Low-dose DNA damage and replication stress responses quantified by optimized automated single-cell image analysis

Cell Cycle

Volumn 8, Issue 16, 2009, Pages 2592-2599

  Mistrik, Martin ^a,b   Oplustilova, Lenka ^a,b   Lukas, Jiri ^a   Bartek, Jiri ^a,b  

^a DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^b PALACKÝ UNIVERSITY   (Czech Republic)

Author keywords

Cancer cells; Cell cycle; DNA breakage repair kinetics; DNA damage; Homologous recombination; Image analysis; Rad51 foci; Replication stress; H2AX

Indexed keywords

HISTONE H2AX; RAD51 PROTEIN; REPLICATION FACTOR A;

ADHERENT CELL; ARTICLE; AUTOANALYSIS; CANCER CELL; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DNA STRAND BREAKAGE; FLUORESCENCE ANALYSIS; FLUORESCENCE MICROSCOPE; HIGH THROUGHPUT SCREENING; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IONIZING RADIATION; KINETICS; MICROCOMPUTER; RADIATION DOSE; SENSITIVITY ANALYSIS; STRESS;

EID: 69249232244     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.8.16.9331     Document Type: Article

References (55)

1. Hoeijmakers JH. Genome maintenance mechanisms for preventing cancer. Nature 2001; 411:366-374
2. Schumacher B, Garinis GA, Hoeijmakers JH. Age to survive: DNA damage and aging. Trends Genet 2008; 24:77-85.
3. Kastan MB, Bartek J. Cell cycle checkpoints and cancer. Nature 2004; 432:316-323
4. Harper JW, Elledge SJ. The DNA damage response: ten years after. Mol Cell 2007; 28:739-745 (Pubitemid 350217064)
5. Bartek J, Lukas J. DNA damage checkpoints: from initiation to recovery or adaptation. Curr Opin Cell Biol 2007; 19:238-245 (Pubitemid 46386406)
6. Jeggo PA, Lobrich M. DNA double strand breaks: their cellular and clinical impact? Oncogene 2007; 26:7717-7719
7. Stucki M, Jackson SP. γ-H2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair 2006; 5:534-543
8. Cimprich KA, Cortez D. ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 2008; 9:616-627 (Pubitemid 352032926)
9. Kinner A, Wu W, Staudt C, Iliakis G. Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res 2008; 36:5678-5694
10. Bartkova J, Bakkenist CJ, Rajpert-De ME, Skakkebaek NE, Sehested M, Lukas J, et al. ATM activation in normal human tissues and testicular cancer. Cell Cycle 2005; 4:838-845 (Pubitemid 41353838)
11. Bonner WM, Redon CE, Dickey JS, Nakamura AJ, Sedelnikova OA, Solier S, et al. GammaH2AX and cancer. Nat Rev Cancer 2008; 8:957-967
12. Bakkenist CJ, Kastan MB. Initiating cellular stress responses. Cell 2004; 118:9-17.
13. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998; 273:5858-5868
14. Hakem R. DNA-damage repair: the good, the bad and the ugly. EMBO J 2008; 27:589-605. (Pubitemid 351273123)
15. Fernandez-Capetillo O, Celeste A, Nussenzweig A. Focusing on foci: H2AX and the recruitment of DNA-damage response factors. Cell Cycle 2003; 2:426-427
16. Sedelnikova OA, Bonner WM. GammaH2AX in cancer cells: a potential biomarker for cancer diagnostics, prediction and recurrence. Cell Cycle 2006; 5:2909-2913
17. MacPhail SH, Banath JP, Yu TY, Chu EH, Lambur H, Olive PL. Expression of phosphorylated histone H2AX in cultured cell lines following exposure to X-rays. Int J Radiat Biol 2003; 79:351-358 (Pubitemid 36920536)
18. Tanaka T, Halicka HD, Traganos F, Seiter K, Darzynkiewicz Z. Induction of ATM activation, histone H2AX phosphorylation and apoptosis by etoposide: relation to cell cycle phase. Cell Cycle 2007; 6:371-376 (Pubitemid 46271585)
19. Albino AP, Huang X, Jorgensen E, Yang J, Gietl D, Traganos F, et al. Induction of H2AX phosphorylation in pulmonary cells by tobacco smoke: a new assay for carcinogens. Cell Cycle 2004; 3:1062-1068 (Pubitemid 40268666)
20. Bouquet F, Muller C, Salles B. The loss of gammaH2AX signal is a marker of DNA double strand breaks repair only at low levels of DNA damage. Cell Cycle 2006; 5:1116-1122 (Pubitemid 43765309)
21. Yu T, MacPhail SH, Banath JP, Klokov D, Olive PL. Endogenous expression of phosphorylated histone H2AX in tumors in relation to DNA double-strand breaks and genomic instability. DNA Repair 2006; 5:935-946 (Pubitemid 44160591)
22. Zhao H, Traganos F, Albino AP, Darzynkiewicz Z. Oxidative stress induces cell cycle dependent Mre11 recruitment, ATM and Chk2 activation and histone H2AX phosphorylation. Cell Cycle 2008; 7:1490-1495
23. Schultz LB, Chehab NH, Malikzay A, halazonetis TD. p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J Cell Biol 2000; 151:1381-1390 (Pubitemid 32047588)
24. Bekker-Jensen S, Lukas C, Kitagawa R, Melander F, Kastan MB, Bartek J, et al. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J Cell Biol 2006; 173:195-206.
25. Bekker-Jensen S, Lukas C, Melander F, Bartek J, Lukas J. Dynamic assembly and sustained retention of 53BP1 at the sites of DNA damage are controlled by Mdc1/NFBD1. J Cell Biol 2005; 170:201-211 (Pubitemid 41043803)
26. Lukas C, Falck J, Bartkova J, Bartek J, Lukas J. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat Cell Biol 2003; 5:255-260 (Pubitemid 36322254)
