Persistence of γ-H2AX and 53BP1 foci in proliferating and non-proliferating human mammary epithelial cells after exposure to γ-rays or iron ions

International Journal of Radiation Biology

Volumn 87, Issue 7, 2011, Pages 696-710

  Groesser, Torsten ^a   Chang, Hang ^a   Fontenay, Gerald ^a   Chen, James ^a   Costes, Sylvain V ^a   Helen Barcellos Hoff, Mary ^a,b   Parvin, Bahram ^a   Rydberg, Bjorn ^a  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

3D; Foci; HMEC; HZE; iron; MCF10A

Indexed keywords

ALPHA6 INTEGRIN; HISTONE H2AX; IRON; PHOSPHOPROTEIN; PROTEIN P53 BINDING PROTEIN 1; UNCLASSIFIED DRUG;

ARTICLE; BREAST EPITHELIUM; CELL CULTURE; CELL GROWTH; CELL PROLIFERATION; CELL STRUCTURE; CHROMATID; CHROMOSOME CONDENSATION; EPITHELIUM CELL; EXTRACELLULAR MATRIX; GAMMA RADIATION; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IONIZING RADIATION; MITOSIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RADIATION DOSE; RADIATION EXPOSURE;

CELL LINE; CELL PROLIFERATION; GAMMA RAYS; HEAVY IONS; HISTONES; HUMANS; IRON; MAMMARY GLANDS, HUMAN; TUMOR SUPPRESSOR PROTEIN P53;

EID: 79960020868     PISSN: 09553002     EISSN: 13623095     Source Type: Journal    
DOI: 10.3109/09553002.2010.549535     Document Type: Article

References (52)

