DNA damage and aging

Mechanisms of Ageing and Development

Volumn 125, Issue 6, 2004, Pages 405-415

  Karanjawala, Zarir E ^a   Lieber, Michael R ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

DNA recombination; DNA repair; Neurodegeneration; NHEJ; Nonhomologous DNA end joining; Pathological aging; Physiological aging; Repetitive genome

Indexed keywords

CELL NUCLEUS DNA; DNA; DOUBLE STRANDED DNA; MITOCHONDRIAL DNA; NUCLEAR PROTEIN; REACTIVE OXYGEN METABOLITE;

AGING; ALZHEIMER DISEASE; ARTICLE; CHROMOSOME ABERRATION; CORRELATION ANALYSIS; DNA CONTENT; DNA METABOLISM; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; DNA SYNTHESIS; EUKARYOTE; GENE DELETION; GENE FREQUENCY; GENE LOCUS; GENE LOSS; GENE MUTATION; GENOME; HUMAN; LIFESPAN; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROGERIA; ROTHMUND THOMSON SYNDROME; SOMATIC MUTATION; WERNER SYNDROME;

EUKARYOTA; MAMMALIA; METAZOA;

EID: 2942595770     PISSN: 00476374     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mad.2004.04.003     Document Type: Article

References (100)

1. Adachi, N., Lieber, M.R., 2002. Bidirectional gene organization: a common architectural motif of the human genome. Cell 109, 807-809.
2. Austad, S.N., Fischer, K.E., 1991. Mammalian aging, metabolism, and ecology: evidence from bats and marsupials. J. Gerontol. 46, B47-53.
3. Barja, G., 2002. Rate of generation of oxidative stress-related damage and animal longevity. Free Rad. Biol. Med. 33, 1167-1172.
4. Barja, G., Herrero, A., 2000. Oxidative damage to mitochondrial DNA is inversely related to maximum lifespan in the heart and brain of mammals. FASEB J. 14, 312-318.
5. Bassing, C.H., Suh, H., Ferguson, D.O., Chua, K.F., Manis, J., Eckersdorff, M., Bronson, R., Lee, C., Alt, F.W., 2003. Histone H2AX: a dosage-dependent suppress of oncogenic translocations and tumors. Cell 114, 359-370.
6. Beckman, K.B., Ames, B.N., 1998. The free radical theory of aging matures. Physiol. Rev. 78, 547-581.
7. Blumenthal, H.T., 2003. The aging-disease dichotomy: true or false? J. Gerontol. 58A, 138-145.
8. Buerstedde, J.M., Takeda, S., 1991. Increased ratio of targeted to random integration after transfection of chicken B cells. Cell 67, 179-188.
9. Burke, B., Stewart, C.L., 2002. Life at the edge: the nuclear envelope and human disease. Nat. Rev. Mol. Cell Biol. 3, 575-585.
10. Burkhart-Schultz, K.J., Jones, I.M., 1997. Deletion and insertion in vivo somatic mutations in the hypoxanthine phosphoribosyl transferase (hprt) gene of human T-lymphocytes. Environ. Mol. Mutagen. 30, 371-384.
11. Burkhart-Schultz, K.J., Thompson, C.L., Jones, I.M., 1996. Spectrum of somatic mutation at the hypoxanthine phosphoribosyltransferase (hprt) gene of healthy people. Carcinogenesis, 1871-1883.
12. Burt, D.W., 2002. Origin and evolution of avian microchromosomes. Cytogenet. Gen. Res. 96, 97-112.
13. Busuttil, R.A., Rubio, M., Dolle, M.E., Campisi, J., Vijg, J., 2003. Oxygen accelerates the accumulation of mutations during the senescence and immortalization of murine cells in culture. Aging Cell 2, 287-294.
