Oxidative genome damage and its repair: Implications in aging and neurodegenerative diseases

Mechanisms of Ageing and Development

Volumn 133, Issue 4, 2012, Pages 157-168

  Hegde, Muralidhar L ^a   Mantha, Anil K ^a   Hazra, Tapas K ^a   Bhakat, Kishor K ^a   Mitra, Sankar ^a   Szczesny, Bartosz ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Aging; DNA base excision repair; DNA glycosylases; Neurodegenerative disorders; Protein protein and protein DNA interactions; Reactive oxygen species; Single strand break repair

Indexed keywords

DNA (APURINIC OR APYRIMIDINIC SITE) LYASE; DNA DIRECTED DNA POLYMERASE BETA; DNA GLYCOSYLTRANSFERASE; DNA POLYMERASE; PROTEIN KINASE C; RNA POLYMERASE II; Y BOX BINDING PROTEIN 1;

AGING; ALKYLATION; ARTICLE; CELL SURVIVAL; DEGENERATIVE DISEASE; DNA REPLICATION; ENDOPLASMIC RETICULUM; ENZYME SPECIFICITY; HOMOLOGOUS RECOMBINATION; HUMAN; MITOCHONDRIAL GENOME; NITROSATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DNA INTERACTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEIN TARGETING; SEQUENCE HOMOLOGY; SINGLE STRANDED DNA BREAK; UBIQUITINATION;

AGE FACTORS; AGING; ANIMALS; CENTRAL NERVOUS SYSTEM; DNA BREAKS, SINGLE-STRANDED; DNA DAMAGE; DNA GLYCOSYLASES; DNA REPAIR; DNA, MITOCHONDRIAL; DNA-(APURINIC OR APYRIMIDINIC SITE) LYASE; HUMANS; NEURODEGENERATIVE DISEASES; OXIDATIVE STRESS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); REACTIVE OXYGEN SPECIES;

MAMMALIA;

EID: 84860704002     PISSN: 00476374     EISSN: 18726216     Source Type: Journal    
DOI: 10.1016/j.mad.2012.01.005     Document Type: Article

References (168)

1. Acevedo-Torres K., Berrios L., Rosario N., Dufault V., Skatchkov S., Eaton M.J., Torres-Ramos C.A., Ayala-Torres S. Mitochondrial DNA damage is a hallmark of chemically induced and the R6/2 transgenic model of Huntington's disease. DNA Repair (Amst.) 2009, 8:126-136.
2. Adlam V.J., Harrison J.C., Porteous C.M., James A.M., Smith R.A., Murphy M.P., Sammut I.A. Targeting an antioxidant to mitochondria decreases cardiac ischemia-reperfusion injury. FASEB J. 2005, 19:1088-1095.
3. Aguirre N., Beal M.F., Matson W.R., Bogdanov M.B. Increased oxidative damage to DNA in an animal model of amyotrophic lateral sclerosis. Free Radic. Res. 2005, 39:383-388.
4. Ahel I., Rass U., El-Khamisy S.F., Katyal S., Clements P.M., McKinnon P.J., Caldecott K.W., West S.C. The neurodegenerative disease protein aprataxin resolves abortive DNA ligation intermediates. Nature 2006, 443:713-716.
5. Akbari M., Visnes T., Krokan H.E., Otterlei M. Mitochondrial base excision repair of uracil and AP sites takes place by single-nucleotide insertion and long-patch DNA synthesis. DNA Repair (Amst.) 2008, 7:605-616.
6. Alam Z.I., Jenner A., Daniel S.E., Lees A.J., Cairns N., Marsden C.D., Jenner P., Halliwell B. Oxidative DNA damage in the parkinsonian brain: an apparent selective increase in 8-hydroxyguanine levels in substantia nigra. J. Neurochem. 1997, 69:1196-1203.
7. Anderson C.T., Friedberg E.C. The presence of nuclear and mitochondrial uracil-DNA glycosylase in extracts of human KB cells. Nucleic Acids Res. 1980, 8:875-888.
8. Anderson S., Bankier A.T., Barrell B.G., de Bruijn M.H., Coulson A.R., Drouin J., Eperon I.C., Nierlich D.P., Roe B.A., Sanger F., Schreier P.H., Smith A.J., Staden R., Young I.G. Sequence and organization of the human mitochondrial genome. Nature 1981, 290:457-465.
9. Arai T., Kelly V.P., Minowa O., Noda T., Nishimura S. High accumulation of oxidative DNA damage, 8-hydroxyguanine, in Mmh/Ogg1 deficient mice by chronic oxidative stress. Carcinogenesis 2002, 23:2005-2010.
10. Bandaru V., Sunkara S., Wallace S.S., Bond J.P. A novel human DNA glycosylase that removes oxidative DNA damage and is homologous to Escherichia coli endonuclease VIII. DNA Repair (Amst.) 2002, 1:517-529.
11. Banerjee, D., Mandal, S.M., Das, A., Hegde, M.L., Das, S., Bhakat, K.K., Boldogh, I., Sarkar, P.S., Mitra, S., Hazra, T.K. Preferential repair of oxidized base damage in the transcribed genes of mammalian cells. J. Biol. Chem., in press.
12. Berneburg M., Kamenisch Y., Krutmann J., Rocken M. 'To repair or not to repair - no longer a question': repair of mitochondrial DNA shielding against age and cancer. Exp. Dermatol. 2006, 15:1005-1015.
