Dynamics of the DNA damage response: Insights fromlive-cell imaging

Briefings in Functional Genomics

Volumn 12, Issue 2, 2013, Pages 109-117

  Karanam, Ketki ^a   Loewer, Alexander ^b   Lahav, Galit ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Max Delbruek Center   (Germany)

Author keywords

DNA damage; Dynamics; Fluorescence microscopy; Live cell imaging; Single cell

Indexed keywords

CELL PROTEIN; GREEN FLUORESCENT PROTEIN;

ARTICLE; CELLULAR DISTRIBUTION; DNA DAMAGE; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; EXCISION REPAIR; GENE FUSION; HUMAN; IMAGING; LIVE CELL IMAGING; MOLECULAR DYNAMICS; NONHUMAN; TIME LAPSE IMAGING;

ANIMALS; CELL SURVIVAL; DNA DAMAGE; DNA REPAIR; HUMANS; IMAGING, THREE-DIMENSIONAL; SINGLE-CELL ANALYSIS; TIME-LAPSE IMAGING;

EID: 84875763763     PISSN: 20412649     EISSN: 20412657     Source Type: Journal    
DOI: 10.1093/bfgp/els059     Document Type: Article

References (70)

1. Lobrich M, Jeggo PA. The impact of a negligent G2/M checkpoint on genomic instability and cancer induction. Nat Rev Cancer 2007;7:861-9.
2. Kastan MB, Bartek J. Cell-cycle checkpoints and cancer. Nature 2004;432:316-23.
3. Su TT. Cellular responses to DNA damage: one signal, multiple choices. Ann Rev Genet 2006;40:187-208.
4. Zhou BB, Elledge SJ. The DNA damage response: putting checkpoints in perspective. Nature 2000;408:433-9.
5. Harrison JC, Haber JE. Surviving the breakup: the DNA damage checkpoint. Ann Rev Genet 2006;40:209-35.
6. Helleday T, Petermann E, Lundin C, et al. DNA repair pathways as targets for cancer therapy. Nat Rev Cancer 2008;8:193-204.
7. Berenbaum MC. In vivo determination of the fractional kill of human tumor cells by chemotherapeutic agents. Cancer Chemother Rep1 1972;56:563-571.
8. Chabner BA, Longo DL. CancerChemotherapyandBiotherapy: Principles and Practice. Philadelphia: Lippincott Williams&Wilkins, 2006.
9. Skeel RT. Handbook of Cancer Chemotherapy. Philadelphia: Lippincott Williams&Wilkins, 2003.
10. Reya T, Morrison SJ, Clarke MF, et al. Stem cells, cancer, and cancer stem cells. Nature 2001;414:105-11.
11. Loewer A, Lahav G. We are all individuals: causes and consequences of non-genetic heterogeneity in mammalian cells. Curr Opin Genet Dev 2011;21:753-8.
12. Snijder B, Pelkmans L. Origins of regulated cell-to-cell variability. Nat. Rev.Mol Cell Biol 2011;12:119-25.
13. Feinerman O, Veiga J, Dorfman JR, et al. Variability and robustness in T cell activation from regulated heterogeneity in protein levels. Science 2008;321:1081-4.
14. Spencer SL, Gaudet S, Albeck JG, et al. Non-genetic origins of cell-to-cell variability in TRAIL-induced apoptosis. Nature 2009;459:428-32.
15. Chang HH, Hemberg M, Barahona M, et al. Transcriptome-wide noise controls lineage choice in mammalian progenitor cells. Nature 2008;453:544-7.
16. Iliakis GE, Cicilioni O, Metzger L. Measurement of DNA double-strand breaks in CHO cells at various stages of the cell cycle using pulsed field gel electrophoresis: calibration by means of 125I decay. Int J Radiation Biol 1991;59:343-57.
17. Shaposhnikov S, Frengen E, Collins AR. Increasing the resolution of the comet assay using fluorescent in situ hybridization-a review. Mutagenesis 2009;24:383-9.
18. Maser RS, Monsen KJ, Nelms BE, et al. hMre11 and hRad50 nuclear foci are induced during the normal cellular response to DNA double-strand breaks. Mol Cell Biol 1997; 17:6087-96.
19. Haaf T, Golub EI, Reddy G, et al. Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc Natl Acad Sci USA 1995;92:2298-302.
20. Scully R, Chen J, Ochs RL, et al. Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 1997;90:425-35.
