleomycin in human cells. Mutation Research. 1995;337(1):19–23. doi: 10.1016/0921-8777(95)00008-8. [DOI] [PubMed] [Google Scholar]

[CR146] 146.Anson R.M., Croteau D.L., Stierum R.H., Filburn F., Parsell R., Bohr V.A. Homogenous repair of singlet oxygen-induced DNA damage in differentially transcribed regions and strands of human mitochondrial DNA. Nucleic Acids Research. 1998;26(2):662–668. doi: 10.1093/nar/26.2.662. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR147] 147.Taffe B.G., Larminat F., Laval J., Croteau D.L., Anson R.M., Bohr V.A. Gene-specific nuclear and mitochondrial repair of formamidopyrimidine DNA glycosylase-sensitive sites in Chinese hamster ovary cells. Mutation Research. 1996;364(3):183–192. doi: 10.1016/s0921-8777(96)00031-6. [DOI] [PubMed] [Google Scholar]

[CR148] 148.Epe B., Pflaum M., Boiteux S. DNA damage induced by photosensitizers in cellular and cell-free systems. Mutation Research. 1993;299:135–145. doi: 10.1016/0165-1218(93)90091-Q. [DOI] [PubMed] [Google Scholar]

[CR149] 149.Epe B., Pflaum M., Haring M., Hegler J., Rudiger H. Use of repair endonucleases to characterize DNA damage induced by reactive oxygen species in cellular and cell-free systems. Toxicol Lett. 1993;67:57–72. doi: 10.1016/0378-4274(93)90046-Z. [DOI] [PubMed] [Google Scholar]

[CR150] 150.Horai S., Hayasaka K. Intraspecific nucleotide sequence differences in the major noncoding region of human mitochondrial DNA. American Journal of Human Genetics. 1990;46:828–842. [PMC free article] [PubMed] [Google Scholar]

[CR151] 151.Crawford D.R., Wang Y., Schools G.P., Kochheiser J., Davies K.J. Down-regulation of mammalian mitochondrial RNAs during oxidative stress. Free Radic Biol Med. 1997;22(3):551–559. doi: 10.1016/S0891-5849(96)00380-2. [DOI] [PubMed] [Google Scholar]

[CR152] 152.Abramova N.E., Davies K.J.A., Crawford D.R. Polynucleotide degradation during early stage response to oxidative stress is specific to mitochondria. Free Radical Biology and Medicine. 2000;28(2):281–288. doi: 10.1016/S0891-5849(99)00239-7. [DOI] [PubMed] [Google Scholar]

[CR153] 153.Tang J.T., Yamazaki H., Inoue T., et al. Mitochondrial DNA influences radiation sensitivity and induction of apoptosis in human fibroblasts. Anticancer Research. 1999;19(6B):4959–4964. [PubMed] [Google Scholar]

[CR154] 154.Fung H., Kow Y.W., Van Houten B., et al. Asbestos increases mammalian AP-endonuclease gene expression, protein levels, and enzyme activity in mesothelial cells. Cancer Res. 1998;58(2):189–194. [PubMed] [Google Scholar]

[CR155] 155.Souza-Pinto N.C., Croteau D.L., Hudson E.K., Hansford R.G., Bohr V.A. Age-associated increase in 8-oxo-deoxyguanosine glycosylase/AP lyase activity in rat mitochondria. Nucleic Acids Research. 1999;27(8):1935–1942. doi: 10.1093/nar/27.8.1935. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR156] 156.Anderson C.T., Friedberg E.C. The presence of nuclear and mitochondrial uracil-DNA glycosylase in extracts of human KB cells. Nucleic Acids Research. 1980;8(4):875–888. [PMC free article] [PubMed] [Google Scholar]

[CR157] 157.Caradonna S., Ladner R., Hansbury M., Kosciuk M., Lynch F., Muller S. Affinity purification and comparative analysis of two distinct human uracil DNA glycosylases. Exp Cell Res. 1996;222(2):345–359. doi: 10.1006/excr.1996.0044. [DOI] [PubMed] [Google Scholar]

[CR158] 158.Nilsen H., Otterlei M., Haug T., et al. Nuclear and mitochondrial uracil-DNA glycosylases are generated by alternative splicing and transcription from different positions in the UNG gene. Nucleic Acids Research. 1997;25(4):750–755. doi: 10.1093/nar/25.4.750. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR159] 159.Tomkinson AE, Bonk RT, Linn S. Mitochondrial endonuclease activities specific for apurinic/apyrimidinic sites in DNA from mouse cells. Journal of Biological Chemistry. 1988;263(25):12532–12537. [PubMed]

[CR160] 160.Croteau DL, ap Rhys CM, Hudson EK, Dianov GL, Hansford RG, Bohr VA. An oxidative damage-specific endonuclease from rat liver mitochondria. J Biol Chem. 1997;272(43):27338–27344. [DOI] [PubMed]

