Cellular responses to DNA damage: One signal, multiple choices

Annual Review of Genetics

Volumn 40, Issue , 2006, Pages 187-208

  Su, Tin Tin ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Apoptosis; Checkpoints; DNA damage; DNA repair

Indexed keywords

DOUBLE STRANDED DNA;

APOPTOSIS; CELL CYCLE; CELL DIVISION; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TELOMERE;

ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; GENES, CDC; HUMANS; SIGNAL TRANSDUCTION; TELOMERE;

EID: 33845627082     PISSN: 00664197     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.genet.40.110405.090428     Document Type: Review

References (114)

1. Andrews EA, Palecek J, Sergeant J, Taylor E, Lehmann AR, Watts FZ. 2005. Nse2, a component of the Smc5-6 complex, is a SUMO ligase required for the response to DNA damage. Mol. Cell Biol. 25:185-96
2. Aten JA, Stap J, Krawczyk PM, van Oven CH, Hoebe RA, et al. 2004. Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 303:92-95
3. Bakkenist CJ, Kastan MB. 2003. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421:499-506
4. Bao S, Tibbetts RS, Brumbaugh KM, Fang Y, Richardson DA, et al. 2001. ATR/ATM-mediated phosphorylation of human Rad17 is required for genotoxic stress responses. Nature 411:969-74
5. Bekker-Jensen S, Lukas C, Melander F, Bartek J, Lukas J. 2005. Dynamic assembly and sustained retention of 53BP1 at the sites of DNA damage are controlled by Mdc1/NFBD1. J. Cell Biol. 170:201-11
6. Brodsky MH, Weinert BT, Tsang G, Rong YS, McGinnis NM, et al. 2004. Drosophila melanogaster MNK/Chk2 and p53 regulate multiple DNA repair and apoptotic pathways following DNA damage. Mol. Cell Biol. 24:1219-31
7. Burma S, Chen BP, Murphy M, Kurimasa A, Chen DJ. 2001. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem. 276:42462-67
8. Canman CE, Lim DS, Cimprich KA, Taya Y, Tamai K, et al. 1998. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281:1677-79
9. Carson CT, Schwartz RA, Stracker TH, Lilley CE, Lee DV, Weitzman MD. 2003. The Mre11 complex is required for ATM activation and the G2/M checkpoint. EMBO J. 22:6610-20
10. Deleted in proof
11. Celeste A, Fernandez-Capetillo O, Kruhlak MJ, Pilch DR, Staudt DW, et al. 2003. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol. 5:675-79
12. Celeste A, Petersen S, Romanienko PJ, Fernandez-Capetillo O, Chen HT, et al. 2002. Genomic instability in mice lacking histone H2AX. Science 296:922-27
13. Chan TA, Hermeking H, Lengauer C, Kinzler KW, Vogelstein B. 1999. 14-3-3 Sigma is required to prevent mitotic catastrophe after DNA damage. Nature 401:616-20
14. 1 by stabilizing p53. Genes Dev. 14:278-88
15. Chen G, Yuan SS, Liu W, Xu Y, Trujillo K, et al. 1999. Radiation-induced assembly of Rad51 and Rad52 recombination complex requires ATM and c-Abl. J. Biol. Chem. 274:12748-52
16. Chipuk JE, Green DR. 2004. Cytoplasmic p53: bax and forward. Cell Cycle 3:429-31
17. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, et al. 2004. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 303:1010-14
18. Chowdhury D, Keogh MC, Ishii H, Peterson CL, Buratowski S, Lieberman J. 2005. gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol. Cell 20:801-9
19. Cohen-Fix O, Koshland D. 1997. The anaphase inhibitor of Saccharomyces cerevisiae Pds1p is a target of the DNA damage checkpoint pathway. Proc. Natl. Acad. Sci. USA 94:14361-66
20. Costanzo V, Paull T, Gottesman M, Gautier J. 2004. Mre11 assembles linear DNA fragments into DNA damage signaling complexes. PLoS Biol. 2: E110
21. Costanzo V, Robertson K, Ying CY, Kim E, Avvedimento E, et al. 2000. Reconstitution of an ATM-dependent checkpoint that inhibits chromosomal DNA replication following DNA damage. Mol. Cell 6:649-59