13. Bhakat K.K., Hazra T.K., Mitra S. Acetylation of the human DNA glycosylase NEIL2 and inhibition of its activity. Nucleic Acids Res. 2004, 32:3033-3039.
14. Bhakat K.K., Mantha A.K., Mitra S. Transcriptional regulatory functions of mammalian AP-endonuclease (APE1/Ref-1), an essential multifunctional protein. Antioxid. Redox Signal. 2009, 11:621-638.
15. Bhakat K.K., Mokkapati S.K., Boldogh I., Hazra T.K., Mitra S. Acetylation of human 8-oxoguanine-DNA glycosylase by p300 and its role in 8-oxoguanine repair in vivo. Mol. Cell. Biol. 2006, 26:1654-1665.
16. Bhattacharyya A., Chattopadhyay R., Burnette B.R., Cross J.V., Mitra S., Ernst P.B., Bhakat K.K., Crowe S.E. Acetylation of apurinic/apyrimidinic endonuclease-1 regulates Helicobacter pylori-mediated gastric epithelial cell apoptosis. Gastroenterology 2009, 136:2258-2269.
17. Bogdanov M., Brown R.H., Matson W., Smart R., Hayden D., O'Donnell H., Flint Beal M., Cudkowicz M. Increased oxidative damage to DNA in ALS patients. Free Radic. Biol. Med. 2000, 29:652-658.
18. Bohr V.A. Repair of oxidative DNA damage in nuclear and mitochondrial DNA, and some changes with aging in mammalian cells. Free Radic. Biol. Med. 2002, 32:804-812.
19. Bohr V.A., Ottersen O.P., Tonjum T. Genome instability and DNA repair in brain, ageing and neurological disease. Neuroscience 2007, 145:1183-1186.
20. Bolden A., Noy G.P., Weissbach A. DNA polymerase of mitochondria is a gamma-polymerase. J. Biol. Chem. 1977, 252:3351-3356.
21. Busso C.S., Iwakuma T., Izumi T. Ubiquitination of mammalian AP endonuclease (APE1) regulated by the p53-MDM2 signaling pathway. Oncogene 2009, 28:1616-1625.
22. Cadenas E., Davies K.J. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic. Biol. Med. 2000, 29:222-230.
23. Caldecott K.W. Mammalian single-strand break repair: mechanisms and links with chromatin. DNA Repair (Amst.) 2007, 6:443-453.
24. Caldecott K.W. Single-strand break repair and genetic disease. Nat. Rev. Genet. 2008, 9:619-631.
25. Caldecott K.W., McKeown C.K., Tucker J.D., Ljungquist S., Thompson L.H. An interaction between the mammalian DNA repair protein XRCC1 and DNA ligase III. Mol. Cell. Biol. 1994, 14:68-76.
26. Chattopadhyay R., Das S., Maiti A.K., Boldogh I., Xie J., Hazra T.K., Kohno K., Mitra S., Bhakat K.K. Regulatory role of human AP-endonuclease (APE1/Ref-1) in YB-1-mediated activation of the multidrug resistance gene MDR1. Mol. Cell. Biol. 2008, 28:7066-7080.
27. Chattopadhyay R., Wiederhold L., Szczesny B., Boldogh I., Hazra T.K., Izumi T., Mitra S. Identification and characterization of mitochondrial abasic (AP)-endonuclease in mammalian cells. Nucleic Acids Res. 2006, 34:2067-2076.
28. Chen D., Cao G., Hastings T., Feng Y., Pei W., O'Horo C., Chen J. Age-dependent decline of DNA repair activity for oxidative lesions in rat brain mitochondria. J. Neurochem. 2002, 81:1273-1284.
29. Clayton D.A., Doda J.N., Friedberg E.C. The absence of a pyrimidine dimer repair mechanism in mammalian mitochondria. Proc. Natl. Acad. Sci. U.S.A. 1974, 71:2777-2781.
30. Cooke M.S., Evans M.D., Dizdaroglu M., Lunec J. Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J. 2003, 17:1195-1214.
31. Coppede F., Ceravolo R., Migheli F., Fanucchi F., Frosini D., Siciliano G., Bonuccelli U., Migliore L. The hOGG1 Ser326Cys polymorphism is not associated with sporadic Parkinson's disease. Neurosci. Lett. 2010, 473:248-251.
32. Coppede F., Mancuso M., Lo Gerfo A., Carlesi C., Piazza S., Rocchi A., Petrozzi L., Nesti C., Micheli D., Bacci A., Migliore L., Murri L., Siciliano G. Association of the hOGG1 Ser326Cys polymorphism with sporadic amyotrophic lateral sclerosis. Neurosci. Lett. 2007, 420:163-168.
33. Coppede F., Mancuso M., Lo Gerfo A., Manca M.L., Petrozzi L., Migliore L., Siciliano G., Murri L. A Ser326Cys polymorphism in the DNA repair gene hOGG1 is not associated with sporadic Alzheimer's disease. Neurosci. Lett. 2007, 414:282-285.
34. Coppede F., Migheli F., Lo Gerfo A., Fabbrizi M.R., Carlesi C., Mancuso M., Corti S., Mezzina N., del Bo R., Comi G.P., Siciliano G., Migliore L. Association study between XRCC1 gene polymorphisms and sporadic amyotrophic lateral sclerosis. Amyotroph. Lateral Scler. 2010, 11:122-124.
