DNA damage and base excision repair in mitochondria and their role in aging

Journal of Aging Research

Volumn 2011, Issue , 2011, Pages

  Gredilla, Ricardo ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

AGING; APURINIC SITE; APYRIMIDINIC SITE; CELL LOSS; DNA CLEAVAGE; DNA DAMAGE; DNA FRAGMENTATION; DNA METABOLISM; DOUBLE STRANDED DNA BREAK; EXCISION REPAIR; GENE REARRANGEMENT; HUMAN; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION;

EID: 84866247628     PISSN: 20902204     EISSN: 20902212     Source Type: Journal    
DOI: 10.4061/2011/257093     Document Type: Review

References (105)

1. Bohr V. A., DNA damage and its processing. Relation to human disease. Journal of Inherited Metabolic Disease 2002 25 3 215 222 2-s2.0-0035990297 10.1023/A:1015681929316 (Pubitemid 34700312)
2. Wilson D. M. III, Bohr V. A., McKinnon P. J., DNA damage, DNA repair, ageing and age-related disease. Mechanisms of Ageing and Development 2008 129 7-8 349 352 2-s2.0-45449100900 10.1016/j.mad.2008.02.013
3. Bohr V. A., Rising from the RecQ-age: the role of human RecQ helicases in genome maintenance. Trends in Biochemical Sciences 2008 33 12 609 620 2-s2.0-56449090762 10.1016/j.tibs.2008.09.003
4. Stevnsner T., Muftuoglu M., Aamann M. D., Bohr V. A., The role of Cockayne Syndrome group B (CSB) protein in base excision repair and aging. Mechanisms of Ageing and Development 2008 129 7-8 441 448 2-s2.0-45449093552 10.1016/j.mad.2008.04.009
5. Seeberg E., Eide L., Bjoras M., The base excision repair pathway. Trends in Biochemical Sciences 1995 20 10 391 397 2-s2.0-0028857681 10.1016/S0968-0004(00)89086-6
6. Aravind L., Walker D. R., Koonin E. V., Conserved domains in DNA repair proteins and evolution of repair systems. Nucleic Acids Research 1999 27 5 1223 1242 2-s2.0-0033105094 10.1093/nar/27.5.1223 (Pubitemid 29206430)
7. Soerensen M., Gredilla R., Muller-Ohldach M., Werner A., Bohr V. A., Osiewacz H. D., Stevnsner T., A potential impact of DNA repair on ageing and lifespan in the ageing model organism Podospora anserina: decrease in mitochondrial DNA repair activity during ageing. Mechanisms of Ageing and Development 2009 130 8 487 496 2-s2.0-67651001697 10.1016/j.mad.2009.05.003
8. Krokan H. E., Standal R., Slupphaug G., DNA glycosylases in the base excision repair of DNA. Biochemical Journal 1997 325 1 1 16 2-s2.0-0030861915 (Pubitemid 27322679)
9. Hyun M., Bohr V. A., Ahn B., Biochemical characterization of the WRN-1 RecQ helicase of Caenorhabditis elegans. Biochemistry 2008 47 28 7583 7593 2-s2.0-47249104754 10.1021/bi800197m (Pubitemid 351991035)
10. Beckman K. B., Ames B. N., Endogenous oxidative damage of mtDNA. Mutation Research 1999 424 1-2 51 58 2-s2.0-0033535365 10.1016/S0027-5107(99)00007-X (Pubitemid 29101607)
11. Barja G., Mitochondrial oxygen radical generation and leak: sites of production in States 4 and 3, organ specificity, and relation to aging and longevity. Journal of Bioenergetics and Biomembranes 1999 31 4 347 366 2-s2.0-0033369476 10.1023/A:1005427919188 (Pubitemid 30058570)
12. Trifunovic A., Wredenberg A., Falkenberg M., Spelbrink J. N., Rovio A. T., Bruder C. E., Bohlooly-Y M., Gldlöf S., Oldfors A., Wibom R., Törnell J., Jacobs H. T., Larsson N. G., Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 2004 429 6990 417 423 2-s2.0-2642580016 10.1038/nature02517 (Pubitemid 38715133)