14. Celeste, A., Difilippantonio, S., Difilippantonio, M.J., Fernandez-Capetillo, O., Pilch, D.R., Sedelnikova, O.A., Eckhaus, M., Ried, T., Bonner, W.M., Nussenzweig, A., 2003. H2AX haploinsufficiency modifies genomic stability and tumor susceptibility. Cell 114, 371-383.
15. Chance, B., Sies, H., Boveris, A., 1979. Hydroperoxide metabolism in mammalian organs. Physiol. Rev. 59, 527-603.
16. Cole, J., Skopek, T.R., 1994. International Commission for Protection Against Environmental Mutagens and Carcinogens. Working Paper no. 3. Somatic mutant frequency, mutation rates, and mutational spectra in the human population in vivo. Mutat. Res. 304, 33-105.
17. Colgin, L.M., Hackmann, A.F., Emond, M.J., Monnat, R.J., 2002. The unexpected landscape of in vivo somatic mutation in a human epithelial cell lineage. Proc. Natl. Acad. Sci. U.S.A. 99, 1437-1442.
18. Cooper, M.P., Machwe, A., Orren, D.K., Brosh, R.M., Ramsden, D., Bohr, V.A., 2000. Ku complex interacts with and stimulates the Werner protein. Genes Dev. 14, 907-912.
19. deSandre-Giovannoli, A., Bernard, R., Cau, P., Navarro, C., Amiel, J., Boccaccio, I., Lyonnet, S., Stewart, C.L., Munnich, A., LeMerrer, M., Levy, N., 2003. Lamin A truncation in Hutchinson-Gilford progeria. Science 300, 2055.
20. Dolle, M.E., Synder, W.K., Dunson, D.B., Vijg, J., 2002. Mutational fingerprints of aging. Nucl. Acids Res. 30, 545-549.
21. Dolle, M.E., Vijg, J., 2002. Genome dynamics in aging mice. Genome Res. 12, 1732-1738.
22. Eriksson, M., Brown, W.T., Gordon, L.B., Glynn, M.W., Singer, J., Scott, L., Erdos, M.R., Robbins, C.M., Moses, T.Y., Berglund, P., Dutra, A., Pak, E., Durkin, S., Csoka, A.B., Boehnke, M., Glover, T.W., Collins, F.S., 2003. Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 423, 293-298.
23. Espejel, S., Franco, S., Rodriguez-Perales, S., Bouffler, S.D., Cigudosa, J.C., Blasco, M.A., 2002. Mammalian Ku86 mediates chromosomal fusions and apoptosis caused by critically short telomeres. EMBO J. 21, 2207-2219.
24. Fagagna, F.D.A.d., Hande, M.P., Tong, W., Roth, D., Lansdorp, P.M., Wang, Z., Jackson, S.P., 2001. Effects of DNA nonhomologous end-joining factors on telomere length and chromosomal stability in mammalian cells. Curr. Biol. 11, 1192-1196.
25. Ferguson, D.O., Sekiguchi, J.M., Chang, S., Frank, K.M., Gao, Y., De-Pinho, R.A., Alt, F.W., 2000. The nonhomologous end-joining pathway of DNA repair is required for genomic stability and the uppression of translocations. Proc. Natl. Acad. Sci. U.S.A. 97, 6630-6633.
26. Fernandez-Checa, J.C., 2003. Redox regulation and signaling lipids in mitochondria apoptosis. Biochem. Biophys. Res. Commun. 304, 471-479.
27. Finch, C. E., 1990. Longevity, Senescence, and the Genome. University of Chicago, Chicago.
28. Floyd, R.A., West, M., Hensley, K., 2001. Oxidative biochemical markers clues to understanding aging in long-lived species. Exp. Gerontol. 36, 619-640.
29. Friedberg, E.C., Walker, G.C., Siede, W., 1995. DNA Repair and Mutagenesis. ASM Press, Washington, DC.
30. Gao, Y., Chaudhurri, J., Zhu, C., Davidson, L., Weaver, D.T., Alt, F.W., 1998. A targeted DNA-PKcs-null mutation reveals DNA-PK independent for Ku in V(D)J recombination. Immunity 9, 367-376.
31. Gensler, H.L., Bernstein, H., 1981. DNA damage as the primary cause of aging. Quart. Rev. Biol. 56, 279-303.