27. Kolas NK, Chapman JR, Nakada S, Ylanko J, Chahwan R, Sweeney FD, et al. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 2007; 318:1637-1640 (Pubitemid 350233664)
28. Mailand N, Bekker-Jensen S, Faustrup H, Melander F, Bartek J, Lukas C, et al. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 2007; 131:887-900. (Pubitemid 350138084)
29. Huen MS, Grant R, Manke I, Minn K, Yu X, Yaffe MB, Chen J. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 2007; 131:901-914 (Pubitemid 350138083)
30. Doil C, Mailand N, Bekker-Jensen S, Menard P, Larsen DH, Pepperkok R, et al. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 2009; 136:435-446
31. Stewart GS, Panier S, Townsend K, Al-Hakim AK, Kolas NK, Miller ES, et al. The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 2009; 136:420-434
32. Stewart GS. Solving the RIDDLE of 53BP1 recruitment to sites of damage. Cell Cycle 2009; 8:1532-1538
33. Yeykal CC, Greene EC. Visualizing the behavior of human Rad51 at the single-moleculelevel. Cell Cycle 2006; 5:1033-1038 (Pubitemid 43765294)
34. Warmerdam DO, Freire R, Kanaar R, Smits VAJ. Cell cycle-dependent processing of DNA lesions controls localization of Rad9 to sites of genotoxic stress. Cell Cycle 2009; 8:1765-1774
35. Muslimovic A, Ismail IH, Gao Y, Hammarsten O. An optimized method for measurement of gamma-H2AX in blood mononuclear and cultured cells. Nat Protoc 2008; 3:1187-1193
36. Elkind MM. Repair processes in radiation biology. Radiat Res 1984; 100:424-425
37. Burma S, Chen BP, Murphy M, Kurimasa A, Chen DJ. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J Biol Chem 2001; 276:42462-42467 (Pubitemid 37371158)
38. Falck J, Coates J, Jackson SP. Conserved modes of recruitment of ATM, ATR and DNAPKcs to sites of DNA damage. Nature 2005; 434:605-611
39. Stiff T, O'Driscoll M, Rief N, Iwabuchi K, Lobrich M, Jeggo PA. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res 2004; 64:2390-2396 (Pubitemid 38523891)
40. Pilch DR, Sedelnikova OA, Redon C, Celeste A, Nussenzweig A, Bonner WM. Characteristics of gamma-H2AX foci at DNA double-strand breaks sites. Biochem Cell Biol 2003; 81:123-129 (Pubitemid 37076234)
41. Bartek J, Lukas J, Bartkova J. DNA damage response as an anti-cancer barrier: damage threshold and the concept of 'conditional haploinsufficiency'. Cell Cycle 2007; 6:2344-2347
42. Halazonetis TD, Gorgoulis VG, Bartek J. An oncogene-induced DNA damage model for cancer development. Science 2008; 319:1352-1355 (Pubitemid 351354863)
43. DiTullio RA Jr, Mochan TA, Venere M, Bartkova J, Sehested M, Bartek J, et al. 53BP1 functions in an ATM-dependent checkpoint pathway that is constitutively activated in human cancer. Nat Cell Biol 2002; 4:998-1002. (Pubitemid 35469432)
44. Sorensen CS, Hansen LT, Dziegielewski J, Syljuasen RG, Lundin C, Bartek J, et al. The cell cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat Cell Biol 2005; 7:195-201. (Pubitemid 40268135)
45. Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, Bartek J, et al. Human CtIP promotes DNA end resection. Nature 2007; 450:509-514 (Pubitemid 350190253)
46. Sorensen CS, Syljuasen RG, Lukas J, Bartek J. ATR, Claspin and the Rad9-Rad1-Hus1 complex regulate Chk1 and Cdc25A in the absence of DNA damage. Cell Cycle 2004; 3:941-945 (Pubitemid 40179476)
47. Jazayeri A, Falck J, Lukas C, Bartek J, Smith GC, Lukas J, et al. ATM- and cell cycledependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol 2006; 8:37-45. (Pubitemid 43064795)
48. Liu S, Bekker-Jensen S, Mailand N, Lukas C, Bartek J, Lukas J. Claspin operates downstream of TopBP1 to direct the ATR signalling towards Chk1 activation. Mol Cell Biol 2006; 26:6056-6064 (Pubitemid 44204525)
49. Horejsi Z, Falck J, Bakkenist CJ, Kastan MB, Lukas J, Bartek J. Distinct functional domains of Nbs1 modulate the timing and magnitude of ATM activation after low doses of ionizing radiation. Oncogene 2004; 23:3122-3127 (Pubitemid 38648203)
50. Bartkova J, Horejsi Z, Koed K, Kramer A, Tort F, Zieger K, et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005; 434:864-870 (Pubitemid 40558993)
51. Gorgoulis VG, Vassiliou LV, Karakaidos P, Zacharatos P, Kotsinas A, Liloglou T, et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005; 434:907-913 (Pubitemid 40559004)
52. Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N, et al. Oncogeneinduced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 2006; 444:633-637 (Pubitemid 44864442)
53. DiMicco, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, Luise C, et al. Oncogeneinduced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 2006; 444:638-642 (Pubitemid 44864443)
54. Pierce AJ, Hu P, Han M, Ellis N, Jasin M. Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev 2001; 15:3237-3242 (Pubitemid 34008189)
55. Griffith E, Walker S, Martin C-A, Vagnarelli P, Stiff T, Vernay B, et al. Mutations in pericentrin cause Seckel syndrome with defective ATR-dependent DNA damage signaling. Nature Genet 2008; 40:232-236 (Pubitemid 351171398)