35. Coppede F., Migliore L. DNA damage and repair in Alzheimer's disease. Curr. Alzheimer Res. 2009, 6:36-47.
36. Croteau D.L., Bohr V.A. Repair of oxidative damage to nuclear and mitochondrial DNA in mammalian cells. J. Biol. Chem. 1997, 272:25409-25412.
37. Cymerman I.A., Chung I., Beckmann B.M., Bujnicki J.M., Meiss G. EXOG, a novel paralog of Endonuclease G in higher eukaryotes. Nucleic Acids Res. 2008, 36:1369-1379.
38. Das A., Boldogh I., Lee J.W., Harrigan J.A., Hegde M.L., Piotrowski J., de Souza Pinto N., Ramos W., Greenberg M.M., Hazra T.K., Mitra S., Bohr V.A. The human Werner syndrome protein stimulates repair of oxidative DNA base damage by the DNA glycosylase NEIL1. J. Biol. Chem. 2007, 282:26591-26602.
39. Das B.B., Dexheimer T.S., Maddali K., Pommier Y. Role of tyrosyl-DNA phosphodiesterase (TDP1) in mitochondria. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:19790-19795.
40. Das S., Chattopadhyay R., Bhakat K.K., Boldogh I., Kohno K., Prasad R., Wilson S.H., Hazra T.K. Stimulation of NEIL2-mediated oxidized base excision repair via YB-1 interaction during oxidative stress. J. Biol. Chem. 2007, 282:28474-28484.
41. Davydov V., Hansen L.A., Shackelford D.A. Is DNA repair compromised in Alzheimer's disease?. Neurobiol. Aging 2003, 24:953-968.
42. Dawson T.L., Gores G.J., Nieminen A.L., Herman B., Lemasters J.J. Mitochondria as a source of reactive oxygen species during reductive stress in rat hepatocytes. Am. J. Physiol. 1993, 264:C961-C967.
43. De Boeck M., Lison D., Kirsch-Volders M. Evaluation of the in vitro direct and indirect genotoxic effects of cobalt compounds using the alkaline comet assay. Influence of interdonor and interexperimental variability. Carcinogenesis 1998, 19:2021-2029.
44. de Souza-Pinto N.C., Mason P.A., Hashiguchi K., Weissman L., Tian J., Guay D., Lebel M., Stevnsner T.V., Rasmussen L.J., Bohr V.A. Novel DNA mismatch-repair activity involving YB-1 in human mitochondria. DNA Repair (Amst.) 2009, 8:704-719.
45. Dizdaroglu M., Jaruga P., Birincioglu M., Rodriguez H. Free radical-induced damage to DNA: mechanisms and measurement. Free Radic. Biol. Med. 2002, 32:1102-1115.
46. Dogru-Abbasoglu S., Aykac-Toker G., Hanagasi H.A., Gurvit H., Emre M., Uysal M. The Arg194Trp polymorphism in DNA repair gene XRCC1 and the risk for sporadic late-onset Alzheimer's disease. Neurol. Sci. 2007, 28:31-34.
47. Dorszewska J., Florczak J., Rozycka A., Kempisty B., Jaroszewska-Kolecka J., Chojnacka K., Trzeciak W.H., Kozubski W. Oxidative DNA damage and level of thiols as related to polymorphisms of MTHFR, MTR, MTHFD1 in Alzheimer's and Parkinson's diseases. Acta. Neurobiol. Exp. (Wars.) 2007, 67:113-129.
48. Dou H., Mitra S., Hazra T.K. Repair of oxidized bases in DNA bubble structures by human DNA glycosylases NEIL1 and NEIL2. J. Biol. Chem. 2003, 278:49679-49684.
49. Dou H., Theriot C.A., Das A., Hegde M.L., Matsumoto Y., Boldogh I., Hazra T.K., Bhakat K.K., Mitra S. Interaction of the human DNA glycosylase NEIL1 with proliferating cell nuclear antigen. The potential for replication-associated repair of oxidized bases in mammalian genomes. J. Biol. Chem. 2008, 283:3130-3140.
50. Doublie S., Bandaru V., Bond J.P., Wallace S.S. The crystal structure of human endonuclease VIII-like 1 (NEIL1) reveals a zincless finger motif required for glycosylase activity. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:10284-10289.
51. Driggers W.J., LeDoux S.P., Wilson G.L. Repair of oxidative damage within the mitochondrial DNA of RINr 38 cells. J. Biol. Chem. 1993, 268:22042-22045.
52. Duxin J.P., Dao B., Martinsson P., Rajala N., Guittat L., Campbell J.L., Spelbrink J.N., Stewart S.A. Human Dna2 is a nuclear and mitochondrial DNA maintenance protein. Mol. Cell. Biol. 2009, 29:4274-4282.
53. Edwards M., Rassin D.K., Izumi T., Mitra S., Perez-Polo J.R. APE/Ref-1 responses to oxidative stress in aged rats. J. Neurosci. Res. 1998, 54:635-638.
54. El-Khamisy S.F., Hartsuiker E., Caldecott K.W. TDP1 facilitates repair of ionizing radiation-induced DNA single-strand breaks. DNA Repair (Amst.) 2007, 6:1485-1495.
55. El-Khamisy S.F., Saifi G.M., Weinfeld M., Johansson F., Helleday T., Lupski J.R., Caldecott K.W. Defective DNA single-strand break repair in spinocerebellar ataxia with axonal neuropathy-1. Nature 2005, 434:108-113.
56. Ellenberger T., Tomkinson A.E. Eukaryotic DNA ligases: structural and functional insights. Annu. Rev. Biochem. 2008, 77:313-338.