32. Gilley, D., Tanaka, H., Hande, M., Kurimasa, A., Li, G., Oshimura, M., Chen, D.J., 2001. DNA-PKcs is critical for telomere capping. Proc. Natl. Acad. Sci. U.S.A. 98, 15084-15088.
33. Goedecke, W., Eijpe, M., Offenberg, H.H., Aalderen, M.v., Heyting, C., 1999. Mre11 and Ku70 interact in somatic cells, but are differentially expressed in early meiosis. Nat. Genet. 23, 194-198.
34. Goss, K., Risinger, M., Kordich, J., Sanz, M., Straughen, J., Slovek, L., Capobianco, A., German, J., Boivin, G., Groden, J., 2002. Enhanced tumor formation in mice heterozygous for Blm mutation. Science 297, 2051-2053.
35. Gredilla, R., Sanz, A., Lopez-Torres, M., Barja, G., 2001. Caloric restriction decreases mitochondrial free radical generation at Complex I and lowers oxidative damage to mitochondrial DNA in the rat heart. FASEB J. 15, 1589-1591.
36. Gu, Y., Jin, S., Gao, Y., Weaver, D.T., Alt, F.W., 1997. Ku70-deficient embryonic stem cells have increased ionizing radiosensitivity, defective DNA end-binding activity, and inability to support V(D)J recombination. Proc. Natl. Acad. Sci. U.S.A. 94, 8076-8081.
37. Gu, Y., Seidl, K., Rathbun, G.A., Zhu, C., Manis, J.P., vanderStoep, N., Davidson, L., Cheng, H.L., Sekiguchi, J., Frank, K., Stanhope-Baker, P., Schlissel, M.S., Roth, D.B., Alt, F.W., 1997. Growth retardation and leaky SCID phenotype of Ku70-deficient mice. Immunity 7, 653-665.
38. Gu, Y., Sekiguchi, J., Gao, Y., Dikkes, P., Frank, K., Ferguson, D., Hasty, P., Chun, J., Alt, F.W., 2000. Defective embryonic neurogenesis in Ku-deficient but not DNA-dependent protein kinase catalytic subunit-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 97, 2668-2673.
39. Hackman, P., Hou, S.M., Nyberg, F., Pershagen, G., Lambert, B., 2000. Mutational spectra at the hypoxanthine-guanine phosphoribosyltransferase (HPRT) locus in T-lymphocytes of nonsmoking and smoking lung cancer patients. Mutat. Res. 468, 45-61.
40. Hamilton, M.L., Remmen, H.V., Drake, J.A., Yang, H., Guo, Z.M., Kewitt, K., Walter, C.A., Richardson, A., 2001. Does oxidative damage to DNA increase with age? Proc. Natl. Acad. Sci. U.S.A. 98, 10469-10474.
41. Harman, D., 1956. Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 11, 298-300.
42. Hasty, P., Campisi, J., Hoeijmakers, J., vanSteeg, H., Vijg, J., 2003. Aging and genome maintenance: lessons from the mouse? Science 299, 1355-1359.
43. Heidenreich, E., Novotny, R., Kneidinger, B., Holzmann, V., Wintersberger, U., 2003. Non-homologous end joining as an important mutagenic process in cell cycle-arrested cells. EMBO J. 22, 2274-2283.
44. Hekimi, S., Guarente, L., 2003. Genetics and the specificity of the aging process. Science 299, 351-1354.
45. Herrero, A., Barja, G., 1999. 8-Oxodeoxyguanosine levels in heart and brain mitochondrial and nuclear DNA of two mammals and three birds in relation to their different rates of aging. Aging 11, 294-300.
46. Holmes, D.J., Fluckiger, R., Austad, S.N., 2001. Comparative biology of aging in birds: an update. Exp. Gerontol. 36, 869-884.
47. Imlay, J.A., 2002. How oxygen damages microbes: oxygen tolerance and obligate anaerobiosis. Adv. Microb. Physiol. 46, 111-153.