22. Costanzo V, Shechter D, Lupardus PJ, Cimprich KA, Gottesman M, Gautier J. 2003. An ATR- and Cdc7-dependent DNA damage checkpoint that inhibits initiation of DNA replication. Mol. Cell 11:203-13
23. de Vries HI, Uyetake L, Lemstra W, Brunsting JF, Su TT, et al. 2005. Grp/DChk1 is required for G2-M checkpoint activation in Drosophila S2 cells, whereas Dmnk/DChk2 is dispensable. J. Cell Sci. 118:1833-42
24. Digweed M, Rothe S, Demuth I, Scholz R, Schindler D, et al. 2002. Attenuation of the formation of DNA-repair foci containing RAD51 in Fanconi anaemia. Carcinogenesis 23:1121-26
25. Downs JA, Lowndes NF, Jackson SP. 2000. A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 408:1001-4
26. Duck P, Nasim A, James AP. 1976. Temperature-sensitive mutant of Schizosaccharomyces pombe exhibiting enhanced radiation sensitivity. J. Bacteriol. 128:536-39
27. Dupre A, Boyer-Chatenet L, Gautier H. 2006. Two-step activation of ATM by DNA and the Mre11-Rad50-Nbs1 complex. Nat. Struct. Mol. Biol. 13:451-57
28. Espinosa JM, Verdun RE, Emerson BM. 2003. p53 functions through stress- and promoter-specific recruitment of transcription initiation components before and after DNA damage. Mol. Cell 12:1015-27
29. Falck J, Coates J, Jackson SP. 2005. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434:605-11
30. Falck J, Mailand N, Syljuasen RG, Bartek J, Lukas J. 2001. The ATM-Chk2-Cdc25A checkpoint pathway guards against radioresistant DNA synthesis. Nature 410:842-47
31. Fei P, El-Deiry WS. 2003. P53 and radiation responses. Oncogene 22:5774-83
32. Fernandez-Capetillo O, Chen HT, Celeste A, Ward I, Romanienko PJ, et al. 2002. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 4:993-97
33. Fogarty P, Campbell SD, Abu-Shumays R, Phalle BS, Yu KR, et al. 1997. The Drosophila grapes gene is related to checkpoint gene chk1/rad21 and is required for late syncytial division fidelity. Curr. Biol. 7:418-26
34. Friedl AA, Beisker W, Hahn K, Eckardt-Schupp F, Kellerer AM. 1993. Application of pulsed field gel electrophoresis to determine gamma-ray-induced double-strand breaks in yeast chromosomal molecules. Int. J. Radiat. Biol. 63:173-81
35. Game JC, Williamson MS, Baccari C. 2005. X-ray survival characteristics and genetic analysis for nine Saccharomyces deletion mutants that show altered radiation sensitivity. Genetics 169:51-63
36. Garcia-Higuera I, Taniguchi T, Ganesan S, Meyn MS, Timmers C, et al. 2001. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol. Cell 7:249-62
37. Goldberg M, Stucki M, Falck J, D'Amours D, Rahman D, et al. 2003. MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature 421:952-56
38. Gomes NP, Bjerke G, Llorente B, Szostek SA, Emerson BM, Espinosa JM. 2006. Gene-specific requirement for P-TEFb activity and RNA polymerase II phosphorylation within the p53 transcriptional program. Genes Dev. 20:601-12
39. Hari KL, Santerre A, Sekelsky JJ, McKim KS, Boyd JB, Hawley RS. 1995. The mei-41 gene of D. melanogaster is a structural and functional homolog of the human ataxia telangiectasia gene. Cell 82:815-21
40. Harrison J, Haber JE. 2006. Surviving the breakup: the DNA damage checkpoint. Annu. Rev. Genet. 40:209-35
41. Herbig U, Jobling WA, Chen BP, Chen DJ, Sedivy JM. 2004. Telomere shortening triggers senescence of human cells through a pathway involving ATM, p53, and p21(CIP1), but not p16(INK4a). Mol. Cell 14:501-13
42. Hut HM, Lemstra W, Blaauw EH, Van Cappellen GW, Kampinga HH, Sibon OC. 2003. Centrosomes split in the presence of impaired DNA integrity during mitosis. Mol. Biol. Cell 14:1993-2004