57. Englander E.W., Hu Z., Sharma A., Lee H.M., Wu Z.H., Greeley G.H. Rat MYH, a glycosylase for repair of oxidatively damaged DNA, has brain-specific isoforms that localize to neuronal mitochondria. J. Neurochem. 2002, 83:1471-1480.
58. Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., Ellenberger T. DNA Repair and Mutagenesis 2006, ASM Press, Washington. 2nd edition.
59. Fritz G., Kaina B. Phosphorylation of the DNA repair protein APE/REF-1 by CKII affects redox regulation of AP-1. Oncogene 1999, 18:1033-1040.
60. Gao Y., Katyal S., Lee Y., Zhao J., Rehg J.E., Russell H.R., McKinnon P.J. DNA ligase III is critical for mtDNA integrity but not Xrcc1-mediated nuclear DNA repair. Nature 2011, 471:240-244.
61. Graziewicz M.A., Longley M.J., Copeland W.C. DNA polymerase gamma in mitochondrial DNA replication and repair. Chem. Rev. 2006, 106:383-405.
62. Gredilla R., Garm C., Holm R., Bohr V.A., Stevnsner T. Differential age-related changes in mitochondrial DNA repair activities in mouse brain regions. Neurobiol. Aging 2010, 31:993-1002.
63. Greenberg M.M., Weledji Y.N., Kim J., Bales B.C. Repair of oxidized abasic sites by exonuclease III, endonuclease IV, and endonuclease III. Biochemistry 2004, 43:8178-8183.
64. Gu H., Marth J.D., Orban P.C., Mossmann H., Rajewsky K. Deletion of a DNA polymerase beta gene segment in T cells using cell type-specific gene targeting. Science 1994, 265:103-106.
65. Guzder S.N., Torres-Ramos C., Johnson R.E., Haracska L., Prakash L., Prakash S. Requirement of yeast Rad1-Rad10 nuclease for the removal of 3'-blocked termini from DNA strand breaks induced by reactive oxygen species. Genes Dev. 2004, 18:2283-2291.
66. Hanawalt P.C. Emerging links between premature ageing and defective DNA repair. Mech. Ageing Dev. 2008, 129:503-505.
67. Hanssen-Bauer A., Solvang-Garten K., Sundheim O., Pena-Diaz J., Andersen S., Slupphaug G., Krokan H.E., Wilson D.M., Akbari M., Otterlei M. XRCC1 coordinates disparate responses and multiprotein repair complexes depending on the nature and context of the DNA damage. Environ. Mol. Mutagen. 2011, 52:623-635.
68. Hayward C., Colville S., Swingler R.J., Brock D.J. Molecular genetic analysis of the APEX nuclease gene in amyotrophic lateral sclerosis. Neurology 1999, 52:1899-1901.
69. Hazra T.K., Izumi T., Boldogh I., Imhoff B., Kow Y.W., Jaruga P., Dizdaroglu M., 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. 2002, 99:3523-3528.
70. Hazra T.K., Izumi T., Maidt L., Floyd R.A., Mitra S. The presence of two distinct 8-oxoguanine repair enzymes in human cells: their potential complementary roles in preventing mutation. Nucleic Acids Res. 1998, 26:5116-5122.
71. Hazra T.K., Kow Y.W., Hatahet Z., Imhoff B., Boldogh I., Mokkapati S.K., Mitra S., Izumi T. Identification and characterization of a novel human DNA glycosylase for repair of cytosine-derived lesions. J. Biol. Chem. 2002, 277:30417-30420.
72. Hegde M.L., Bharathi P., Suram A., Venugopal C., Jagannathan R., Poddar P., Srinivas P., Sambamurti K., Rao K.J., Scancar J., Messori L., Zecca L., Zatta P. Challenges associated with metal chelation therapy in Alzheimer's disease. J. Alzheimers Dis. 2009, 17:457-468.
73. Hegde M.L., Hazra T.K., Mitra S. Early steps in the DNA base excision/single-strand interruption repair pathway in mammalian cells. Cell Res. 2008, 18:27-47.
74. Hegde M.L., Hazra T.K., Mitra S. Functions of disordered regions in mammalian early base excision repair proteins. Cell. Mol. Life Sci. 2010, 67:3573-3587.
75. Hegde M.L., Hegde P.M., Holthauzen L.M., Hazra T.K., Rao K.S., Mitra S. Specific inhibition of NEIL-initiated repair of oxidized base damage in human genome by copper and iron: potential etiological linkage to neurodegenerative diseases. J. Biol. Chem. 2010, 285:28812-28825.
76. Hegde, M.L., Hegde, P.M., Jagannatha Rao, K.S., Mitra, S. Oxidative genome damage and its repair in neurodegenerative diseases: function of transition metals as a double-edged sword. J. Alzheimers Dis., in press.
77. Hegde M.L., Shanmugavelu P., Vengamma B., Rao T.S., Menon R.B., Rao R.V., Rao K.S. Serum trace element levels and the complexity of inter-element relations in patients with Parkinson's disease. J. Trace Elem. Med. Biol. 2004, 18:163-171.
78. Hegde M.L., Theriot C.A., Das A., Hegde P.M., Guo Z., Gary R.K., Hazra T.K., Shen B., Mitra S. Physical and functional interaction between human oxidized base-specific DNA glycosylase NEIL1 and flap endonuclease 1. J. Biol. Chem. 2008, 283:27028-27037.
