Making ends meet in old age: DSB repair and aging

Mechanisms of Ageing and Development

Volumn 126, Issue 6-7, 2005, Pages 621-628

  Gorbunova, Vera ^a   Seluanov, Andrei ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

Author keywords

Aging; DNA repair; Double strand DNA breaks; Homologous recombination; Nonhomologous DNA end joining

Indexed keywords

DOUBLE STRANDED DNA;

AGING; CELL AGING; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; GENE MUTATION; GENE REARRANGEMENT; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; SENESCENCE; SHORT SURVEY;

EID: 18844457575     PISSN: 00476374     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mad.2005.02.008     Document Type: Article

References (103)

1. R.T. Abraham Cell cycle checkpoint signaling through the ATM and ATR kinases Genes Dev. 15 2001 2177 2196
2. N. Akyuz, G.S. Boehden, S. Susse, A. Rimek, U. Preuss, K.H. Scheidtmann, and L. Wiesmuller DNA substrate dependence of p53-mediated regulation of double-strand break repair Mol. Cell. Biol. 22 2002 6303 6317
3. Y. Andegeko, L. Moyal, L. Mittelman, I. Tsarfaty, Y. Shiloh, and G. Rotman Nuclear retention of ATM at sites of DNA double strand breaks J. Biol. Chem. 276 2001 38224 38230
4. M.L. Arbones, H.A. Austin, D.J. Capon, and G. Greenburg Gene targeting in normal somatic cells: inactivation of the interferon-gamma receptor in myoblasts Nat. Genet. 6 1994 90 97
5. C.J. Bakkenist, R. Drissi, J. Wu, M.B. Kastan, and J.S. Dome Disappearance of the telomere dysfunction-induced stress response in fully senescent cells Cancer Res. 64 2004 3748 3752
6. J. Bartek, J. Falck, and J. Lukas CHK2 kinase - a busy messenger Nat. Rev., Mol. Cell. Biol. 2 2001 877 886
7. K. Baynton, M. Otterlei, M. Bjoras, C. von Kobbe, V.A. Bohr, and E. Seeberg WRN interacts physically and functionally with the recombination mediator protein RAD52 J. Biol. Chem. 278 2003 36476 36486
8. P. Bertrand, D. Rouillard, A. Boulet, C. Levalois, T. Soussi, and B.S. Lopez Increase of spontaneous intrachromosomal homologous recombination in mammalian cells expressing mutant p53 protein Oncogene 14 1997 1117 1122
9. C.A. Bill, Y. Yu, N.R. Miselis, J.B. Little, and J.A. Nickoloff A role for p53 in DNA end rejoining by human cell extracts Mutat. Res. 385 1997 21 29
10. V.A. Bohr Human premature aging syndromes and genomic instability Mech. Ageing Dev. 123 2002 987 993
11. L. Chen, and J. Oshima Werner syndrome J. Biomed. Biotechnol. 2 2002 46 54
12. W.H. Cheng, C. von Kobbe, P.L. Opresko, L.M. Arthur, K. Komatsu, M.M. Seidman, J.P. Carney, and V.A. Bohr Linkage between Werner syndrome protein and the Mre11 complex via Nbs1 J. Biol. Chem. 279 2004 21169 21176
13. M. Chevanne, R. Caldini, D. Tombaccini, A. Mocali, G. Gori, and F. Paoletti Comparative levels of DNA breaks and sensitivity to oxidative stress in aged and senescent human fibroblasts: a distinctive pattern for centenarians Biogerontology 4 2003 97 104
14. L. Comai, and B. Li The Werner syndrome protein at the crossroads of DNA repair and apoptosis Mech. Ageing Dev. 125 2004 521 528
15. S.E. Critchlow, and S.P. Jackson DNA end-joining: from yeast to man Trends Biochem. Sci. 23 1998 394 398
16. H. Curtis, and C. Crowley Chromosome aberrations in the liver cells in relation to the somatic mutation theory of aging Radiat. Res. 19 1963 337 344
17. F. d'Adda di Fagagna, P.M. Reaper, L. Clay-Farrace, H. Fiegler, P. Carr, T. Von Zglinicki, G. Saretzki, N.P. Carter, and S.P. Jackson A DNA damage checkpoint response in telomere-initiated senescence Nature 426 2003 194 198
18. J.L. Dempsey, M. Pfeiffer, and A.A. Morley Effect of dietary restriction on in vivo somatic mutation in mice Mutat. Res. 291 1993 141 145