13. Sastre J., Pallardo F. V., Garcia de la Asuncion J., Vina J., Mitochondria, oxidative stress and aging. Free Radical Research 2000 32 3 189 198 2-s2.0-0034016125 (Pubitemid 30140162)
14. Beal M. F., Mitochondria take center stage in aging and neurodegeneration. Annals of Neurology 2005 58 4 495 505 2-s2.0-25444474703 10.1002/ana.20624 (Pubitemid 41377212)
15. Melov S., Modeling mitochondrial function in aging neurons. Trends in Neurosciences 2004 27 10 601 606 2-s2.0-4544307465 10.1016/j.tins.2004.08.004 (Pubitemid 39221396)
16. Vermulst M., Bielas J. H., Kujoth G. C., Ladiges W. C., Rabinovitch P. S., Prolla T. A., Loeb L. A., Mitochondrial point mutations do not limit the natural lifespan of mice. Nature Genetics 2007 39 4 540 543 2-s2.0-34047116291 10.1038/ng1988 (Pubitemid 46514771)
17. Harman D., The biologic clock: the mitochondria? Journal of the American Geriatrics Society 1972 20 4 145 147 2-s2.0-0015319592
18. Miquel J., Economos A. C., Fleming J., Johnson J. E. Jr., Mitochondrial role in cell aging. Experimental Gerontology 1980 15 6 575 591 2-s2.0-0019160038 10.1016/0531-5565(80)90010-8 (Pubitemid 11243249)
19. 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 2-s2.0-0033972463 (Pubitemid 30086068)
20. Hamilton M. L., Guo Z., Fuller C. D., Van Remmen H., Ward W. F., Austad S. N., Troyer D. A., Thompson I., Richardson A., A reliable assessment of 8-oxo-2-deoxyguanosine levels in nuclear and mitochondrial DNA using the sodium iodide method to isolate DNA. Nucleic Acids Research 2001 29 10 2117 2126 2-s2.0-0035872902 (Pubitemid 32472082)
21. Albring M., Griffith J., Attardi G., Association of a protein structure of probable membrane derivation with HeLa cell mitochondrial DNA near its origin of replication. Proceedings of the National Academy of Sciences of the United States of America 1977 74 4 1348 1352 2-s2.0-3242866272 (Pubitemid 8086893)
22. Holt I. J., He J., Mao C. C., Boyd-Kirkup J. D., Martinsson P., Sembongi H., Reyes A., Spelbrink J. N., Mammalian mitochondrial nucleoids: organizing an independently minded genome. Mitochondrion 2007 7 5 311 321 2-s2.0-34548159301 10.1016/j.mito.2007.06.004 (Pubitemid 47304014)
23. Spelbrink J. N., Li F. Y., Tiranti V., Nikali K., Yuan Q. P., Tariq M., Wanrooij S., Garrido N., Comi G., Morandi L., Santoro L., Toscano A., Fabrizi G. M., Somer H., Croxen R., Beeson D., Poulton J., Suomalainen A., Jacobs H. T., Zeviani M., Larsson C., Human mitochondrial DNA deletions associated with mutations in the gene encoding Twinkle, a phage T7 gene 4-like protein localized in mitochondria. Nature Genetics 2001 28 3 223 231 2-s2.0-0034938364 10.1038/90058 (Pubitemid 32626024)
24. Clayton D. A., Doda J. N., Friedberg E. C., The absence of a pyrimidine dimer repair mechanism in mammalian mitochondria. Proceedings of the National Academy of Sciences of the United States of America 1974 71 7 2777 2781 2-s2.0-0000825475
25. Liu P., Demple B., DNA repair in mammalian mitochondria: much more than we thought? Environmental and Molecular Mutagenesis 2010 51 5 417 426 2-s2.0-77953484497 10.1002/em.20576
26. Robertson A. B., Klungland A., Rognes T., Leiros I., Base excision repair: the long and short of it. Cellular and Molecular Life Sciences 2009 66 6 981 993 2-s2.0-62349120246 10.1007/s00018-009-8736-z
