Image-based modeling reveals dynamic redistribution of DNA damage into nuclear sub-domains

PLoS Computational Biology

Volumn 3, Issue 8, 2007, Pages 1477-1488

  Costes, Sylvain V ^a   Ponomarev, Artem ^b,c   Chen, James L ^a   Nguyen, David ^a   Cucinotta, Francis A ^b   Barcellos Hoff, Mary Helen ^a  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b NASA JOHNSON SPACE CENTER   (United States)

^c UNIVERSITIES SPACE RESEARCH ASSOCIATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOINFORMATICS; ELECTROPHORESIS; ENERGY TRANSFER; INTELLIGENT SYSTEMS; IONIZING RADIATION; MONTE CARLO METHODS; PHOSPHORYLATION; POISSON DISTRIBUTION;

DNA DAMAGES; DNA DENSITY; DNA DOUBLE STRAND BREAKS; DOUBLE STRAND BREAKS; DYNAMIC REDISTRIBUTION; HIGH LINEAR ENERGY TRANSFERS; IMAGE-BASED MODELS; LOW LINEAR ENERGY TRANSFERS; RADIATION-INDUCED; SUBDOMAIN;

DNA;

DNA FRAGMENT; PROTEIN; DNA;

ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA STRAND BREAKAGE; GENE FREQUENCY; GENE LOCATION; HUMAN; HUMAN CELL; IONIZING RADIATION; LINEAR ENERGY TRANSFER; MONTE CARLO METHOD; PULSED FIELD GEL ELECTROPHORESIS; BIOLOGICAL MODEL; CELL NUCLEUS; CHEMISTRY; COMPUTER ASSISTED DIAGNOSIS; COMPUTER SIMULATION; DNA REPAIR; EPITHELIUM CELL; METABOLISM; METHODOLOGY; PHYSIOLOGY; RADIATION EXPOSURE; ULTRASTRUCTURE;

CELL NUCLEUS; COMPUTER SIMULATION; DNA; DNA DAMAGE; DNA REPAIR; EPITHELIAL CELLS; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MODELS, BIOLOGICAL;

EID: 34548414588     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.0030155     Document Type: Article

References (44)

1. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858-5868.
2. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, et al. (2000) A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 10: 886-895.
3. Celeste A, Petersen S, Romanienko PJ, Fernandez-Capetillo O, Chen HT, et al. (2002) Genomic instability in mice lacking histone H2AX. Science 296: 922-927.
4. MacPhail SH, Banath JP, Yu TY, Chu EH, Lambur H, et al. (2003) Expression of phosphorylated histone H2AX in cultured cell lines following exposure to X-rays. Int J Radiat Biol 79: 351-358.
5. Kurz EU, Lees-Miller SP (2004) DNA damage-induced activation of ATM and ATM-dependent signaling pathways. DNA Repair (Amst) 3: 889-900.
6. Balajee AS, Geard CR (2004) Replication protein A and gamma-H2AX foci assembly is triggered by cellular response to DNA double-strand breaks. Exp Cell Res 300: 320-334.
7. Karlsson KH, Stenerlow B (2004) Focus formation of DNA repair proteins in normal and repair-deficient cells irradiated with high-LET ions. Radiat Res 161: 517-527.
8. Anderson L, Henderson C, Adachi Y (2001) Phosphorylation and rapid relocalization of 53BP1 to nuclear foci upon DNA damage. Mol Cell Biol 21: 1719-1729.
9. Rappold I, Iwabuchi K, Date T, Chen J (2001) Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways. J Cell Biol 153: 613-620.
10. Schultz LB, Chehab NH, Malikzay A, Halazonetis TD (2000) p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J Cell Biol 151: 1381-1390.
11. Costes SV, Boissiere A, Ravani SA, Romano R, Parvin B, et al. (2006) Imaging features that discriminate between high and low LET radiation-induced foci in human fibroblasts. Radiat Res 165: 505-515.
12. Han J, Hendzel MJ, Allalunis-Turner J (2006) Quantitative analysis reveals asynchronous and more than DSB-associated histone H2AX phosphorylation after exposure to ionizing radiation. Radiat Res 165: 283-292.
13. Reitsema TJ, Banath JP, MacPhail SH, Olive PL (2004) Hypertonic saline enhances expression of phosphorylated histone H2AX after irradiation. Radiat Res 161: 402-408.
14. MacPhail SH, Banath JP, Yu Y, Chu E, Olive PL (2003) Cell cycle-dependent expression of phosphorylated histone H2AX: Reduced expression in unirradiated but not X-irradiated G1-phase cells. Radiat Res 159: 759-767.
15. Jakob B, Scholz M, Taucher-Scholz G (2003) Biological imaging of heavy charged-particle tracks. Radiat Res 159: 676-684.
16. Magee JL, Chatterjee A (1980) Radiation chemistry of heavy-particle tracks. 1. General considerations. J Phys Chem 84: 3529-3536.
17. Zeiss GD, Meath WJ, MacDonald JCF, Dawson DJ (1975) Dipole spectrum of water vapor and its relation to the energy loss of fast-charged particles. Rad Res 63: 64-82.
18. Cucinotta FA, Nikjoo H, Goodhead DT (1999) Applications of amorphous track models in radiation biology. Radiat Environ Biophys 38: 81-92.
19. Sachs RK, Ponomarev AL, Hahnfeldt P, Hlatky LR (1999) Locations of radiation-produced DNA double strand breaks along chromosomes: A stochastic cluster process formalism. Math Biosci 159: 165-187.
20. Ponomarev AL, Cucinotta FA, Sachs RK, Brenner DJ, Peterson LE (2001) Extrapolation of the dna fragment-size distribution after high-dose irradiation to predict effects at low doses. Radiat Res 156: 594-597.
21. Ponomarev AL, Brenner D, Hlatky LR, Sachs RK (2000) A polymer, random walk model for the size-distribution of large DNA fragments after high linear energy transfer radiation. Radiat Environ Biophys 39: 111-120.
22. Ponomarev AL, Cucinotta FA (2006) Chromatin loops are responsible for higher counts of small DNA fragments induced by high-LET radiation, while chromosomal domains do not affect the fragment sizes. Int J Radiat Biol 82: 293-305.
23. Munkel C, Eils R, Dietzel S, Zink D, Mehring C, et al. (1999) Compartmentalization of interphase chromosomes observed in simulation and experiment. J Mol Biol 285: 1053-1065.
24. Ponomarev AL, Cucinotta FA (2006) Novel image processing interface to relate DSB spatial distribution from experiments with phosphorylation foci to the state-of-the-art models of DNA breakage. Radiat Meas Space Radiat Trans Shielding Risk Assess Models 41: 1075-1079.
25. Stenerlow B, Karlsson KH, Cooper B, Rydberg B (2003) Measurement of prompt DNA double-strand breaks in mammalian cells without including heat-labile sites: Results for cells deficient in nonhomologous end joining. Radiat Res 159: 502-510.
26. Costes SV, Daelemans D, Cho EH, Dobbin Z, Pavlakis G, et al. (2004) Automatic and quantitative measurement of protein-protein colocalization in live cells. Biophys J 86: 3993-4003.
27. 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.
28. Andegeko Y, Moyal L, Mittelman L, Tsarfaty I, Shiloh Y, et al. (2001) Nuclear retention of ATM at sites of DNA double strand breaks. J Biol Chem 276: 38224-38230.
29. 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: 19579-19582.
30. Bekker-Jensen S, Lukas C, Kitagawa R, Melander F, Kastan MB, et al. (2006) Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J Cell Biol 173: 195-206. doi:10.1083/jcb. 200510130
31. Shiloh Y (2000) ATM: Sounding the double-strand break alarm. Cold Spring Harb Symp Quant Biol 65: 527-533.
32. 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: 823-834. doi:10.1083/jcb.200510015
33. Bakkenist CJ, Kastan MB (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421: 499-506.
34. Cremer T, Cremer C (2001) Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet 2: 292-301.
35. Chuang CH, Carpenter AE, Fuchsova B, Johnson T, de Lanerolle P, et al. (2006) Long-range directional movement of an interphase chromosome site. Curr Biol 16: 825-831.
36. Savage JR (1996) Insight into sites. Mutat Res 366: 81-95.
37. Savage JR (2002) Reflections and meditations upon complex chromosomal exchanges. Mutat Res 512: 93-109.
38. Lisby M, Mortensen UH, Rothstein R (2003) Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat Cell Biol 5: 572-577.
39. DiBiase SJ, Zeng ZC, Chen R, Hyslop T, Curran WJ Jr, et al. (2000) DNA-dependent protein kinase stimulates an independently active, nonhomologous, end-joining apparatus. Cancer Res 60: 1245-1253.
40. Dupre A, Boyer-Chatenet L, Gautier J (2006) Two-step activation of ATM by DNA and the Mre11-Rad50-Nbs1 complex. Nat Struct Mol Biol 13: 451-457.
41. Stampfer MR (1985) Isolation and growth of human mammary epithelial cells. J Tissue Culture Met 9: 107-115.
42. Th'ng JP, Sung R, Ye M, Hendzel MJ (2005) H1 family histones in the nucleus. Control of binding and localization by the C-terminal domain. J Biol Chem 280: 27809-27814.
43. Bocker W, Iliakis G (2006) Computational methods for analysis of foci: Validation for radiation-induced gamma-H2AX foci in human cells. Radiat Res 165: 113-124.
44. Cucinotta FA, Nikjoo H, Goodhead DT (2000) Model for radial dependence of frequency distributions for energy imparted in nanometer volumes from HZE particles. Radiat Res 153: 459-468.