43. Huyen Y, Zgheib O, Ditullio RAJ, Gorgoulis VG, Zacharatos P, et al. 2004. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432:406-11
44. Ira G, Pellicioli A, Balijja A, Wang X, Fiorani S, et al. 2004. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431:1011-17
45. Irwin M, Marin MC, Phillips AC, Seelan RS, Smith DI, et al. 2000. Role for the p53 homologue p73 in E2F-1-induced apoptosis. Nature 407:645-48
46. Jaklevic BR, Su TT. 2004. Relative contribution of DNA repair, cell cycle checkpoints, and cell death to survival after DNA damage in Drosophila larvae. Curr. Biol. 14:23-32
47. Jazayeri A, Falck J, Lukas C, Bartek J, Smith GC, et al. 2006. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol. 8:37-45
48. Jin J, Shirogane T, Xu L, Nalepa G, Qin J, et al. 2003. SCFbeta-TRCP links Chk1 signaling to degradation of the Cdc25A protein phosphatase. Genes Dev. 17:3062-74
49. Karlseder J, Hoke K, Mirzoeva OK, Bakkenist C, Kastan MB, et al. 2004. The telomeric protein TRF2 binds the ATM kinase and can inhibit the ATM-dependent DNA damage response. PLoS Biol. 2:E240
50. Keogh MC, Kim JA, Downey M, Fillingham J, Chowdhury D, et al. 2006. A phosphatase complex that dephosphorylates gammaH2AX regulates DNA damage checkpoint recovery. Nature 439:497-501
51. Kim JS, Krasieva TB, LaMorte V, Taylor AM, Yokomori K. 2002. Specific recruitment of human cohesin to laser-induced DNA damage. J. Biol. Chem. 277:45149-53
52. Kitagawa R, Bakkenist CJ, McKinnon PJ, Kastan MB. 2004. Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev. 18:1423-38
53. Kruhlak MJ, Celeste A, Dellaire G, Fernandez-Capetillo O, Muller WG, et al. 2006. Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J. Cell Biol. 172:823-34
54. Kumagai A, Lee J, Yoo HY, Dunphy WG. 2006. TopBP1 activates the ATR-ATRIP complex. Cell 124:943-55
55. Laurencon A, Purdy A, Sekelsky J, Hawley RS, Su TT. 2003. Phenotypic analysis of separation-of-function alleles of MEI-41, Drosophila ATM/ATR. Genetics 164:589-601
56. Lee JH, Paull TT. 2005. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308:551-54
57. Leith JT, Dexter DL, DeWyngaert JK, Zeman EM, Chu MY, et al. 1982. Differential responses to x-irradiation of subpopulations of two heterogeneous human carcinomas in vitro. Cancer Res. 42:2556-61
58. Li J, Stern DF. 2005. DNA damage regulates Chk2 association with chromatin. J. Biol. Chem. 280:37948-56
59. Li L, Zou L. 2005. Sensing, signaling, and responding to DNA damage: organization of the checkpoint pathways in mammalian cells. J. Cell Biochem. 94:298-306
60. Lisby M, Barlow JH, Burgess RC, Rothstein R. 2004. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118:699-713
61. Lisby M, Mortensen UH, Rothstein R. 2003. Colocalization of multiple DNA double-strand breaks at a single Rad52 repair center. Nat. Cell Biol. 5:572-77
62. Liu K, Luo Y, Lin FT, Lin WC. 2004. TopBP1 recruits Brg1/Brm to repress E2F1-induced apoptosis, a novel pRb-independent and E2F1-specific control for cell survival. Genes Dev. 18:673-86
63. Llorente B, Symington LS. 2004. The Mre11 nuclease is not required for 5′ to 3′ resection at multiple HO-induced double-strand breaks. Mol. Cell Biol. 24:9682-94
64. Lukas J, Lukas C, Bartek J. 2004. Mammalian cell cycle checkpoints: signaling pathways and their organization in space and time. DNA Repair 3:997-1007
65. Mailand N, Falck J, Lukas C, Syljuasen RG, Welcker M, et al. 2000. Rapid destruction of human Cdc25A in response to DNA damage. Science 288:1425-29
66. Maya R, Balass M, Kim ST, Shkedy D, Leal JF, et al. 2001. ATM-dependent phosphorylation of Mdm2 on serine 395: role in p53 activation by DNA damage. Genes Dev. 15:1067-77