[CR161] 161.Rosenquist T.A., Zharkov D.O., Grollman A.P. Cloning and characterization of a mammalian 8-oxoguanine DNA glycosylase. Proc Natl Acad Sci U S A. 1997;94(14):7429–7434. doi: 10.1073/pnas.94.14.7429. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR162] 162.Takao M., Aburatani H., Kobayashi K., Yasui A. Mitochondrial targeting of human DNA glycosylases for repair of oxidative DNA damage. Nucleic Acids Res. 1998;26(12):2917–2922. doi: 10.1093/nar/26.12.2917. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR163] 163.Vanderstraeten S, Van den Brule S, Hu J, Foury F. The role of 3′-5′ exonucleolytic proofreading and mismatch repair in yeast mitochondrial DNA error avoidance. J Biol Chem. 1998; 273(37):23690–23697. [DOI] [PubMed]

[CR164] 164.Pinz K.G., Bogenhagen D.F. Efficient repair of abasic sites in DNA by mitochondrial enzymes. Mol Cell Biol. 1998;18(3):1257–1265. doi: 10.1128/mcb.18.3.1257. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR165] 165.Reenan R.A., Kolodner R.D. Characterization of insertion mutations in the Saccharomyces cerevisiae MSH1 and MSH2 genes: evidence for separate mitochondrial and nuclear functions. Genetics. 1992;132:975–985. doi: 10.1093/genetics/132.4.975. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR166] 166.Shadel G.S., Clayton D.A. Mitochondrial DNA maintenance in vertebrates. Annu Rev Biochem. 1997;66:409–435. doi: 10.1146/annurev.biochem.66.1.409. [DOI] [PubMed] [Google Scholar]

[CR167] 167.Awadalla P., Eyre-Walker A., Smith J.M. Linkage disequilibrium and recombination in hominid mitochondrial DNA. Science. 1999;286(5449):2524–2525. doi: 10.1126/science.286.5449.2524. [DOI] [PubMed] [Google Scholar]

[CR168] 168.Hagelberg E., Goldman N., Lio P., et al. Evidence for mitochondrial DNA recombination in a human population of island Melanesia. Proc R Soc Lond B Biol Sci. 1999;266(1418):485–492. doi: 10.1098/rspb.1999.0663. [DOI] [PMC free article] [PubMed] [Google Scholar]

[CR169] 169.Ikeda S., Ozaki K. Action of mitochondrial endonuclease G on DNA damaged by L-ascorbic acid, peplomycin, and cis-diamminedichloroplatinum (II) Biochem Biophys Res Commun. 1997;235(2):291–294. doi: 10.1006/bbrc.1997.6786. [DOI] [PubMed] [Google Scholar]

[CR170] 170.Le X.C., Xing J.Z., Lee J., Leadon S.A., Weinfeld M. Inducible repair of thymine glycol detected by an ultrasensitive assay for DNA damage. Science. 1998;280(5366):1066–1069. doi: 10.1126/science.280.5366.1066. [DOI] [PubMed] [Google Scholar]

[CR171] 171.Ku H.H., Sohal R.S. Comparison of mitochondrial pro-oxidant generation and anti-oxidant defenses between rat and pigeon: possible basis of variation in longevity and metabolic potential. Mechanisms of Ageing and Development. 1993;72:67–76. doi: 10.1016/0047-6374(93)90132-B. [DOI] [PubMed] [Google Scholar]

[CR172] 172.Barja G., Cadenas S., Rojas C., Perez-Campo R., Lopez-Torres M. Low mitochondrial free radical production per unit O2 consumption can explain the simultaneous presence of high longevity and high aerobic metabolic rate in birds. Free Radic Res. 1994;21(5):317–327. doi: 10.3109/10715769409056584. [DOI] [PubMed] [Google Scholar]

[CR173] 173.Ogburn C.E., Austad S.N., Holmes D.J., et al. Cultured renal epithelial cells from birds and mice: Enhanced resistance of avian cells to oxidative stress and DNA damage. Journals of Gerontology Series A-Biological Sciences and Medical Sciences. 1998;53(4):B287–B292. doi: 10.1093/gerona/53a.4.b287. [DOI] [PubMed] [Google Scholar]

[CR174] 174.Herrero A., Barja G. 8-oxo-deoxyguanosine levels in heart and brain mitochondrial and nuclear DNA of two mammals and three birds in relation to their different rates of aging. Aging-Clinical And Experimental Research. 1999;11(5):294–300. doi: 10.1007/BF03339803. [DOI] [PubMed] [Google Scholar]

[CR175] 175.Barja G., Herrero A. Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. FASEB Journal. 2000;14(2):312–318. doi: 10.1096/fasebj.14.2.312. [DOI] [PubMed] [Google Scholar]

[CR176] 176.Williams MD, Van Remmen H, Conrad CC, Huang TT, Epstein CJ, Richardson A. Increased oxidative damage is correlated to altered mitochondrial function in heterozygous manganese superoxide dismutase knockout mice. J Biol Chem. 1998;273(43):28510–28515. [DOI] [PubMed]

PERMALINK

Mitochondria, oxidative DNA damage, and aging

R Michael Anson

Vilhelm A Bohr

Abstract

Full Text

Contributor Information

References

ACTIONS

PERMALINK

RESOURCES

Cite

Add to Collections

PERMALINK

Mitochondria, oxidative DNA damage, and aging

R Michael Anson

Vilhelm A Bohr

Abstract

Full Text

Contributor Information

References

ACTIONS

PERMALINK

RESOURCES

Similar articles

Cited by other articles

Links to NCBI Databases