27. Xu G., Herzig M., Rotrekl V., Walter C. A., Base excision repair, aging and health span. Mechanisms of Ageing and Development 2008 129 7-8 366 382 2-s2.0-46149083468 10.1016/j.mad.2008.03.001
28. 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 2009 8 6 704 719 2-s2.0-67349125744 10.1016/j.dnarep.2009.01.021
29. Mason P. A., Lightowlers R. N., Why do mammalian mitochondria possess a mismatch repair activity? FEBS Letters 2003 554 1-2 6 9 2-s2.0-0142153431 10.1016/S0014-5793(03)01169-4 (Pubitemid 37324805)
30. Szczesny B., Tann A. W., Longley M. J., Copeland W. C., Mitra S., Long patch base excision repair in mammalian mitochondrial genomes. Journal of Biological Chemistry 2008 283 39 26349 26356 2-s2.0-55049124777 10.1074/jbc.M803491200
31. 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. Molecular and Cellular Biology 2008 28 16 4975 4987 2-s2.0-49449102611 10.1128/MCB.00457-08
32. 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 2008 7 4 605 616 2-s2.0-40649109989 10.1016/j.dnarep.2008.01.002
33. Aamann M. D., Sorensen M. M., Hvitby C., Berquist B. R., Muftuoglu M., Tian J., De Souza-Pinto N. C., Scheibye-Knudsen M., Wilson D. M., Stevnsner T., Bohr V. A., Cockayne syndrome group B protein promotes mitochondrial DNA stability by supporting the DNA repair association with the mitochondrial membrane. FASEB Journal 2010 24 7 2334 2346 2-s2.0-77954436746 10.1096/fj.09-147991
34. Hu J., De Souza-Pinto N. C., Haraguchi K., Hogue B. A., Jaruga P., Greenberg M. M., Dizdaroglu M., Bohr V. A., Repair of formamidopyrimidines in DNA involves different glycosylases: role of the OGG1, NTH1, and NEIL1 enzymes. Journal of Biological Chemistry 2005 280 49 40544 40551 2-s2.0-28844478775 10.1074/jbc.M508772200 (Pubitemid 41780543)
35. 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. Molecular Cell 2008 32 3 325 336 2-s2.0-55049112210 10.1016/j.molcel.2008.09.024
36. Pamplona R., Barja G., Highly resistant macromolecular components and low rate of generation of endogenous damage: two key traits of longevity. Ageing Research Reviews 2007 6 3 189 210 2-s2.0-34548655310 10.1016/j.arr.2007.06.002 (Pubitemid 47405306)
37. Maddukuri L., Speina E., Christiansen M., Dudziska D., Zaim J., Obtuowicz T., Kabaczyk S., Komisarski M., Bukowy Z., Szczegielniak J., Wójcik A., Kuśmierek J. T., Stevnsner T., Bohr V. A., Tudek B., Cockayne syndrome group B protein is engaged in processing of DNA adducts of lipid peroxidation product trans-4-hydroxy-2-nonenal. Mutation Research 2009 666 1-2 23 31 2-s2.0-67349121698 10.1016/j.mrfmmm.2009.03.007
38. Janowska B., Komisarski M., Prorok P., Sokoowska B., Kuśmierek J., Janion C., Tudek B., Nucleotide excision repair and recombination are engaged in repair of trans-4-hydroxy-2-nonenal adducts to DNA bases in Escherichia coli. International Journal of Biological Sciences 2009 5 6 611 620 2-s2.0-74049140453
39. Bohr V. A., Repair of oxidative DNA damage in nuclear and mitochondrial DNA, and some changes with aging in mammalian cells. Free Radical Biology and Medicine 2002 32 9 804 812 2-s2.0-0036570012 10.1016/S0891-5849(02)00787-6 (Pubitemid 34439251)
40. Slupphaug G., Kavli B., Krokan H. E., The interacting pathways for prevention and repair of oxidative DNA damage. Mutation Research 2003 531 1-2 231 251 2-s2.0-0344585940 10.1016/j.mrfmmm.2003.06.002 (Pubitemid 37456735)