67. Michelson RJ, Rosenstein S, Weinert T. 2005. A telomeric repeat sequence adjacent to a DNA double-stranded break produces an anticheckpoint. Genes Dev. 19:2546-59
68. Mikhailov A, Cole RW, Rieder CL. 2002. DNA damage during mitosis in human cells delays the metaphase/anaphase transition via the spindle-assembly checkpoint. Curr. Biol. 12:1797-806
69. Mirzaie-Joniani H, Eriksson D, Johansson A, Lofroth PO, Johansson L, et al. 2002. Apoptosis in HeLa Hep2 cells is induced by low-dose, low-dose-rate radiation. Radiat. Res. 158:634-40
70. Mochan TA, Venere M, DiTullio RAJ, Halazonetis TD. 2003. 53BP1 and NFBD1/MDC1-Nbs1 function in parallel interacting pathways activating ataxia-telangiectasia mutated (ATM) in response to DNA damage. Cancer Res. 63:8586-91
71. Moreno-Herrero F, de Jager M, Dekker NH, Kanaar R, Wyman C, Dekker C. 2005. Mesoscale conformational changes in the DNA-repair complex Rad50/Mre11/Nbs1 upon binding DNA. Nature 437:440-43
72. Niida H, Nakanishi M. 2006. DNAdamage checkpoints in mammals. Mutagenesis 21:3-9
73. Pilch DR, Sedelnikova OA, Redon C, Celeste A, Nussenzweig A, Bonner WM. 2003. Characteristics of gamma-H2AX foci at DNA double-strand breaks sites. Biochem. Cell Biol. 81:123-29
74. Purdy A, Su TT. 2004. Telomeres: Not all breaks are equal. Curr. Biol. 14:R613-14
75. Rich T, Allen RL, Wyllie AH. 2000. Defying death after DNA damage. Nature 407:777-83
76. Rogakou EP, Boon C, Redon C, Bonner WM. 1999. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146:905-16
77. 75a. Ruiz de Almodovar JM, Steel GG, Whitaker SJ, McMillan TJ. 1994. A comparison of methods for calculating DNA double-strand break induction frequency in mammalian cells by pulsed-field gel electrophoresis. Int. J. Radiat. Biol. 65:641-49
78. Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S. 2004. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73:39-85
79. Sanchez Y, Bachant J, Wang H, Hu F, Liu D, et al. 1999. Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. Science 286:1166-71
80. Sanders SL, Portoso M, Mata J, Bahler J, Allshire RC, Kouzarides T. 2004. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 119:603-14
81. Shieh SY, Ahn J, Tamai K, Taya Y, Prives C. 2000. The human homologs of checkpoint kinases Chk1 and Cds1 (Chk2) phosphorylate p53 at multiple DNA damage-inducible sites. Genes Dev. 14:289-300
82. Shroff R, Arbel-Eden A, Pilch D, Ira G, Bonner WM, et al. 2004. Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr. Biol. 14:1703-11
83. Sibon OC, Laurencon A, Hawley R, Theurkauf WE. 1999. The Drosophila ATM homologue Mei-41 has an essential checkpoint function at the midblastula transition. Curr. Biol. 9:302-12
84. Sibon OC, Stevenson VA, Theurkauf WE. 1997. DNA-replication checkpoint control at the Drosophila midblastula transition. Nature 388:93-97
85. Slee EA, O'Connor DJ, Lu X. 2004. To die or not to die: How does p53 decide? Oncogene 23:2809-18
86. Smits VA, Klompmaker R, Arnaud L, Rijksen G, Nigg EA, Medema RH. 2000. Polo-like kinase-1 is a target of the DNA damage checkpoint. Nat. Cell Biol. 2:672-76
87. Smits VA, Reaper PM, Jackson SP. 2006. Rapid PIKK-dependent release of Chk1 from chromatin promotes the DNA-damage checkpoint response. Curr. Biol. 16:150-59
88. Stevens C, La Thangue NB. 2004. The emerging role of E2F-1 in the DNA damage response and checkpoint control. DNA Repair 3:1071-79
89. Stewart GS, Wang B, Bignell CR, Taylor AM, Elledge SJ. 2003. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421:961-66
90. Strom L, Lindroos HB, Shirahige K, Sjogren C. 2004. Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol. Cell 16:1003-15