21. Lobrich M, Shibata A, Beucher A, et al. gammaH2AX foci analysis for monitoring DNA double-strand break repair: strengths, limitations and optimization. Cell Cycle 2010;9: 662-69.
22. Ciccia A, Elledge SJ. The DNA damage response: making it safe to play with knives. Mol Cell 2010;40:179-204.
23. Lisby M, Rothstein R. Choreography of recombination proteins during the DNA damage response. DNA Repair 2009;8:1068-76.
24. Polo SE, Jackson SP. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev 2011;25:409-33.
25. Bekker-Jensen S, Mailand N. Assembly and function of DNA double-strand break repair foci in mammalian cells. DNA Repair 2010;9:1219-28.
26. Essers J, Houtsmuller AB, van Veelen L, et al. Nuclear dynamics of RAD52 group homologous recombination proteins in response to DNA damage. EMBO J 2002;21: 2030-7.
27. Jeyasekharan AD, Ayoub N, Mahen R, et al. DNA damage regulates the mobility of Brca2 within the nucleoplasm of living cells. Proc Natl Acad Sci USA 2010;107:21937-42.
28. Lukas C, Falck J, Bartkova J, et al. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat Cell Biol 2003;5:255-60.
29. Lukas C, Melander F, Stucki M, et al. Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J 2004;23: 2674-83.
30. Bekker-Jensen S, Lukas C, Melander F, et al. Dynamic assembly and sustained retention of 53BP1 at the sites of DNA damage are controlled by Mdc1/NFBD1. J Cell Biol 2005;170:201-11.
31. Lisby M, Mortensen UH, Rothstein R. Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat Cell Biol 2003;5:572-7.
32. Mine-Hattab J, Rothstein R. Increased chromosome mobility facilitates homology search during recombination. Nat Cell Biol 2012;14:510-7.
33. Dion V, Kalck V, Horigome C, et al. Increased mobility of double-strand breaks requires Mec1, Rad9 and the homologous recombination machinery. Nat Cell Biol 2012; 14:502-9.
34. Nagai S, Dubrana K, Tsai-Pflugfelder M, etal. Functional targeting of DNA damage to a nuclear pore-associated SUMOdependent ubiquitin ligase. Science 2008;322:597-602.
35. Soutoglou E, Dorn JF, Sengupta K, et al. Positional stability of single double-strand breaks in mammalian cells. Nat Cell Biol 2007;9:675-82.
36. Krawczyk PM, Borovski T, Stap J, etal. Chromatin mobility is increased at sites of DNA double-strand breaks. JCell Sci 2012;125:2127-33.
37. Kruhlak MJ, Celeste A, Dellaire G, et al. Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. JCell Biol 2006;172:823-34.
38. Dimitrova N, Chen YC, Spector DL, etal. 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature 2008;456:524-8.
39. Aten JA, Stap J, Krawczyk PM, et al. Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 2004;303:92-5.
40. Tsien RY. The green fluorescent protein. AnnRev Biochem 1998;67:509-44.
41. Patterson G, Davidson M, Manley S, et al. Superresolution imaging using single-molecule localization. Ann Rev Phys Chem 2010;61:345-67.
42. Stepanenko OV, Shcherbakova DM, Kuznetsova IM, et al. Modern fluorescent proteins: from chromophore formation to novel intracellular applications. BioTechniques 2011;51: 313-14, 316, 318 passim.
43. Nagy Z, Soutoglou E. DNA repair: easy to visualize, difficult to elucidate. Trends Cell Biol 2009;19:617-29.
44. Houtsmuller AB, Vermeulen W. Macromolecular dynamics in living cell nuclei revealed by fluorescence redistribution after photobleaching. Histochem Cell Biol 2001;115:13-21.
45. Reits EA, Neefjes JJ. From fixed to FRAP: measuring protein mobility and activity in living cells. Nat Cell Biol 2001;3:E145-7.
46. Dundr M, Misteli T. Measuring dynamics of nuclear proteins by photobleaching, Current protocols in cell biology/ editorial board, Juan S. Bonifacino. [et al.] 2003; Chapter 13: Unit 13 15.