41. Nilsen H., Otterlei M., Haug T., Solum K., Nagelhus T. A., Skorpen F., Krokan H. E., Nuclear and mitochondrial uracil-DNA glycosylases are generated by alternative splicing and transcription from different positions in the UNG gene. Nucleic Acids Research 1997 25 4 750 755 2-s2.0-0030841051 10.1093/nar/25.4.750 (Pubitemid 27299828)
42. Lindahl T., An N glycosidase from Escherichia coli that releases free uracil from DNA containing deaminated cytosine residues. Proceedings of the National Academy of Sciences of the United States of America 1974 71 9 3649 3653 2-s2.0-0000476915
43. 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. Journal of Biological Chemistry 2002 277 34 30417 30420 2-s2.0-0037162995 10.1074/jbc.C200355200 (Pubitemid 34970730)
44. 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. Proceedings of the National Academy of Sciences of the United States of America 2002 99 6 3523 3528 2-s2.0-0037133684 10.1073/pnas.062053799 (Pubitemid 34252141)
45. Gredilla R., Garm C., Holm R., Bohr V. A., Stevnsner T., Differential age-related changes in mitochondrial DNA repair activities in mouse brain regions. Neurobiology of Aging 2010 31 6 993 1002 2-s2.0-77951978898 10.1016/j.neurobiolaging.2008.07.004
46. Dou H., Mitra S., Hazra T. K., Repair of oxidized bases in DNA bubble structures by human DNA glycosylases NEIL1 and NEIL2. Journal of Biological Chemistry 2003 278 50 49679 49684 2-s2.0-0347379928 10.1074/jbc.M308658200 (Pubitemid 37548799)
47. Vartanian V., Lowell B., Minko I. G., Wood T. G., Ceci J. D., George S., Ballinger S. W., Corless C. L., McCullough A. K., Lloyd R. S., The metabolic syndrome resulting from a knockout of the NEIL1 DNA glycosylase. Proceedings of the National Academy of Sciences of the United States of America 2006 103 6 1864 1869 2-s2.0-32444434993 10.1073/pnas.0507444103 (Pubitemid 43228784)
48. Hanna M., Chow B. L., Morey N. J., Jinks-Robertson S., Doetsch P. W., Xiao W., Involvement of two endonuclease III homologs in the base excision repair pathway for the processing of DNA alkylation damage in Saccharomyces cerevisiae. DNA Repair 2004 3 1 51 59 2-s2.0-0347510578 10.1016/j.dnarep.2003. 09.005 (Pubitemid 38021995)
49. Demple B., Harrison L., Repair of oxidative damage to DNA: enzymology and biology. Annual Review of Biochemistry 1994 63 915 948 2-s2.0-0028342951 (Pubitemid 24218652)
50. Hegde M. L., Hazra T. K., Mitra S., Early steps in the DNA base excision/single-strand interruption repair pathway in mammalian cells. Cell Research 2008 18 1 27 47 2-s2.0-38049112778 10.1038/cr.2008.8
51. Tell G., Damante G., Caldwell D., Kelley M. R., The intracellular localization of APE1/Ref-1: more than a passive phenomenon? Antioxidants and Redox Signaling 2005 7 3-4 367 384 2-s2.0-14044269479 10.1089/ars.2005.7.367 (Pubitemid 40279805)
52. Xanthoudakis S., Miao G., Wang F., Pan Y. C. E., Curran T., Redox activation of Fos-Jun DNA binding activity is mediated by a DNA repair enzyme. EMBO Journal 1992 11 9 3323 3335 2-s2.0-0026714672
53. Bhakat K. K., Mantha A. K., Mitra S., Transcriptional regulatory functions of mammalian AP-endonuclease (APE1/Ref-1), an essential multifunctional protein. Antioxidants and Redox Signaling 2009 11 3 621 637 2-s2.0-58849117092 10.1089/ars.2008.2198