91. Stucki M, Clapperton JA, Mohammad D, Yaffe MB, Smerdon SJ, Jackson SP. 2005. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123:1213-26
92. Stucki M, Jackson SP. 2006. gammaH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair 5:534-43
93. Su TT, Jaklevic B. 2001. DNA damage leads to a cyclin A-dependent delay in metaphase-anaphase transition in the Drosophila gastrula. Curr. Biol. 11:8-17
94. Su TT, Walker J, Stumpff J. 2000. Activating the DNA damage checkpoint in a developmental context. Curr. Biol. 10:119-26
95. Sweeney FD, Yang F, Chi A, Shabanowitz J, Hunt DF, Durocher D. 2005. Saccharomyces cerevisiae Rad9 acts as a Mec1 adaptor to allow Rad53 activation. Curr. Biol. 15:1364-75
96. Takada S, Kelkar A, Theurkauf WE. 2003. Drosophila checkpoint kinase 2 couples centrosome function and spindle assembly to genomic integrity. Cell 113:87-99
97. Takai H, Smogorzewska A, de Lange T. 2003. DNA damage foci at dysfunctional telomeres. Curr. Biol. 13:1549-56
98. Theunissen JW, Kaplan MI, Hunt PA, Williams BR, Ferguson DO, et al. 2003. Checkpoint failure and chromosomal instability without lymphomagenesis in Mre11(ATLD1/ATLD1) mice. Mol. Cell 12:1511-23
99. Tibbetts RS, Cortez D, Brumbaugh KM, Scully R, Livingston D, et al. 2000. Functional interactions between BRCA1 and the checkpoint kinase ATR during, genotoxic stress. Genes Dev. 14:2989-3002
100. Tsai MH, Chen X, Chandramouli GV, Chen Y, Yan H, et al. 2006. Transcriptional responses to ionizing radiation reveal that p53R2 protects against radiation-induced mutagenesis in human lymphoblastoid cells. Oncogens 25:622-32
101. Tsukuda T, Fleming AB, Nickoloff JA, Osley MA. 2005. Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 438:379-83
102. Unal E, Arbel-Eden A, Sattler U, Shroff R, Lichten M, et al. 2004. DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol. Cell 16:991-1002
103. Urist M, Tanaka T, Poyurovsky MV, Prives C. 2004. p73 induction after DNA damage is regulated by checkpoint kinases Chk1 and Chk2. Genes Dev. 18:3041-54
104. Uziel T, Lerenthal Y, Moyal L, Andegeko Y, Mittelman L, Shiloh Y. 2003. Requirement of the MRN complex for ATM activation by DNA damage. EMBO J. 22:5612-21
105. Ward IM, Minn K, Jorda KG, Chen J. 2003. Accumulation of checkpoint protein 53BP1 at DNA breaks involves its binding to phosphorylated histone H2AX. J. Biol. Chem. 278:19579-82
106. Wolner B, van Komen S, Sung P, Peterson CL. 2003. Recruitment of the recombinational repair machinery to a DNA double-strand break in yeast. Mol. Cell 12:221-32
107. Wu WS, Heinrichs S, Xu D, Garrison SP, Zambetti GP, et al. 2005. Slug antagonizes p53-mediated apoptosis of hematopoietic progenitors by repressing puma. Cell 123:641-53
108. Xu X, Stern DF. 2003. NFBD1/MDC1 regulates ionizing radiation-induced focus formation by DNA checkpoint signaling and repair factors. FASEB J. 17:1842-48
109. Yamane K, Wu X, Chen J. 2002. A DNA damage-regulated BRCT-containing protein, TopBP1, is required for cell survival. Mol. Cell Biol. 22:555-66
110. You Z, Chahwan C, Bailis J, Hunter T, Russell P. 2005. ATM activation and its recruitment to damaged DNA require binding to the C terminus of Nbs1. Mol. Cell Biol. 25:5363-79
111. Zhang W, Fletcher L, Muschel RJ. 2005. The role of Polo-like kinase 1 in the inhibition of centrosome separation after ionizing radiation. J. Biol. Chem. 280:42994-99
112. Zhou BB, Elledge SJ. 2000. The DNA damage response: putting checkpoints in perspective. Nature 408:433-39
113. Zou L, Elledge SJ. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542-48
114. Zou L, Liu D, Elledge SJ. 2003. Replication protein A-mediated recruitment and activation of Rad17 complexes. Proc. Natl. Acad. Sci. USA 100:13827-32