19. R.A. DePinho The age of cancer Nature 408 2000 248 254
20. M.J. Difilippantonio, J. Zhu, H.T. Chen, E. Meffre, M.C. Nussenzweig, E.E. Max, T. Ried, and A. Nussenzweig DNA repair protein Ku80 suppresses chromosomal aberratons and malignant transformation Nature 404 2000 510 514
21. M.E.T. Dolle, H. Giese, C.L. Hopkins, H.-J. Martus, J.M. Hausdorf, and J. Vijg Rapid accumulation of genome rearrangements in liver but not in brain of old mice Nat. Genet. 17 1997 431 434
22. M.E.T. Dolle, W.K. Snyder, J.A. Gossen, P.H.M. Lohman, and J. Vijg Distinct spectra of somatic mutations accumulated with age in mouse heart and small intestine Proc. Natl. Acad. Sci. U.S.A. 97 2000 8403 8408
23. C. Dudenhoffer, M. Kurth, F. Janus, W. Depport, and L. Wiesmuller p53 domains involved in the control of recombination Oncogene 18 1999 5773 5784
24. M. Dumble, C. Gatza, S. Tyner, S. Venkatachalam, and L.A. Donehower Insights into aging obtained from p53 mutant mouse models Ann. N. Y. Acad. Sci. 1019 2004 171 177
25. C.J. Epstein, G.M. Martin, A.L. Schultz, and A.G. Motulsky Werner's syndrome a review of its symptomatology, natural history, pathologic features, genetics and relationship to the natural aging process Medicine (Baltimore) 45 1966 177 221
26. S. Espejel, M. Martin, P. Klatt, J. Martin-Caballero, J.M. Flores, and M.A. Blasco Shorter telomeres, accelerated ageing and increased lymphoma in DNA-PKcs-deficient mice EMBO Rep. 5 2004 503 509
27. M.G. Ferreira, and J.P. Cooper Two modes of DNA double-strand break repair are reciprocally regulated through the fission yeast cell cycle Genes Dev. 18 2004 2249 2254
28. B.A. Finette, L.M. Sullivan, J.P. O'Neill, J.A. Nicklas, P.M. Vacek, and R.J. Albertini Determination of hprt mutant frequencies in T-lymphocytes from a healthy pediatric population: statistical comparison between newborn, children and adult mutant frequencies, cloning efficiency and age Mutat. Res. 308 1994 223 231
29. Fry, M., 2002. The Werner syndrome helicase-nuclease - one protein, many mysteries. Sci. Aging Knowl. Environ. 2002, re2.
30. K. Fukuchi, G.M. Martin, and R.J. Monnat Mutator phenotype of Werner syndrome is characterized by extensive deletions Proc. Natl. Acad. Sci. U.S.A. 86 1989 5893 5897
31. V. Gorbunova, and A.A. Levy Nonhomologous DNA end joining in plant cells is associated with deletions and filler DNA insertions Nucleic Acids Res. 25 1997 4650 4657
32. M. Goto Hierarchical deterioration of body systems in Werner's syndrome: implications for normal ageing Mech. Ageing Dev. 98 1997 239 254
33. S.A. Grist, M. McCarron, A. Kutlaca, D.R. Turner, and A.A. Morley In vivo human somatic mutation: frequency and spectrum with age Mutat. Res. 266 1992 189 196
34. T. Helleday Pathways for mitotic homologous recombination in mammalian cells Mutat. Res. 532 2003 103 115
35. I.D. Hickson RecQ helicases: caretakers of the genome Nat. Rev. Cancer 3 2003 169 178
36. K. Itahana, G. Dimri, and J. Campisi Regulation of cellular senescence by p53 Eur. J. Biochem. 268 2001 2784 2791
37. S.P. Jackson Sensing and repairing DNA double-strand breaks Carcinogenesis 23 2002 687 696
38. R.D. Johnson, and M. Jasin Double-strand-break-induced homologous recombination in mammalian cells Biochem. Soc. Trans. 29 2001 196 201
39. I.M. Jones, C.B. Thomas, B. Tucker, C.L. Thompson, P. Pleshanov, I. Vorobtsova, and D.H. Moore II Impact of age and environment on somatic mutation at the hprt gene of T lymphocytes in humans Mutat. Res. 338 1995 129 139