54. Mitra S., Izumi T., Boldogh I., Bhakat K. K., Chattopadhyay R., Szczesny B., Intracellular trafficking and regulation of mammalian AP-endonuclease 1 (APE1), an essential DNA repair protein. DNA Repair 2007 6 4 461 469 2-s2.0-33847666362 10.1016/j.dnarep.2006.10.010 (Pubitemid 46357051)
55. 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 Research 2006 34 7 2067 2076 2-s2.0-33645928711 10.1093/nar/gkl177 (Pubitemid 44314205)
56. Izumi T., Hazra T. K., Boldogh I., Tomkinson A. E., Park M. S., Ikeda S., Mitra S., Requirement for human AP endonuclease 1 for repair of 3'-blocking damage at DNA single-strand breaks induced by reactive oxygen species. Carcinogenesis 2000 21 7 1329 1334 2-s2.0-0033923815 (Pubitemid 30455991)
57. 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 1-2 43 65 2-s2.0-0242268065 10.1016/S0300-483X(03)00289-0 (Pubitemid 37340143)
58. Ludwig D. L., MacInnes M. A., Takiguchi Y., Purtymun P. E., Henrie M., Flannery M., Meneses J., Pedersen R. A., Chen D. J., A murine AP-endonuclease gene-targeted deficiency with post-implantation embryonic progression and ionizing radiation sensitivity. Mutation Research 1998 409 1 17 29 2-s2.0-0031720426 10.1016/S0921-8777(98)00039-1 (Pubitemid 28467991)
59. Klungland A., Lindahl T., Second pathway for completion of human DNA base excision-repair: reconstitution with purified proteins and requirement for DNase IV (FEN1). EMBO Journal 1997 16 11 3341 3348 2-s2.0-0030957997 10.1093/emboj/16.11.3341 (Pubitemid 27234971)
60. Demple B., DeMott M. S., Dynamics and diversions in base excision DNA repair of oxidized abasic lesions. Oncogene 2002 21 58 8926 8934 2-s2.0-0037115910 10.1038/sj.onc.1206178 (Pubitemid 36110822)
61. Kalifa L., Beutner G., Phadnis N., Sheu S. S., Sia E. A., Evidence for a role of FEN1 in maintaining mitochondrial DNA integrity. DNA Repair 2009 8 10 1242 1249 2-s2.0-70149110390 10.1016/j.dnarep.2009.07.008
62. Stuart J. A., Mayard S., Hashiguchi K., Souza-Pinto N. C., Bohr V. A., Localization of mitochondrial DNA base excision repair to an inner membrane-associated particulate fraction. Nucleic Acids Research 2005 33 12 3722 3732 2-s2.0-22244476422 10.1093/nar/gki683 (Pubitemid 41418541)
63. Spelbrink J. N., Functional organization of mammalian mitochondrial DNA in nucleoids: history, recent developments, and future challenges. IUBMB Life 2010 62 1 19 32 2-s2.0-77950573964 10.1002/iub.282
64. Alam T. I., Kanki T., Muta T., Ukaji K., Abe Y., Nakayama H., Takio K., Hamasaki N., Kang D., Human mitochondrial DNA is packaged with TFAM. Nucleic Acids Research 2003 31 6 1640 1645 2-s2.0-0037443884 10.1093/nar/gkg251 (Pubitemid 36336565)
65. Kanki T., Ohgaki K., Gaspari M., Gustafsson C. M., Fukuoh A., Sasaki N., Hamasaki N., Kang D., Architectural role of mitochondrial transcription factor a in maintenance of human mitochondrial DNA. Molecular and Cellular Biology 2004 24 22 9823 9834 2-s2.0-7644237446 10.1128/MCB.24.22.9823-9834.2004 (Pubitemid 39458810)
66. Canugovi C., Maynard S., Bayne A. C. V., Sykora P., Tian J., de Souza-Pinto N. C., Croteau D. L., Bohr V. A., BohrV@nih.gov The mitochondrial transcription factor A functions in mitochondrial base excision repair. DNA Repair 2010 9 10 1080 1089 10.1016/j.dnarep.2010.07.009