48. Imlay, J.A., Linn, S., 1988. DNA damage and oxygen radical toxicity. Science 240, 1302-1309.
49. Jinnah, H.A., DeGregorio, L., Harris, J.C., Nyhan, W.L., O'Neill, J.P., 2000. The spectrum of inherited mutations causing HPRT deficiency: new cases and a review of 196 previously reported cases. Mutat. Res. 463, 309-326.
50. Kanaar, R., Hoeijmakers, J.H.J., 1997. Recombination and joining: different means to the same ends. Genes Funct. 1, 165-174.
51. Karanjawala, Z.E., Adachi, N., Irvine, R.A., Oh, E.K., Shibata, D., Schwarz, K., Hsieh, C.L., Lieber, M.R., 2002. The embryonic lethality in DNA ligase IV-deficient mice is rescued by deletion of Ku: implications for unifying the heterogeneous phenotypes of NHEJ mutants. DNA Repair 1, 1017-1026.
52. Karanjawala, Z.E., Grawunder, U., Hsieh, C.-L., Lieber, M.R., 1999. The nonhomologous DNA end joining pathway is important for chromosome stability in primary fibroblasts. Curr. Biol. 9, 1501-1504.
53. Karanjawala, Z.E., Murphy, N., Hinton, D.R., Hsieh, C.-L., Lieber, M.R., 2002. Oxygen metabolism causes chromosome breaks and is associated with the neuronal apoptosis observed in double-strand break repair mutants. Curr. Biol. 12, 397-402.
54. Kirkwood, T.B.L., Boys, R.J., Gillespie, C.S., Proctor, C.J., Shanley, D.P., Wilkinson, D.J., 2003. Towards an e-biology of ageing: integrating theory and data. Nature Rev. Mol. Cell. Biology 4, 243-249.
55. Kirkwood, T.B.L., Proctor, C.J., 2003. Somatic mutations and ageing in silico. Mech. Age. Dev. 124, 85-92.
56. Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., Yokochi, M., Mizuno, Y., Shimizu, N., 1998. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392, 605-608.
57. Klungland, A., Rosewell, I., Hollenbach, S., Larsen, E., Daly, G., Epe, B., Seeberg, E., Lindahl, T., Barnes, D.E., 1999. Accumulation of premutagenic DNA lesions in mice defective in removal of oxidative base damage. Proc. Natl. Acad. Sci. U.S.A. 96, 13300-13305.
58. Kraus, E., Leung, W.Y., Haber, J.E., 2001. Break-induced replication: a review and an example in budding yeast. Proc. Natl. Acad. Sci. U.S.A. 98, 8255-8262.
59. Ku, H.H., Brunk, U.T., Sohal, R., 1993. Relationship between mitochondrial superoxide and hydrogen peroxide production and longevity of mammalian species. Free Radic. Biol. Med. 15, 621-627.
60. Ku, H.H., Sohal, R.S., 1993. Comparison of mitochondrial pro-oxidant generation and anti-oxidant defenses between rat and pigeon: possible basis of variation in longevity and metabolic potential. Mech. Ageing Dev. 72, 67-76.
61. Kucherlapati, M., Yang, K., Kuraguchi, M., Zhao, J., Lia, M., Heyer, J., Kane, M., Fan, K., Russell, R., Brown, A., Kneitz, B., Edelmann, W., Kolodner, R.D., Lipkin, M., Kucherlapati, R., 2002. Haploinsufficiency of flap endonuclease (Fen1) leads to rapid tumor progression. Proc. Natl. Acad. Sci. 99, 9924-9929.
62. Lebel, M., Leder, P., 1998. A deletion within the murine Werner syndrome helicase induces sensitivity to inhibitors of topoisomerase and loss of cellular proliferative capacity. Proc. Natl. Acad. Sci. U.S.A. 95, 13097-13102.