40. P. Karmakar, J. Piotrowski, R.M. Brosh Jr., J.A. Sommers, S.P. Miller, W.H. Cheng, C.M. Snowden, D.A. Ramsden, and V.A. Bohr Werner protein is a target of DNA-dependent protein kinase in vivo and in vitro, and its catalytic activities are regulated by phosphorylation J. Biol. Chem. 277 2002 18291 18302
41. P. Karmakar, C.M. Snowden, D.A. Ramsden, and V.A. Bohr Ku heterodimer binds to both ends of the Werner protein and functional interaction occurs at the Werner N-terminus Nucleic Acids Res. 30 2002 3583 3591
42. K.K. Khanna, and S.P. Jackson DNA double-strand breaks: signaling, repair and the cancer connection Nat. Genet. 27 2001 247 254
43. L.J. Ko, and C. Prives p53: puzzle and paradigm Genes Dev. 10 1996 1054 1072
44. S.W. Kohler, G.S. Provost, A. Fieck, P.L. Kretz, W.O. Bullock, J.A. Sorge, D.L. Putman, and J.M. Short Spectra of spontaneous and mutagen-induced mutations in the LacI gene in transgenic mice Proc. Natl. Acad. Sci. U.S.A. 88 1991 7958 7962
45. I. Kruger, K. Rothkamm, and M. Lobrich Enhanced fidelity for rejoining radiation-induced DNA double-strand breaks in the G2 phase of Chinese hamster ovary cells Nucleic Acids Res. 32 2004 2677 2684
46. A.J. Levine p53, the cellular gatekeeper for growth and division Cell 88 1997 323 331
47. B. Li, and L. Comai Functional interaction between Ku and the werner syndrome protein in DNA end processing J. Biol. Chem. 275 2000 28349 28352
48. F. Liang, M. Han, P.J. Romanienko, and M. Jasin Homology-directed repair is a major double strand break repair pathway in mammalian cells Proc. Natl. Acad. Sci. U.S.A. 95 1998 5172 5177
49. M.R. Lieber The biochemistry and biological significance of nonhomologous DNA end joining: an essential repair process in multicellular eukaryotes Genes Cells 4 1999 77 85
50. M.R. Lieber, Y. Ma, U. Pannicke, and K. Schwarz Mechanism and regulation of human non-homologous DNA end-joining Nat. Rev., Mol. Cell. Biol. 4 2003 712 720
51. Y. Lin, and A.S. Waldman Capture of DNA sequences at double strand breaks in mammalian chromosomes Genetics 195 2001 1665 1674
52. Y. Lin, and A.S. Waldman Promiscuous patching of broken chromosomes in mammalian cells with extrachromosomal DNA Nucleics Acids Res. 29 2001 3975 3981
53. Y. Lin, B.C. Waldman, and A.S. Waldman Suppression of high-fidelity double-strand break repair in mammalian chromosomes by pifithrin-alpha, a chemical inhibitor of p53 DNA Repair (Amst.) 2 2003 1 11
54. B. Maier, W. Gluba, B. Bernier, T. Turner, K. Mohammad, T. Guise, A. Sutherland, M. Thorner, and H. Scrable Modulation of mammalian life span by the short isoform of p53 Genes Dev. 18 2004 306 319
55. G.M. Martin, A.C. Smith, D.J. Ketterer, C.E. Ogburn, and C.M. Disteche Increased chromosomal aberrations in first metaphases of cells isolated from the kidneys of aged mice Isr. J. Med. Sci. 21 1985 296 301
56. M.A. McMurray, and D.E. Gottschling An age-induced switch to a hyper-recombinational state Science 301 2003 1908 1911
57. K.L. Mekeel, W. Tang, L.A. Kachnic, C.-M. Luo, J.S. DeFrank, and S.N. Powell Inactivation of p53 results in high rates of homologous recombination Oncogene 14 1997 1847 1857
58. Monnat, R.J., Jr., Saintigny, Y., 2004. Werner syndrome protein - unwinding function to explain disease. Sci. Aging Knowl. Environ. 2004, re3.
59. A. Morley Somatic mutation and aging Ann. N. Y. Acad. Sci. 854 1998 20 22
60. A.A. Morley, S. Cox, and R. Holliday Human lymphocytes resistant to 6-thioguanine increase with age Mech. Ageing Dev. 19 1982 21 26
61. L.J. Niedernhofer, H. Odijk, M. Budzowska, E. van Drunen, A. Maas, A.F. Theil, J. de Wit, N.G. Jaspers, H.B. Beverloo, J.H. Hoeijmakers, and R. Kanaar The structure-specific endonuclease Ercc1-Xpf is required to resolve DNA interstrand cross-link-induced double-strand breaks Mol. Cell. Biol. 24 2004 5776 5787