79. Hirano R., Interthal H., Huang C., Nakamura T., Deguchi K., Choi K., Bhattacharjee M.B., Arimura K., Umehara F., Izumo S., Northrop J.L., Salih M.A., Inoue K., Armstrong D.L., Champoux J.J., Takashima H., Boerkoel C.F. Spinocerebellar ataxia with axonal neuropathy: consequence of a Tdp1 recessive neomorphic mutation?. EMBO J. 2007, 26:4732-4743.
80. Hoeijmakers J.H. DNA damage, aging, and cancer. N. Engl. J. Med. 2009, 361:1475-1485.
81. Hsieh M.M., Hegde V., Kelley M.R., Deutsch W.A. Activation of APE/Ref-1 redox activity is mediated by reactive oxygen species and PKC phosphorylation. Nucleic Acids Res. 2001, 29:3116-3122.
82. Huang E., Qu D., Zhang Y., Venderova K., Haque M.E., Rousseaux M.W., Slack R.S., Woulfe J.M., Park D.S. The role of Cdk5-mediated apurinic/apyrimidinic endonuclease 1 phosphorylation in neuronal death. Nat. Cell Biol. 2010, 12:563-571.
83. Hubscher U., Kuenzle C.C., Spadari S. Functional roles of DNA polymerases beta and gamma. Proc. Natl. Acad. Sci. U.S.A. 1979, 76:2316-2320.
84. Ikeda S., Biswas T., Roy R., Izumi T., Boldogh I., Kurosky A., Sarker A.H., Seki S., Mitra S. Purification and characterization of human NTH1, a homolog of Escherichia coli endonuclease III. Direct identification of Lys-212 as the active nucleophilic residue. J. Biol. Chem. 1998, 273:21585-21593.
85. Izumi T., Wiederhold L.R., Roy G., Roy R., Jaiswal A., Bhakat K.K., Mitra S., Hazra T.K. Mammalian DNA base excision repair proteins: their interactions and role in repair of oxidative DNA damage. Toxicology 2003, 193:43-65.
86. Kakkar P., Singh B.K. Mitochondria: a hub of redox activities and cellular distress control. Mol. Cell. Biochem. 2007, 305:235-253.
87. Katyal S., McKinnon P.J. DNA strand breaks, neurodegeneration and aging in the brain. Mech. Ageing Dev. 2008, 129:483-491.
88. Kavli B., Sundheim O., Akbari M., Otterlei M., Nilsen H., Skorpen F., Aas P.A., Hagen L., Krokan H.E., Slupphaug G. hUNG2 is the major repair enzyme for removal of uracil from U:A matches, U:G mismatches, and U in single-stranded DNA, with hSMUG1 as a broad specificity backup. J. Biol. Chem. 2002, 277:39926-39936.
89. Kieper J., Lauber C., Gimadutdinow O., Urbanska A., Cymerman I., Ghosh M., Szczesny B., Meiss G. Production and characterization of recombinant protein preparations of Endonuclease G-homologs from yeast, C. elegans and humans. Protein Expr. Purif. 2010, 73:99-106.
90. Klungland A., Rosewell I., Hollenbach S., Larsen E., Daly G., Epe B., Seeberg E., Lindahl T., Barnes D.E. Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:13300-13305.
91. Krishnamurthy N., Zhao X., Burrows C.J., David S.S. Superior removal of hydantoin lesions relative to other oxidized bases by the human DNA glycosylase hNEIL1. Biochemistry 2008, 47:7137-7146.
92. Lakshmipathy U., Campbell C. The human DNA ligase III gene encodes nuclear and mitochondrial proteins. Mol. Cell. Biol. 1999, 19:3869-3876.
93. Lakshmipathy U., Campbell C. Mitochondrial DNA ligase III function is independent of Xrcc1. Nucleic Acids Res. 2000, 28:3880-3886.
94. Larsen N.B., Rasmussen M., Rasmussen L.J. Nuclear and mitochondrial DNA repair: similar pathways?. Mitochondrion 2005, 5:89-108.
95. 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.
96. Lemon J.A., Boreham D.R., Rollo C.D. A dietary supplement abolishes age-related cognitive decline in transgenic mice expressing elevated free radical processes. Exp. Biol. Med. 2003, 228:800-810.
97. Li H., Swiercz R., Englander E.W. Elevated metals compromise repair of oxidative DNA damage via the base excision repair pathway: implications of pathologic iron overload in the brain on integrity of neuronal DNA. J. Neurochem. 2009, 110:1774-1783.
98. Lindahl T. Instability and decay of the primary structure of DNA. Nature 1993, 362:709-715.
99. Liu J., Head E., Gharib A.M., Yuan W., Ingersoll R.T., Hagen T.M., Cotman C.W., Ames B.N. Memory loss in old rats is associated with brain mitochondrial decay and RNA/DNA oxidation: partial reversal by feeding acetyl-l-carnitine and/or R-alpha-lipoic acid. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:2356-2361.
100. Liu M., Bandaru V., Bond J.P., Jaruga P., Zhao X., Christov P.P., Burrows C.J., Rizzo C.J., Dizdaroglu M., Wallace S.S. The mouse ortholog of NEIL3 is a functional DNA glycosylase in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:4925-4930.
101. Liu P., Qian L., Sung J.S., de Souza-Pinto N.C., Zheng L., Bogenhagen D.F., Bohr V.A., Wilson D.M., Shen B., Demple B. Removal of oxidative DNA damage via FEN1-dependent long-patch base excision repair in human cell mitochondria. Mol. Cell. Biol. 2008, 28:4975-4987.