67. Di Re M., Sembongi H., He J., Reyes A., Yasukawa T., Martinsson P., Bailey L. J., Goffart S., Boyd-kirkup J. D., Wong T. S., Fersht A. R., Spelbrink J. N., Holt I. J., The accessory subunit of mitochondrial DNA polymerase γ determines the DNA content of mitochondrial nucleoids in human cultured cells. Nucleic Acids Research 2009 37 17 5701 5713 2-s2.0-73049113711 10.1093/nar/gkp614
68. Boesch P., Ibrahim N., Dietrich A., Lightowlers R. N., Membrane association of mitochondrial DNA facilitates base excision repair in mammalian mitochondria. Nucleic Acids Research 2009 38 5 1478 1488 2-s2.0-77950509082 10.1093/nar/gkp1143
69. Licht C. L., Stevnsner T., Bohr V. A., Cockayne syndrome group B cellular and biochemical functions. American Journal of Human Genetics 2003 73 6 1217 1239 2-s2.0-0346101496 10.1086/380399 (Pubitemid 38037417)
70. Osenbroch P. O., Auk-Emblem P., Halsne R., Strand J., Forstrom R. J., Van Der Pluijm I., Eide L., Accumulation of mitochondrial DNA damage and bioenergetic dysfunction in CSB defective cells. FEBS Journal 2009 276 10 2811 2821 2-s2.0-65349127253 10.1111/j.1742-4658.2009.07004.x
71. Kujoth C. C., Hiona A., Pugh T. D., Someya S., Panzer K., Wohlgemuth S. E., Hofer T., Seo A. Y., Sullivan R., Jobling W. A., Morrow J. D., Van Remmen H., Sedivy J. M., Yamasoba T., Tanokura M., Weindruch R., Leeuwenburgh C., Prolla T. A., Medicine: mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 2005 309 5733 481 484 2-s2.0-22344456832 10.1126/science.1112125 (Pubitemid 40994689)
72. Kujoth G. C., Bradshaw P. C., Haroon S., Prolla T. A., The role of mitochondrial DNA mutations in mammalian aging. PLoS Genetics 2007 3 2 e24 2-s2.0-34147181042 10.1371/journal.pgen.0030024
73. Kukat A., Trifunovic A., Somatic mtDNA mutations and aging-facts and fancies. Experimental Gerontology 2009 44 1-2 101 105 2-s2.0-57349098450 10.1016/j.exger.2008.05.006
74. Edgar D., Trifunovic A., The mtDNA mutator mouse: dissecting mitochondrial involvement in aging. Aging 2009 1 12 1028 1032 2-s2.0-77953630947
75. Vermulst M., Wanagat J., Kujoth G. C., Bielas J. H., Rabinovitch P. S., Prolla T. A., Loeb L. A., DNA deletions and clonal mutations drive premature aging in mitochondrial mutator mice. Nature Genetics 2008 40 4 392 394 2-s2.0-41349087783 10.1038/ng.95 (Pubitemid 351450885)
76. Edgar D., Shabalina I., Camara Y., Wredenberg A., Calvaruso M. A., Nijtmans L., Nedergaard J., Cannon B., Larsson N. G., Trifunovic A., Random point mutations with major effects on protein-coding genes are the driving force behind premature aging in mtDNA mutator mice. Cell Metabolism 2009 10 2 131 138 2-s2.0-68049115765 10.1016/j.cmet.2009.06.010
77. Reeve A. K., Krishnan K. J., Taylor G., Elson J. L., Bender A., Taylor R. W., Morris C. M., Turnbull D. M., The low abundance of clonally expanded mitochondrial DNA point mutations in aged substantia nigra neurons. Aging Cell 2009 8 4 496 498 2-s2.0-67651166799 10.1111/j.1474-9726.2009.00492.x
78. Krishnan K. J., Reeve A. K., Samuels D. C., Chinnery P. F., Blackwood J. K., Taylor R. W., Wanrooij S., Spelbrink J. N., Lightowlers R. N., Turnbull D. M., What causes mitochondrial DNA deletions in human cells? Nature Genetics 2008 40 3 275 279 2-s2.0-39749124232 10.1038/ng.f.94 (Pubitemid 351311775)