62. P.C. Nowell The clonal evolution of tumor cell populations Science 194 1976 23 28
63. A.L. Okorokov, L. Warnock, and J. Milner Effect of wild-type, S15D and R175H p53 proteins on DNA end joining in vitro: potential mechanism of DNA double-strand break repair modulation Carcinogenesis 23 2002 549 557
64. P.L. Opresko, W.H. Cheng, C. von Kobbe, J.A. Harrigan, and V.A. Bohr Werner syndrome and the function of the Werner protein; what they can teach us about the molecular aging process Carcinogenesis 24 2003 791 802
65. D.K. Orren, A. Machwe, P. Karmakar, J. Piotrowski, M.P. Cooper, and V.A. Bohr A functional interaction of Ku with Werner exonuclease facilitates digestion of damaged DNA Nucleic Acids Res. 29 2001 1926 1934
66. J. Oshima, S. Huang, C. Pae, J. Campisi, and R.H. Schiestl Lack of WRN results in extensive deletion at nonhomologous joining ends Cancer Res. 62 2002 547 551
67. T.T. Paull, E.P. Rogakou, V. Yamazaki, C.U. Kirchgessner, M. Gellert, and W.M. Bonner A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage Curr. Biol. 10 2000 886 895
68. P.R. Prince, M.J. Emond, and R.J. Monnat Jr. Loss of Werner syndrome protein function promotes aberrant mitotic recombination Genes Dev. 15 2001 933 938
69. M.J. Ramsey, D.H. Moore, J.F. Briner, D.A. Lee, L.A. Olsen, J.R. Senft, and J.D. Tucker The effects of age and lifestyle factors on the accumulation of cytogenetic damage as measured by chromosome painting Mutat. Res. 338 1995 95 106
70. K. Ren, and S.P. de Ortiz Non-homologous DNA end joining in the mature rat brain J. Neurochem. 80 2002 949 959
71. E.P. Rogakou, C. Boon, C. Redon, and W.M. Bonner Megabase chromatin domains involved in DNA double-strand breaks in vivo J. Cell Biol. 146 1999 905 916
72. K. Rothkamm, I. Kruger, L.H. Thompson, and M. Lobrich Pathways of DNA double-strand break repair during the mammalian cell cycle Mol. Cell. Biol. 23 2003 5706 5715
73. K.L. Rudolph, S. Chang, H.W. Lee, M. Blasco, G.J. Gottlieb, C. Greider, and R.A. DePinho Longevity, stress response, and cancer in aging telomerase-deficient mice Cell 96 1999 701 712
74. S. Sakamoto, K. Nishikawa, S.J. Heo, M. Goto, Y. Furuichi, and A. Shimamoto Werner helicase relocates into nuclear foci in response to DNA damaging agents and co-localizes with RPA and Rad51 Genes Cells 6 2001 421 430
75. N. Saleh-Gohari, and T. Helleday Conservative homologous recombination preferentially repairs DNA double-strand breaks in the S phase of the cell cycle in human cells Nucleic Acids Res. 32 2004 3683 3688
76. R.G. Sargent, M.A. Branneman, and J.H. Wilson Repair of site-specific double-strand breaks in mammalian chromosome by homologous and illegitimate recombination Mol. Cell. Biol. 17 1997 267 277
77. O.A. Sedelnikova, I. Horikawa, D.B. Zimonjic, N.C. Popescu, W.M. Bonner, and J.C. Barrett Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks Nat. Cell Biol. 6 2004 168 170
78. A. Seluanov, V. Gorbunova, A. Falcovitz, A. Sigal, M. Milyavsky, I. Zurer, G. Shohat, N. Goldfinger, and V. Rotter Change of the death pathway in senescent human fibroblasts in response to DNA damage is caused by an inability to stabilize p53 Mol. Cell. Biol. 21 2001 1552 1564
79. A. Seluanov, D. Mittelman, O.M. Pereira-Smith, J.H. Wilson, and V. Gorbunova DNA end joining becomes less efficient and more error-prone during cellular senescence Proc. Natl. Acad. Sci. U.S.A. 101 2004 7624 7629
80. Y. Shiloh ATM and ATR: networking callular responses to DNA damage Curr. Opin. Genet. Dev. 11 2001 71 77
81. Y. Shiloh, and M.B. Kastan ATM: genome stability, neuronal development, and cancer cross paths Adv. Cancer Res. 83 2001 209 254