102. Liu P., Qian L., Sung J.S., de Souza-Pinto N.C., Zheng L., Bogenhagen D.F., Bohr V.A., Wilson D.M., Shen B., Demple B. Removal of oxidative DNA damage via FEN1-dependent long-patch base excision repair in human cell mitochondria. Mol. Cell. Biol. 2008.
103. Liu P.K., Hsu C.Y., Dizdaroglu M., Floyd R.A., Kow Y.W., Karakaya A., Rabow L.E., Cui J.K. Damage, repair, and mutagenesis in nuclear genes after mouse forebrain ischemia-reperfusion. J. Neurosci. 1996, 16:6795-6806.
104. Liu X., Roy R. Truncation of amino-terminal tail stimulates activity of human endonuclease III (hNTH1). J. Mol. Biol. 2002, 321:265-276.
105. Liu Y., Kao H.I., Bambara R.A. Flap endonuclease 1: a central component of DNA metabolism. Annu. Rev. Biochem. 2004, 73:589-615.
106. Longley M.J., Ropp P.A., Lim S.E., Copeland W.C. Characterization of the native and recombinant catalytic subunit of human DNA polymerase gamma: identification of residues critical for exonuclease activity and dideoxynucleotide sensitivity. Biochemistry (Mosc.) 1998, 37:10529-10539.
107. Lu A.L., Chang D.Y. Repair of single base-pair transversion mismatches of Escherichia coli in vitro: correction of certain A/G mismatches is independent of dam methylation and host mutHLS gene functions. Genetics 1988, 118:593-600.
108. Lu T., Pan Y., Kao S.Y., Li C., Kohane I., Chan J., Yankner B.A. Gene regulation and DNA damage in the ageing human brain. Nature 2004, 429:883-891.
109. Lynn S., Lai H.T., Kao S.M., Lai J., Jan K.Y. Cadmium inhibits DNA strand break rejoining in methyl methanesulfonate-treated CHO-K1 cells. Toxicol. Appl. Pharmacol. 1997, 144:171-176.
110. Lyras L., Cairns N.J., Jenner A., Jenner P., Halliwell B. An assessment of oxidative damage to proteins, lipids, and DNA in brain from patients with Alzheimer's disease. J. Neurochem. 1997, 68:2061-2069.
111. Mason P.A., Matheson E.C., Hall A.G., Lightowlers R.N. Mismatch repair activity in mammalian mitochondria. Nucleic Acids Res. 2003, 31:1052-1058.
112. McCullough A.K., Dodson M.L., Lloyd R.S. Initiation of base excision repair: glycosylase mechanisms and structures. Annu. Rev. Biochem. 1999, 68:255-285.
113. McNeill D.R., Narayana A., Wong H.K., Wilson D.M. Inhibition of Ape1 nuclease activity by lead, iron, and cadmium. Environ. Health Perspect. 2004, 112:799-804.
114. Michaels M.L., 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. 1992, 174:6321-6325.
115. Miller F.J., Rosenfeldt F.L., Zhang C., Linnane A.W., Nagley P. Precise determination of mitochondrial DNA copy number in human skeletal and cardiac muscle by a PCR-based assay: lack of change of copy number with age. Nucleic Acids Res. 2003, 31:e61.
116. Minowa O., Arai T., Hirano M., Monden Y., Nakai S., Fukuda M., Itoh M., Takano H., Hippou Y., Aburatani H., Masumura K., Nohmi T., Nishimura S., Noda T. Mmh/Ogg1 gene inactivation results in accumulation of 8-hydroxyguanine in mice. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:4156-4161.
117. Mitra S., Boldogh I., Izumi T., Hazra T.K. Complexities of the DNA base excision repair pathway for repair of oxidative DNA damage. Environ. Mol. Mutagen. 2001, 38:180-190.
118. Mitra S., Hegde M.L., Theriot C.A., Das A., Hegde P.M., Hazra T.K. Complexity in repair of oxidative genome damage and its regulation. Proceedings of Princess Takamatsu Symposium 2009.
119. Mostoslavsky R., Chua K.F., Lombard D.B., Pang W.W., Fischer M.R., Gellon L., Liu P., Mostoslavsky G., Franco S., Murphy M.M., Mills K.D., Patel P., Hsu J.T., Hong A.L., Ford E., Cheng H.L., Kennedy C., Nunez N., Bronson R., Frendewey D., Auerbach W., Valenzuela D., Karow M., Hottiger M.O., Hursting S., Barrett J.C., Guarente L., Mulligan R., Demple B., Yancopoulos G.D., Alt F.W. Genomic instability and aging-like phenotype in the absence of mammalian SIRT6. Cell 2006, 124:315-329.
120. Nishioka K., Ohtsubo T., Oda H., Fujiwara T., Kang D., Sugimachi K., 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 1999, 10:1637-1652.
121. Nouspikel T., Hanawalt P.C. DNA repair in terminally differentiated cells. DNA Repair (Amst.) 2002, 1:59-75.
122. Osterod M., Hollenbach S., Hengstler J.G., Barnes D.E., Lindahl T., Epe B. Age-related and tissue-specific accumulation of oxidative DNA base damage in 7,8-dihydro-8-oxoguanine-DNA glycosylase (Ogg1) deficient mice. Carcinogenesis 2001, 22:1459-1463.