79. Bender A., Krishnan K. J., Morris C. M., Taylor G. A., Reeve A. K., Perry R. H., Jaros E., Hersheson J. S., Betts J., Klopstock T., Taylor R. W., Turnbull D. M., High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease. Nature Genetics 2006 38 5 515 517 2-s2.0-33646375711 10.1038/ng1769
80. Kraytsberg Y., Kudryavtseva E., McKee A. C., Geula C., Kowall N. W., Khrapko K., Mitochondrial DNA deletions are abundant and cause functional impairment in aged human substantia nigra neurons. Nature Genetics 2006 38 5 518 520 2-s2.0-33646351299 10.1038/ng1778
81. Bailey L. J., Cluett T. J., Reyes A., Prolla T. A., Poulton J., Leeuwenburgh C., Holt I. J., Mice expressing an error-prone DNA polymerase in mitochondria display elevated replication pausing and chromosomal breakage at fragile sites of mitochondrial DNA. Nucleic Acids Research 2009 37 7 2327 2335 2-s2.0-65549121567 10.1093/nar/gkp091
82. Hazkani-Covo E., Zeller R. M., Martin W., Molecular poltergeists: mitochondrial DNA copies (numts) in sequenced nuclear genomes. PLoS Genetics 2010 6 2 2-s2.0-77649210966 10.1371/journal.pgen.1000834 e1000834
83. Turner C., Killoran C., Thomas N. S. T., Rosenberg M., Chuzhanova N. A., Johnston J., Kemel Y., Cooper D. N., Biesecker L. G., Human genetic disease caused by de novo mitochondrial-nuclear DNA transfer. Human Genetics 2003 112 3 303 309 2-s2.0-0037359926 (Pubitemid 36869088)
84. Osiewacz H. D., Genes, mitochondria and aging in filamentous fungi. Ageing Research Reviews 2002 1 3 425 442 2-s2.0-0036596451 10.1016/S1568- 1637(02)00010-7 (Pubitemid 38340334)
85. Osiewacz H. D., Esser K., The mitochondrial plasmid of Podospora anserina: a mobile intron of a mitochondrial gene. Current Genetics 1984 8 4 299 305 2-s2.0-0021179991 (Pubitemid 14079441)
86. Wright R. M., Cummings D. J., Integration of mitochondrial gene sequences within the nuclear genome during senescence in a fungus. Nature 1983 302 5903 86 88 2-s2.0-0020659261 (Pubitemid 13138486)
87. Richter C., Do mitochondrial DNA fragments promote cancer and aging? FEBS Letters 1988 241 1-2 1 5 2-s2.0-0024266283 (Pubitemid 19004971)
88. Cheng X., Ivessa A. S., ivessaan@umdnj.edu The migration of mitochondrial DNA fragments to the nucleus affects the chronological aging process of Saccharomyces cerevisiae. Aging Cell 2010 9 5 919 923 10.1111/j.1474-9726.2010. 00607.x
89. Caro P., Gómez J., Arduini A., Mitochondrial DNA sequences are present inside nuclear DNA in rat tissues and increase with age. Mitochondrion 2010 10 479 486 2-s2.0-77953517114 10.1016/j.mito.2010.05.004
90. Aspnes L. E., Lee C. M., Weindruch R., Chung S. S., Roecker E. B., Aiken J. M., Caloric restriction reduces fiber loss and mitochondrial abnormalities in aged rat muscle. FASEB Journal 1997 11 7 573 581 2-s2.0-0030982145 (Pubitemid 27274431)
91. Cassano P., Lezza A. M. S., Leeuwenburgh C., Cantatore P., Gadaleta M. N., Measurement of the 4,834-bp mitochondrial DNA deletion level in aging rat liver and brain subjected or not to caloric restriction diet. Annals of the New York Academy of Sciences 2004 1019 269 273 2-s2.0-3242714939 10.1196/annals.1297.045 (Pubitemid 38951318)
92. Gredilla R., Barja G., The role of oxidative stress in relation to caloric restriction and longevity. Endocrinology 2005 146 9 3713 3717 2-s2.0-23844488868 10.1210/en.2005-0378 (Pubitemid 41175737)