82. Y. Shiloh, E. Tabor, and Y. Becker Colony-forming ability of ataxia-telangiectasia skin fibroblasts is an indicator of their early senescence and increased demand for growth factors Exp. Cell Res. 140 1982 191 199
83. N.P. Singh, C.E. Ogburn, N.S. Wolf, G. van Belle, and G.M. Martin DNA double-strand breaks in mouse kidney cells with age Biogerontology 2 2001 261 270
84. A. Smogorzewska, and T. de Lange Different telomere damage signaling pathways in human and mouse cells EMBO J. 21 2002 4338 4348
85. G.R. Stuart, and B.W. Glickman Through a glass, darkly: reflections of mutation from lacI transgenic mice Genetics 155 2000 1359 1367
86. G.R. Stuart, Y. Oda, J.G. de Boer, and B.W. Glickman Mutation frequency and specificity with age in liver, bladder and brain of lacI transgenic mice Genetics 154 2000 1291 1300
87. Y. Suh Cell signaling in aging and apoptosis Mech. Ageing Dev. 123 2002 881 890
88. Y. Suh, K.A. Lee, W.H. Kim, B.G. Han, J. Vijg, and S.C. Park Aging alters the apoptotic response to genotoxic stress Nat. Med. 8 2002 3 4
89. H. Takai, A. Smogorzewska, and T. de Lange DNA damage foci at dysfunctional telomeres Curr. Biol. 13 2003 1549 1556
90. W. Tang, H. Willers, and S.N. Powell p53 directly enhances rejoining of DNA double-strand breaks with cohesive ends in gamma-irradiated mouse fibroblasts Cancer Res. 59 1999 2562 2565
91. J.D. Tucker, M.D. Spruill, M.J. Ramsey, A.D. Director, and J. Nath Frequency of spontaneous chromosome aberrations in mice: effects of age Mutat. Res. 425 1999 135 141
92. S.D. Tyner, S. Venkatachalam, J. Choi, S. Jones, N. Ghebranious, H. Igelmann, X. Lu, G. Soron, B. Cooper, C. Brayton, S. Hee Park, T. Thompson, G. Karsenty, A. Bradley, and L.A. Donehower p53 mutant mice that display early ageing-associated phenotypes Nature 415 2002 45 53
93. J. Vijg Somatic mutations and aging: a re-evaluation Mutat. Res. 447 2000 117 135
94. J. Vijg Impact of genome instability on transcription regulation of aging and senescence Mech. Ageing Dev. 125 2004 747 753
95. J. Vijg, and M.E.T. Dolle Large genome rearrangements as a primary cause of aging Mech. Ageing Dev. 123 2002 907 915
96. J. Vijg, M.E.T. Dolle, H.-J. Martus, and M.E.T.I. Boerrigter Transgenic mouse models for studing mutations in vivo: applications in aging research Mech. Ageing Dev. 98 1997 189 202
97. H. Vogel, D.S. Lim, J. Karsenty, M. Finegold, and P. Hasty Deletion of Ku 86 cases erly onset of senescence in mice Proc. Natl. Acad. Sci. U.S.A. 96 1999 10770 10775
98. T. von Zglinicki, G. Saretzki, J. Ladhoff, F. d'Adda di Fagagna, and S.P. Jackson Human cell senescence as a DNA damage response Mech. Ageing Dev. 126 1 2005 111 117
99. K. Webley, J. Bond, C. Jones, J. Blaydes, A. Craig, T. Hupp, and D. Wynford-Thomas Posttranslational modification of p53 in replicative senescence overlapping but distinct from those induced by DNA damage Mol. Cell. Biol. 20 2000 2803 2808
100. G. Weeda, I. Donker, J. de Wit, H. Morreau, R. Janssens, C.J. Vissers, A. Nigg, H. van Steeg, D. Bootsma, and J.H. Hoeijmakers Disription of mouse ERCC1 results in novel repair syndrome with growth failure, nulear abnormalities and senescence Curr. Biol. 7 1997 427 439
101. S.J. Xia, M.A. Shammas, and R.J. Shmookler Reis Elevated recombination in immortal human cells is mediated by hsRAD51 recombinase Mol. Cell. Biol. 17 1997 7151 7158
102. S.M. Yannone, S. Roy, D.W. Chan, M.B. Murphy, S. Huang, J. Campisi, and D.J. Chen Werner syndrome protein is regulated and phosphorylated by DNA-dependent protein kinase J. Biol. Chem. 276 2001 38242 38248
103. B.B.S. Zhou, and S.J. Elledge The DNA damage response: putting checkpoints in perspective Nature 408 2000 433 439