63. Li, B., Comai, L., 2000. Functional interaction between Ku and the Werner syndrome protein in DNA end processing. J. Biol. Chem. 275, 28349-28352.
64. Li, G.C., Ouyang, H., Li, X., Nagasawa, H., Little, J.B., Chen, D.J., Ling, C.C., Fuks, Z., Cordon-Cardo, C., 1998. Ku70: a candidate tumor suppressor gene for murine T cell lymphoma. Mol. Cell 2, 1-8.
65. Lieber, M.R., 1999. The biochemistry and biological significance of nonhomologous DNA end joining: an essential repair process in multicellular eukaryotes. Genes Cells 4, 77-85.
66. Lieber, M.R., Karanjawala, Z.E., 2004. Ageing, repetitive genomes and DNA damage. Nat. Rev. Mol. Cell. Biol. 5, 69-75.
67. Lieber, M.R., Ma, Y., Pannicke, U., Schwarz, K., 2003. Mechanism and regulation of human non-homologous DNA end-joining. Nat. Rev. Mol. Cell. Biol. 4, 712-720.
68. Longo, V., Finch, C.E., 2003. Evolutionary medicine: from dwarf model systems to healthy centenarians? Science 299, 1342-1346.
69. Malynn, B.A., Blackwell, T.K., Fulop, G.M., Rathbun, G.A., Furley, A.J.W., Ferrier, P., Heinke, L.B., Phillips, R.A., Yancopoulos, G.D., Alt, F.W., 1988. The scid defect affects the final step of the immunoglobulin VDJ recombinase mechanism. Cell 54, 453-460.
70. Martin, G.M., Oshima, J., 2000. Lessons from human progeroid syndromes. Nature 408, 263-266.
71. Martin, G.M., Smith, A.C., Ketterer, D.J., Ogburn, C.E., Disteche, C.M., 1985. Increased chromosomal aberrations in first metaphases of cells isolated from the kidneys of aged mice. Israel J. Med. Sci. 21, 296-301.
72. Mukherjee, A.B., Costello, C., 1998. Aneuploidy analysis in fibroblasts of human premature aging syndromes by FISH during in vitro cellular aging. Mech. Ageing Dev. 103, 209-222.
73. NatlRadProtectBoard, 1986. Living with Radiation. Reading, England.
74. Ogburn, C.E., Carlberg, K., Ottinger, M.A., Holmes, D.J., Martin, G.M., Austad, S.N., 2001. Exceptional cellular resistance to oxidative damage in long-lived birds requires active gene expression. J. Gerontol. Biol. Sci. 56A, B468-B474.
75. Okazaki, K., Nishikawa, S.-I., Sakano, H., 1988. Aberrant immunoglobulin gene rearrangement in scid mouse bone marrow cells. J. Immunol. 141, 1348-1352.
76. Parrinello, S., Samper, E., Krtolica, A., Goldstein, J., Melov, S., Campisi, J., 2003. Oxygen sensitivity severely limits replicative lifespan of murine fibroblasts. Nat. Cell Biol. 5, 741-747.
77. Podlutsky, A., Hou, S.-M., Nyberg, F., Pershagen, G., Lambert, B., 1999. Influence of smoking and donor age on the spectrum of in vivo mutation at the HPRT-locus in T lymphocytes of healthy adults. Mutat. Res. 431, 325-339.
78. Podlutsky, A., Osterholm, A.M., Hou, S.M., Hofmaier, A., Lambert, B., 1998. Spectrum of point mutations in the coding region of the hypoxanthine phophoribosyltransferase (hprt) gene in human T-lymphocytes in vivo. Carcinogenesis 19, 557-566.
79. Prince, P.R., Emond, M.J., Monnat, R.J., 2001. Loss of Werner syndrome protein function promotes aberrant mitotic recombination. Genes Dev. 15, 933-938.
80. Prisee, K.M., Davies, S., Michael, B.D., 1989. Cell killing and DNA damage in Chinese hamster V79 cells treated with hydrogen peroxide. Int. J. Rad. Biol. 55, 583-592.