123. Otterlei M., Warbrick E., Nagelhus T.A., Haug T., Slupphaug G., Akbari M., Aas P.A., Steinsbekk K., Bakke O., Krokan H.E. Post-replicative base excision repair in replication foci. EMBO J. 1999, 18:3834-3844.
124. Parker J.B., Bianchet M.A., Krosky D.J., Friedman J.I., Amzel L.M., Stivers J.T. Enzymatic capture of an extrahelical thymine in the search for uracil in DNA. Nature 2007, 449:433-437.
125. Parlanti E., Locatelli G., Maga G., Dogliotti E. Human base excision repair complex is physically associated to DNA replication and cell cycle regulatory proteins. Nucleic Acids Res. 2007, 35:1569-1577.
126. Paulson H.L., Miller V.M. Breaks in coordination: DNA repair in inherited ataxia. Neuron 2005, 46:845-848.
127. Pesole G., Gissi C., De Chirico A., Saccone C. Nucleotide substitution rate of mammalian mitochondrial genomes. J. Mol. Evol. 1999, 48:427-434.
128. Polidori M.C., Mecocci P., Browne S.E., Senin U., Beal M.F. Oxidative damage to mitochondrial DNA in Huntington's disease parietal cortex. Neurosci. Lett. 1999, 272:53-56.
129. Pouliot J.J., Yao K.C., Robertson C.A., Nash H.A. Yeast gene for a Tyr-DNA phosphodiesterase that repairs topoisomerase I complexes. Science 1999, 286:552-555.
130. Prasad R., Dianov G.L., Bohr V.A., Wilson S.H. FEN1 stimulation of DNA polymerase beta mediates an excision step in mammalian long patch base excision repair. J. Biol. Chem. 2000, 275:4460-4466.
131. Qian Y., Chen W., Wu J., Tao T., Bi L., Xu W., Qi H., Wang Y., Guo L. Association of polymorphism of DNA repair gene XRCC1 with sporadic late-onset Alzheimer's disease and age of onset in elderly Han Chinese. J. Neurol. Sci. 2010, 295:62-65.
132. Quach N., Chan T., Lu T.A., Schreiber S.S., Tan Z. Induction of DNA repair proteins, Ref-1 and XRCC1, in adult rat brain following kainic acid-induced seizures. Brain Res. 2005, 1042:236-240.
133. Rao K.S., Annapurna V.V., Raji N.S. DNA polymerase-beta may be the main player for defective DNA repair in aging rat neurons. Ann. N.Y. Acad. Sci. 2001, 928:113-120.
134. Rao K.S.J., Rao R.V., Shanmugavelu P., Menon R.B. Trace elements in Alzheimer's disease brain: a new hypothesis. Alzheimers Rep. 1999, 2:241-246.
135. Rass U., Ahel I., West S.C. Defective DNA repair and neurodegenerative disease. Cell 2007, 130:991-1004.
136. Sage J.M., Gildemeister O.S., Knight K.L. Discovery of a novel function for human Rad51: maintenance of the mitochondrial genome. J. Biol. Chem. 2010, 285:18984-18990.
137. Sarker A.H., Ikeda S., Nakano H., Terato H., Ide H., Imai K., Akiyama K., Tsutsui K., Bo Z., Kubo K., Yamamoto K., Yasui A., Yoshida M.C., Seki S. Cloning and characterization of a mouse homologue (mNthl1) of Escherichia coli endonuclease III. J. Mol. Biol. 1998, 282:761-774.
138. Seet B.T., Dikic I., Zhou M.M., Pawson T. Reading protein modifications with interaction domains. Nat. Rev. Mol. Cell Biol. 2006, 7:473-483.
139. Sengupta S., Mantha A.K., Mitra S., Bhakat K.K. Human AP endonuclease (APE1/Ref-1) and its acetylation regulate YB-1-p300 recruitment and RNA polymerase II loading in the drug-induced activation of multidrug resistance gene MDR1. Oncogene 2010, 30:482-493.
140. Shen J., Gilmore E.C., Marshall C.A., Haddadin M., Reynolds J.J., Eyaid W., Bodell A., Barry B., Gleason D., Allen K., Ganesh V.S., Chang B.S., Grix A., Hill R.S., Topcu M., Caldecott K.W., Barkovich A.J., Walsh C.A. Mutations in PNKP cause microcephaly, seizures and defects in DNA repair. Nat. Genet. 2010, 42:245-249.
141. 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.
142. Simsek D., Furda A., Gao Y., Artus J., Brunet E., Hadjantonakis A.K., Van Houten B., Shuman S., McKinnon P.J., Jasin M. Crucial role for DNA ligase III in mitochondria but not in Xrcc1-dependent repair. Nature 2011, 471:245-248.
143. Slupphaug G., Mol C.D., Kavli B., Arvai A.S., Krokan H.E., Tainer J.A. A nucleotide-flipping mechanism from the structure of human uracil-DNA glycosylase bound to DNA. Nature 1996, 384:87-92.
144. Sobol R.W., Prasad R., Evenski A., Baker A., Yang X.P., Horton J.K., Wilson S.H. The lyase activity of the DNA repair protein beta-polymerase protects from DNA-damage-induced cytotoxicity. Nature 2000, 405:807-810.
145. Stierum R.H., Croteau D.L., Bohr V.A. Purification and characterization of a mitochondrial thymine glycol endonuclease from rat liver. J. Biol. Chem. 1999, 274:7128-7136.
146. Stierum R.H., Dianov G.L., Bohr V.A. Single-nucleotide patch base excision repair of uracil in DNA by mitochondrial protein extracts. Nucleic Acids Res. 1999, 27:3712-3719.