1. Asaithamby A, Uematsu N, Chatterjee A, Story MD, Burma S, Chen DJ. 2008. Repair of HZE-particle-induced DNA doublestrand breaks in normal human fibroblasts. Radiation Research 169:437-446. (Pubitemid 351620042)
2. Barcellos-Hoff MH, Aggeler J, Ram TG, Bissell MJ. 1989. Functional differentiation and alveolar morphogenesis of primary mammary cultures on reconstituted basement membrane. Development 105:223-235. (Pubitemid 19053272)
3. Bissell MJ, Hall HG, Parry G. 1982. How does the extracellular matrix direct gene expression? Journal of Theoretical Biology 99:31-68. (Pubitemid 13209096)
4. Bryant PE, Gray LJ, Peresse N. 2004. Progress towards understanding the nature of chromatid breakage. Cytogenetic and Genome Research 104:65-71. (Pubitemid 38721054)
5. Bryant PE, Mozdarani H, Marr C. 2008. G2-phase chromatid break kinetics in irradiated DNA repair mutant hamster cell lines using calyculin-induced PCC and colcemid-block. Mutation Research 657:8-12.
6. Chang H, Yang Q, Parvin B. 2007. Segmentation of heterogeneous blob objects through voting and level set formulation. Pattern Recognition Letters 28:1781-1787. (Pubitemid 47058629)
7. Costes SV, Chiolo I, Pluth JM, Barcellos-Hoff MH, Jakob B. 2010. Spatiotemporal characterization of ionizing radiation induced DNA damage foci and their relation to chromatin organization. Mutation Research 704:78-87.
8. Costes SV, Ponomarev A, Chen JL, Nguyen D, Cucinotta FA, Barcellos-Hoff MH. 2007. Image-based modeling reveals dynamic redistribution of DNA damage into nuclear subdomains. PLoS Computational Biology 3:e155.
9. Cucinotta FA, Durante M. 2006. Cancer risk from exposure to galactic cosmic rays: Implications for space exploration by human beings. The Lancet Oncology 7:431-435.
10. Debnath J, Muthuswamy SK, Brugge JS. 2003. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 30:256-268. (Pubitemid 36677560)
11. Desai N, Davis E, ONeill P, Durante M, Cucinotta FA, Wu H. 2005. Immunofluorescence detection of clustered gamma- H2AX foci induced by HZE-particle radiation. Radiation Research 164:518-522. (Pubitemid 41368929)
12. Durante M, Kronenberg A. 2005. Ground-based research with heavy ions for space radiation protection. Advances in Space Research 35:180-184. (Pubitemid 40684050)
13. Durante M, Cucinotta FA. 2008. Heavy ion carcinogenesis and human space exploration. Nature Reviews. Cancer 8:465-472. (Pubitemid 351744960)
14. Frankenberg-Schwager M, Gebauer A, Koppe C, Wolf H, Pralle E, Frankenberg D. 2009. Single-strand annealing, conservative homologous recombination, nonhomologous DNA end joining, and the cell cycle-dependent repair of DNA double-strand breaks induced by sparsely or densely ionizing radiation. Radiation Research 171:265-273.
15. Goldstein JC, Rodier F, Garbe JC, Stampfer MR, Campisi J. 2005. Caspase-independent cytochrome c release is a sensitive measure of low-level apoptosis in cell culture models. Aging Cell 4:217-222. (Pubitemid 41602743)
16. Goodhead DT. 1994. Initial events in the cellular effects of ionizing radiations: Clustered damage in DNA. International Journal of Radiation Biology 65:7-17. (Pubitemid 24063524)
17. Gotoh E, Durante M. 2006. Chromosome condensation outside of mitosis: Mechanisms and new tools. Journal of Cellular Physiology 209:297-304. (Pubitemid 44484619)
18. Hammond SL, Ham RG, Stampfer MR. 1984. Serum-free growth of human mammary epithelial cells: Rapid clonal growth in defined medium and extended serial passage with pituitary extract. Proceedings of the National Academy of Sciences of the USA 81:5435-5439. (Pubitemid 14048762)
19. Han J, Chang H, Yang Q, Barcellos-Hoff MH, Parvin, B. 2007. Segmentation of mammosphere structures from volumetric data. IEEE International Symposium on Biomedical Imaging: From nano to macro. pp 524-528.
20. Han J, Chang H, Yang Q, Fontenay G, Groesser T, Barcellos- Hoff MH, Parvin B. 2010. Multiscale iterative voting for differential analysis of stress response in 2D and 3D cell culture models. Journal of Microscopy. Early view online. Available from: http://onlinelibrary.wiley.com/doi/10.1111/j.1365- 2818.2010.03442.x/pdf
21. Held KD. 2009. Effects of low fluences of radiations found in space on cellular systems. International Journal of Radiation Biology 85:379-390.
22. Iliakis G. 2009. Backup pathways of NHEJ in cells of higher eukaryotes: Cell cycle dependence. Radiotherapy and Oncology 92:310-315.
23. Iliakis G,Metzger L, Muschel RJ, McKenna WG. 1990. Induction and repair of DNA double strand breaks in radiation-resistant cells obtained by transformation of primary rat embryo cells with the oncogenes H-ras and v-myc. Cancer Research 50:6575-6579. (Pubitemid 20348782)
24. Imbalzano KM, Tatarkova I, Imbalzano AN, Nickerson JA. 2009. Increasingly transformed MCF-10A cells have a progressively tumor-like phenotype in three-dimensional basement membrane culture. Cancer Cell International 9:7:1-11.
25. Karlsson KH, Stenerlöw B. 2004. Focus formation of DNA repair proteins in normal and repair-deficient cells irradiated with high-LET ions. Radiation Research 161:517-527. (Pubitemid 40754220)
26. Kato TA, Okayasu R, Bedford JS. 2008. Comparison of the induction and disappearance of DNA double strand breaks and gamma-H2AX foci after irradiation of chromosomes in G1- phase or in condensed metaphase cells. Mutation Research 639:108-112.
27. Kenny PA, Lee GY, Myers CA, Neve RM, Semeiks JR, Spellman PT, Lorenz K, Lee EH, Barcellos-Hoff MH, Petersen OW, et al. 2007. The morphologies of breast cancer cell lines in threedimensional assays correlate with their profiles of gene expression. Mol Oncology 1:84-96. (Pubitemid 46776616)