81. Rong, Y.S., Golic, K.G., 2003. The homologous chromosome is an effective template for the repair of mitotic DNA double-strand breaks in drosophila. Genetics 165, 1831-1842.
82. Roth, D., Wilson, J., 1988. Illegitimate recombination in mammalian cells. In: Kucherlapapti, R., Smith, G.R., Genetic Recombination. American Society for Microbiology, Washington, DC, pp. 621-653.
83. Saintigny, Y., Makienko, K., Swanson, C., Emond, M.J., Monnat, R.J., 2002. Homologous recombination resolution defect in Werner syndrome. Mol. Cell. Biol. 22, 6971-6978.
84. Schuler, W., Weiler, I.J., Schuler, A., Phillips, R.A., Rosenberg, N., Mak, T.W., Kearney, J.F., Perry, R.P., Bosma, M.J., 1986. Rearrangement of antigen receptor genes is defective in mice with severe combined immune deficiency. Cell 46, 963-972.
85. Seidman, J.G., Siedman, C., 2002. Transcription factor haploinsufficiency: when half a loaf is not enough. J. Clin. Invest. 109, 451-455.
86. Sharpless, N.E., Ferguson, D.O., O'Hagen, R., Castrillon, D., Lee, C., Farazi, P., Alson, S., Fleming, J., Morton, C., Frank, K., Chin, L., Alt, F.W., DePinho, R.A., 2001. Impaired nonhomologous DNA end-joining provokes soft tissue sarcomas harboring chromosomal translocations, amplifications, and deletions. Mol. Cell 8, 1187-1196.
87. Sohal, R.S., Ku, H.H., Agarwal, S., Forster, M., Lal, H., 1994. Oxidative damage, mitochondrial oxidant generation and antioxidant defenses during aging and in response to food restriction. Mech. Ageing Dev. 74, 121-133.
88. Sohal, R.S., Mockett, R.J., Orr, W.C., 2002. Mechanisms of aging: an appraisal of the oxidative stress hypothesis. Free Rad. Biol. Med. 33, 575-586.
89. Speakman, J.R., Selman, C., McLaren, J.S., Harper, E.J., 2002. Living fast, dying when? The link between aging and energetics. J. Nutr. 132, 1583S-1597S.
90. Strachen, T., Read, A. P., 1999. Human Molecular Genetics. Wiley-Liss, New York.
91. Takata, M., Sasaki, M.S., Sonoda, E., Morrison, C., Hashimoto, M., Utsumi, H., Yamaguchi-Iwai, Y., Shinohara, A., Takeda, S., 1998. Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 17, 5497-5508.
92. Tatar, M., Bartke, A., Antebi, A., 2003. The endocrine regulation of aging by insulin-like signals. Science 299, 1346-1351.
93. Tower, J., 1996. Aging mechanisms in fruit flies. BioEssays 18, 799-807.
94. Turker, M.S., 2000. Somatic cell mutations: can they provide a link between aging and cancer? Mech. Ageing Dev. 117, 1-19.
95. vandenBussche, R.A., Longmire, J.L., Baker, R.J., 1995. How bats achieve a small C-value: frequency of repetitive DNA in Macrotus. Mamm. Gen. 6, 521-525.
96. vanGent, D.C., Hoeijmakers, J.H.J., Kanaar, R., 2001. Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet. 2, 196-206.
97. Viguera, E., Canceill, D., Ehrlich, S.D., 2002. Replication slippage involves DNA polymerase pausing and dissociation. EMBO J. 20, 2587-2595.
98. Vogel, H., Lim, D.-S., Karsenty, G., Finegold, M., Hasty, P., 1999. Deletion of Ku86 causes early onset of senescence in mice. Proc. Natl. Acad. Sci. U.S.A. 96, 10770-10775.
99. Wallace, D.C., 1999. Mitochondrial diseases in man and mouse. Science 283, 1482-1488.
100. West, S.C., 2003. Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell. Biol. 4, 435-445.