93. Heydari A. R., Unnikrishnan A., Lucente L. V., Richardson A., Caloric restriction and genomic stability. Nucleic Acids Research 2007 35 22 7485 7496 2-s2.0-38049016464 10.1093/nar/gkm860
94. Kisby G. E., Kohama S. G., Olivas A., Churchwell M., Doerge D., Spangler E., Cabo R. D., Ingram D. K., Imhof B., Bao G., Kow Y. W., Effect of caloric restriction on base-excision repair (BER) in the aging rat brain. Experimental Gerontology 2010 45 3 208 216 2-s2.0-76749165751 10.1016/j.exger.2009.12.003
95. Cabelof D. C., Yanamadala S., Raffoul J. J., Guo Z., Soofi A., Heydari A. R., Caloric restriction promotes genomic stability by induction of base excision repair and reversal of its age-related decline. DNA Repair 2003 2 3 295 307 2-s2.0-0037353433 10.1016/S1568-7864(02)00219-7 (Pubitemid 36126398)
96. Stuart J. A., Karahalil B., Hogue B. A., Souza-Pinto N. C., Bohr V. A., Mitochondrial and nuclear DNA base excision repair are affected differently by caloric restriction. The FASEB Journal 2004 18 3 595 597 2-s2.0-2442695594
97. Karahalil B., Hogue B. A., De Souza-Pinto N. C., Bohr V. A., Base excision repair capacity in mitochondria and nuclei: tissue-specific variations. FASEB Journal 2002 16 14 1895 1902 2-s2.0-0036904776 10.1096/fj.02-0463com (Pubitemid 35462609)
98. 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. Journal of Neurochemistry 2002 81 6 1273 1284 2-s2.0-0036316413 10.1046/j.1471-4159.2002.00916.x (Pubitemid 34809261)
99. Imam S. Z., Karahalil B., Hogue B. A., Souza-Pinto N. C., Bohr V. A., Mitochondrial and nuclear DNA-repair capacity of various brain regions in mouse is altered in an age-dependent manner. Neurobiology of Aging 2006 27 8 1129 1136 2-s2.0-33744912521 10.1016/j.neurobiolaging.2005.06.002 (Pubitemid 43850641)
100. Weissman L., de Souza-Pinto N. C., Stevnsner T., Bohr V. A., DNA repair, mitochondria, and neurodegeneration. Neuroscience 2007 145 4 1318 1329 2-s2.0-34247156564 10.1016/j.neuroscience.2006.08.061 (Pubitemid 46602727)
101. 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. Mechanisms of Ageing and Development 1996 87 1 35 46 2-s2.0-0029916343 10.1016/0047-6374(96)01696-X (Pubitemid 26142429)
102. Brown M. R., Geddes J. W., Sullivan P. G., Brain region-specific, age-related, alterations in mitochondrial responses to elevated calcium. Journal of Bioenergetics and Biomembranes 2004 36 4 401 406 2-s2.0-10244261597 10.1023/B:JOBB.0000041775.10388.23 (Pubitemid 39619848)
103. Gredilla R., Weissman L., Yang J.-L., Bohr V. A., Stevnsner T., tvs@mb.au.dk Mitochondrial base excision repair in mouse synaptosomes during normal aging and in a model of Alzheimer's disease. Neurobiology of Aging. In press 10.1016/j.neurobiolaging.2010.06.019
104. Szczesny B., Tann A. W., Mitra S., Age- and tissue-specific changes in mitochondrial and nuclear DNA base excision repair activity in mice: susceptibility of skeletal muscles to oxidative injury. Mechanisms of Ageing and Development 2010 131 5 330 337 2-s2.0-77953036663 10.1016/j.mad.2010.03.009
105. Borghouts C., Kimpel E., Osiewacz H. D., Mitochondrial DNA rearrangements of Podospora anserina are under the control of the nuclear gene grisea. Proceedings of the National Academy of Sciences of the United States of America 1997 94 20 10768 10773 2-s2.0-0030885350 10.1073/pnas.94.20.10768 (Pubitemid 27430809)