47. van Royen ME, Farla P, Mattern KA, et al. Fluorescence recovery after photobleaching (FRAP) to study nuclear protein dynamics in living cells. Methods Mol Biol 2009; 464:363-85.
48. Mueller F, Mazza D, Stasevich TJ, et al. FRAP and kinetic modeling in the analysis of nuclear protein dynamics: what do we really know? Curr Opin Cell Biol 2010;22:403-11.
49. Lippincott-Schwartz J, Snapp E, Kenworthy A. Studying protein dynamics in living cells. Nat Rev Mol Cell Biol 2001;2:444-56.
50. Sprague BL, McNally JG. FRAP analysis of binding: proper and fitting. Trends Cell Biol 2005;15:84-91.
51. Carrero G, McDonald D, Crawford E, et al. Using FRAP and mathematical modeling to determine the in vivo kinetics of nuclear proteins. Methods 2003;29:14-28.
52. Kimura H. Histone dynamics in living cells revealed by photobleaching. DNA Repair 2005;4:939-50.
53. Koster M, Frahm T, Hauser H. Nucleocytoplasmic shuttling revealed by FRAP and FLIP technologies. Curr Opin Biotechnol 2005;16:28-34.
54. Maiti S, Haupts U, Webb WW. Fluorescence correlation spectroscopy: diagnostics for sparse molecules. ProcNatlAcad SciUSA 1997;94:11753-7.
55. Van Craenenbroeck E, Engelborghs Y. Fluorescence correlation spectroscopy: molecular recognition at the single molecule level. JMR 2000;13:93-100.
56. Pramanik A. Ligand-receptor interactions in live cells by fluorescence correlation spectroscopy. Curr Pharmaceutical Biotechnol 2004;5:205-12.
57. Bacia K, Schwille P. A dynamic view of cellular processes by in vivo fluorescence auto- and cross-correlation spectroscopy. Methods 2003;29:74-85.
58. Wachsmuth M, Caudron-Herger M, Rippe K. Genome organization: balancing stability and plasticity. Biochimica et Biophysica Acta 2008;1783:2061-79.
59. Cole NB, Smith CL, Sciaky N, et al. Diffusional mobility of golgi proteins in membranes of living cells. Science 1996; 273:797-801.
60. Gillet LC, Scharer OD. Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem Rev 2006;106:253-76.
61. Michelman-Ribeiro A, Mazza D, Rosales T, et al. Direct measurement of association and dissociation rates of DNA binding in live cells by fluorescence correlation spectroscopy. BiophysJ 2009;97:337-46.
62. Karanam K, Kafri R, Loewer A, et al. Quantitative live cell imaging reveals a gradual shift between DNA repair mechanisms and a maximal use of HR in mid S phase. Mol Cell 2012;47:320-9.
63. Poser I, Sarov M, Hutchins JR, etal. BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals. NatMethods 2008;5:409-15.
64. Sigal A, Milo R, Cohen A, et al. Dynamic proteomics in individual human cells uncovers widespread cellcycle dependence of nuclear proteins. Nat Methods 2006;3: 525-31.
65. Issaeva I, Cohen AA, Eden E, et al. Generation of double-labeled reporter cell lines for studying co-dynamics of endogenous proteins in individual human cells. PloSOne 2010;5:e13524.
66. Li T, Huang S, Zhao X, et al. Modularly assembled designer TAL effector nucleases for targeted gene knockout and gene replacement in eukaryotes. Nucleic Acids Res 2011;39: 6315-25.
67. Howson R, Huh WK, Ghaemmaghami S, et al. Construction, verification and experimental use of two epitope-tagged collections of budding yeast strains. Compar Funct Genom 2005;6:2-16.
68. Filonov GS, Piatkevich KD, Ting LM, et al. Bright and stable near-infrared fluorescent protein for in vivo imaging. Nat Biotechnol 2011;29:757-61.
69. Shu X, Royant A, Lin MZ, et al. Mammalian expression of infrared fluorescent proteins engineered from a bacterial phytochrome. Science 2009;324:804-07.
70. Walter T, Shattuck DW, Baldock R, et al. Visualization of image data from cells to organisms. Nat Methods 2010;7: S26-41.