147. Sykora P., Croteau D.L., Bohr V.A., Wilson D.M. Aprataxin localizes to mitochondria and preserves mitochondrial function. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:7437-7442.
148. Szczesny B., Mitra S. Effect of aging on intracellular distribution of abasic (AP) endonuclease 1 in the mouse liver. Mech. Ageing Dev. 2005, 126:1071-1078.
149. Szczesny B., Tann A.W., Longley M.J., Copeland W.C., Mitra S. Long patch base excision repair in mammalian mitochondrial genomes. J. Biol. Chem. 2008, 283:26349-26356.
150. Takao M., Aburatani H., Kobayashi K., Yasui A. Mitochondrial targeting of human DNA glycosylases for repair of oxidative DNA damage. Nucleic Acids Res. 1998, 26:2917-2922.
151. Takao M., Kanno S., Shiromoto T., Hasegawa R., Ide H., Ikeda S., Sarker A.H., Seki S., Xing J.Z., Le X.C., Weinfeld M., Kobayashi K., Miyazaki J., Muijtjens M., Hoeijmakers J.H., van der Horst G., Yasui A. Novel nuclear and mitochondrial glycosylases revealed by disruption of the mouse Nth1 gene encoding an endonuclease III homolog for repair of thymine glycols. EMBO J. 2002, 21:3486-3493.
152. Tan Z., Sun N., Schreiber S.S. Immunohistochemical localization of redox factor-1 (Ref-1) in Alzheimer's hippocampus. Neuroreport 1998, 9:2749-2752.
153. Tann A.W., Boldogh I., Meiss G., Qian W., Van Houten B., Mitra S., Szczesny B. Apoptosis induced by persistent single-strand breaks in mitochondrial genome: critical role of EXOG (5'-exo/endonuclease) in their repair. J. Biol. Chem. 2011, 286:31975-31983.
154. Taroni F., DiDonato S. Pathways to motor incoordination: the inherited ataxias. Nat. Rev. Neurosci. 2004, 5:641-655.
155. Tell G., Crivellato E., Pines A., Paron I., Pucillo C., Manzini G., Bandiera A., Kelley M.R., Di Loreto C., Damante G. Mitochondrial localization of APE/Ref-1 in thyroid cells. Mutat. Res. 2001, 485:143-152.
156. Thayer M.M., Ahern H., Xing D., Cunningham R.P., Tainer J.A. Novel DNA binding motifs in the DNA repair enzyme endonuclease III crystal structure. EMBO J. 1995, 14:4108-4120.
157. Theriot C.A., Hegde M.L., Hazra T.K., Mitra S. RPA physically interacts with the human DNA glycosylase NEIL1 to regulate excision of oxidative DNA base damage in primer-template structures. DNA Repair (Amst.) 2010, 9:643-652.
158. Turrens J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 2003, 552:335-344.
159. Vascotto C., Fantini D., Romanello M., Cesaratto L., Deganuto M., Leonardi A., Radicella J.P., Kelley M.R., D'Ambrosio C., Scaloni A., Quadrifoglio F., Tell G. APE1/Ref-1 interacts with NPM1 within nucleoli and plays a role in the rRNA quality control process. Mol. Cell. Biol. 2009, 29:1834-1854.
160. Weissman L., Jo D.G., Sorensen M.M., de Souza-Pinto N.C., Markesbery W.R., Mattson M.P., Bohr V.A. Defective DNA base excision repair in brain from individuals with Alzheimer's disease and amnestic mild cognitive impairment. Nucleic Acids Res. 2007, 35:5545-5555.
161. Whiteside J.R., Box C.L., McMillan T.J., Allinson S.L. Cadmium and copper inhibit both DNA repair activities of polynucleotide kinase. DNA Repair (Amst.) 2010, 9:83-89.
162. Wiederhold L., Leppard J.B., Kedar P., Karimi-Busheri F., Rasouli-Nia A., Weinfeld M., Tomkinson A.E., Izumi T., Prasad R., Wilson S.H., Mitra S., Hazra T.K. AP endonuclease-independent DNA base excision repair in human cells. Mol. Cell 2004, 15:209-220.
163. Wilson D.M., McNeill D.R. Base excision repair and the central nervous system. Neuroscience 2007, 145:1187-1200.
164. Wilson S.H. Mammalian base excision repair and DNA polymerase beta. Mutat. Res. 1998, 407:203-215.
165. Yacoub A., Kelley M.R., Deutsch W.A. The DNA repair activity of human redox/repair protein APE/Ref-1 is inactivated by phosphorylation. Cancer Res. 1997, 57:5457-5459.
166. Yang S.W., Burgin A.B., Huizenga B.N., Robertson C.A., Yao K.C., Nash H.A. A eukaryotic enzyme that can disjoin dead-end covalent complexes between DNA and type I topoisomerases. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:11534-11539.
167. Yasuhara T., Hara K., Sethi K.D., Morgan J.C., Borlongan C.V. Increased 8-OHdG levels in the urine, serum, and substantia nigra of hemiparkinsonian rats. Brain Res. 2007, 1133:49-52.
168. Zheng L., Zhou M., Guo Z., Lu H., Qian L., Dai H., Qiu J., Yakubovskaya E., Bogenhagen D.F., Demple B., Shen B. Human DNA2 is a mitochondrial nuclease/helicase for efficient processing of DNA replication and repair intermediates. Mol. Cell 2008, 32:325-336.