28. Lee GY, Kenny PA, Lee EH, BissellMJ. 2007. Three-dimensional culture models of normal and malignant breast epithelial cells. Nature Methods 4:359-365. (Pubitemid 46766981)
29. Löbrich M, Cooper PK, Rydberg B. 1996. Non-random distribution of DNA double-strand breaks induced by particle irradiation. International Journal of Radiation Biology 70:493-503. (Pubitemid 26388940)
30. Meesungnoen J, Benrahmoune M, Filali-Mouhim A, Mankhetkorn S, Jay-Gerin JP. 2001. Monte Carlo calculation of the primary radical and molecular yields of liquid water radiolysis in the linear energy transfer range 0.3-6.5 keV/micrometer: Application to 137Cs gamma rays. Radiation Research 155:269-278. (Pubitemid 32125977)
31. Parvin B, Yang Q, Fontenay G, Barcellos-Hoff MH. 2003. BioSig: An imaging bioinformatics system for phenotypic analysis. IEEE Transactions on Systems, Man, and Cybernetics. Part B, Cybernetics 33:814-824.
32. Parvin B, Yang Q, Han J, Chang H, Rydberg B, Barcellos-Hoff MH. 2007. Iterative voting for inference of structural saliency and characterization of subcellular events. IEEE Transactions on Image Processing 16:615-623. (Pubitemid 46431961)
33. Parvin B, Fontenay G, Yang Q, Barcellos-Hoff MH. 2002. BioSig: An imaging bioinformatic system for studying phenomic. IEEE Computer 35:65-71.
34. Pilch DR, Sedelnikova OA, Redon C, Celeste A, Nussenzweig A, Bonner WM. 2003. Characteristics of gamma-H2AX foci at DNA double-strand breaks sites. Biochemistry and Cell Biology 81:123-129. (Pubitemid 37076234)
35. Raman S, Maxwell CA, Barcellos-Hoff MH, Parvin B. 2007. Geometric approach to segmentation and protein localization in cell culture assays. Journal of Microscopy 225:22-30. (Pubitemid 46213657)
36. Rogakou EP, Boon C, Redon C, Bonner WM. 1999. Megabase chromatin domains involved in DNA double-strand breaks in vivo. The Journal of Cell Biology 146:905-916.
37. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. 1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. The Journal of Biological Chemistry 273:5858-5868. (Pubitemid 28124064)
38. Roig AI, Hight SK, Shay JW. 2009. Two- and three-dimensional models for risk assessment of radiation-enhanced colorectal tumorigenesis. Radiation Research 171:33-40.
39. Rydberg B. 1996. Clusters of DNA damage induced by ionizing radiation: Formation of short DNA fragments. II. Experimental detection. Radiation Research 145:200-209. (Pubitemid 26066331)
40. Rydberg B, Cooper B, Cooper PK, Holley WR, Chatterjee A. 2005. Dose-dependent misrejoining of radiation-induced DNA double-strand breaks in human fibroblasts: Experimental and theoretical study for high- and low-LET radiation. Radiation Research 163:526-534. (Pubitemid 41490648)
41. 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. The Journal of Cell Biology 151:1381-1390. (Pubitemid 32047588)
42. Sedelnikova OA, Rogakou EP, Panyutin IG, Bonner WM. 2002. Quantitative detection of (125)IdU-induced DNA doublestrand breaks with gamma-H2AX antibody. Radiation Research 158:486-492.
43. Sedelnikova OA, Horikawa I, Zimonjic DB, Popescu NC, Bonner WM, Barrett JC. 2004. Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks. Nature Cell Biology 6:168-170. (Pubitemid 38425717)
44. Sedelnikova OA, Horikawa I, Redon C, Nakamura A, Zimonjic DB, Popescu NC, Bonner WM. 2008. Delayed kinetics of DNA double-strand break processing in normal and pathological aging. Aging Cell 7:89-100.
45. Soule HD, Maloney TM, Wolman SR, Peterson WD Jr, Brenz R, McGrath CM, Russo J, Pauley RJ, Jones RF, Brooks SC. 1990. Isolation and characterization of a spontaneously immortalized human breast epithelial cell line, MCF-10. Cancer Research 50:6075-6086. (Pubitemid 20331424)
46. Soutoglou E, Dorn JF, Sengupta K, JasinM, Nussenzweig A, Ried T, Danuser G, Misteli T. 2007. Positional stability of single double-strand breaks in mammalian cells. Nature Cell Biology 9:675-682. (Pubitemid 47214730)
47. Stampfer MR, Pan CH, Hosoda J, Bartholomew J, Mendelsohn J, Yaswen P. 1993. Blockage of EGF receptor signal transduction causes reversible arrest of normal and immortal human mammary epithelial cells with synchronous reentry into the cell cycle. Experimental Cell Research 208:175-188. (Pubitemid 23274503)
48. Stenerlöw B, Höglund E, Carlsson J, Blomquist E. 2000. Rejoining of DNA fragments produced by radiations of different linear energy transfer. International Journal of Radiation Biology 76:549-557. (Pubitemid 30232455)
49. Sudo H, Garbe J, Stampfer MR, Barcellos-Hoff MH, Kronenberg A. 2008. Karyotypic instability and centrosome aberrations in the progeny of finite life-span human mammary epithelial cells exposed to sparsely or densely ionizing radiation. Radiation Research 170:23-32. (Pubitemid 351931184)
50. Suzuki M, Suzuki K, Kodama S, Watanabe M. 2006. Interstitial chromatin alteration causes persistent p53 activation involved in the radiation-induced senescence-like growth arrest. Biochemical and Biophysical Research Communications 340:145-150. (Pubitemid 41827659)
51. Takahashi A, Yamakawa N, Kirita T, Omori K, Ishioka N, Furusawa Y, Mori E, Ohnishi K, Ohnishi T. 2008. DNA damage recognition proteins localize along heavy ion induced tracks in the cell nucleus. Journal of Radiation Research 49:645-652.
52. Zafar F, Seidler SB, Kronenberg A, Schild D, Wiese C. 2010. Homologous recombination contributes to the repair of DNA double-strand breaks induced by high-energy iron ions. Radiation Research 173:27-39.