γ-H2AX foci after low-dose-rate irradiation reveal Atm haploinsufficiency in mice

Radiation Research

Volumn 166, Issue 1 I, 2006, Pages 47-54

  Kato, Takamitsu A ^a   Nagasawa, Hatsumi ^a   Weil, Michael M ^a   Genik, Paula C ^a   Little, J B ^b   Bedford, J S ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; HISTONE H2AX;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; DNA STRAND BREAKAGE; GAMMA RADIATION; GENE MUTATION; HETEROZYGOSITY; HOMOZYGOSITY; IMMUNOCYTOCHEMISTRY; LOW ENERGY RADIATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DETERMINATION; RADIATION DOSE; RADIATION EXPOSURE; RADIOSENSITIVITY; SAMPLING;

ANIMALS; CELL CYCLE PROTEINS; CELLS, CULTURED; DNA; DNA DAMAGE; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, RADIATION; EAR; HAPLOTYPES; HISTONES; MICE; PROTEIN-SERINE-THREONINE KINASES; RADIATION DOSAGE; RADIATION TOLERANCE; TUMOR SUPPRESSOR PROTEINS;

EID: 33745886245     PISSN: 00337587     EISSN: None     Source Type: Journal    
DOI: 10.1667/RR3587.1     Document Type: Article

References (55)

1. 2 phase x-irradiation of cells from cancer-prone individuals implicates deficiency in DNA repair. Proc. Natl. Acad. Sci. USA 80, 5612-5616 (1983).
2. K. K. Sanford, R. Parshad, R. R. Gantt and R. E. Tarone, A deficiency in chromatin repair, genetic instability, and predisposition to cancer. CRC Crit. Rev. Oncog. 1, 323-341 (1989).
3. K. K. Sanford and R. Parshad, Detection of cancer-prone individuals using cytogenetic response to X-rays. In Chromosome Aberrations, Basic and Applied Aspects (G. Obe and A. T. Natarajan, Eds.). Springer-Verlag, Berlin, 1990.
4. S. A. Roberts, A. R. Spreadborough, B. Bulman, J. B. Barber, D. G. R. Evans and D. Scott, Heritability of cellular radiosensitivity: A marker of low-penetrance predisposition genes in breast cancer? Am. J. Hum. Genet. 65, 784-794 (1999).
5. 2-phase lymphocytes as an indicator of cancer predisposition. Radiat. Res. 145, 3-16 (1996).
6. D. Scott, L. A. Jones, S. A. G. Elyan, A. Spreadborough, R. Cowan and G. Ribiero, Identification of A-T heterozygotes. In Atataxia-telangiectasia (R. A. Gatti and R. B. Painter, Eds.). Springer-Verlag, Berlin, 1992.
7. D. Scott, J. B. Barber, A. R. Spreadborough, W. Burrill and S. A. Roberts, Increased chromosomal radiosensitivity in breast cancer patients: A comparison of two assays. Int. J. Radiat. Biol. 75, 1-10 (1999).
8. D. Scott, A. Spreadborough, E. Levine and S. A. Roberts, Genetic predisposition in breast cancer. Lancet 344, 1444 (1994).
9. J. M. Varley, D. G. Evans and J. M. Birch, Li-Fraumeni syndrome- a molecular and clinical review. Br. J. Cancer 76, 1-14 (1997).
10. 2-phase assays for human blood lymphocytes as biomarkers of individual sensitivity to ionizing radiation: Limitations imposed by intraindividual variability. Radiat. Res. 157, 472-477 (2002).
11. A. Vral, H. Thierens, A. Baeyens and R. L. De, Chromosomal aberrations and in vitro radiosensitivity: Intra-individual versus interindividual variability. Toxicol. Lett. 149, 345-352 (2004).
12. S. Neubauer, R. Arutyunyan, M. Stumm, T. Dork, R. Bendix, M. Bremer, R. Varon, R. Sauer and E. Gebhart, Radiosensitivity of ataxia telangiectasia and Nijmegen breakage syndrome homozygotes and heterozygotes as determined by three-color FISH chromosome painting. Radiat. Res. 157, 312-321 (2002).
13. J. C. Leonard, A. M. Mullinger, J. Schmidt, H. J. Cordell and R. T. Johnson, Genome instability in ataxia telangiectasia (A-T) families: camptothecin-induced damage to replicating DNA discriminates be-tween obligate A-T heterozygotes, A-T homozygotes and controls. Biosci. Rep. 24, 617-629 (2004).
14. R. T. Johnson, E. Gotoh, A. M. Mullinger, A. J. Ryan, Y. Shiloh, Y. Ziv and S. Squires, Targeting double-strand breaks to replicating DNA identifies a subpathway of DSB repair that is defective in ataxia-telangiectasia cells. Biochem. Biophys. Res. Commun. 261, 317-325 (1999).
15. P. C. Chen, M. F. Lavin, C. Kidson and D. Moss, Identification of ataxia telangiectasia heterozygotes, a cancer prone population. Nature 274, 484-486 (1978).
16. M. C. Paterson, P. J. Smith, N. T. Bech-Hansen, B. P. Smith and B. M. Sell, Gamma-ray hypersensitivity and faulty DNA repair in cultured cells from humans exhibiting familial cancer proneness. In Radiation Research: Proceedings of the Sixth International Congress of Radiation Research (S. Okada, M. Imamura, T. Terashima and H. Yamaguchi, Eds.), pp. 484-495. Toppan, Tokyo, 1979.
17. H. Nagasawa, S. A. Latt, M. E. Lalande and J. B. Little, Effects of X-irradiation on cell cycle progression, induction of chromosomal aberrations and cell killing in ataxia telangiectasia. Mutat. Res. 148, 71-82 (1985).
18. J. B. Little and H. Nagasawa, Effect of confluent holding on potentially lethal damage repair, cell cycle progression, and chromosomal aberrations in human normal and ataxia-telangiectasia fibroblasts. Radiat. Res. 101, 81-93 (1985).
19. H. Nagasawa, K. H. Kraemer, Y. Shiloh and J. B. Little, Detection of ataxia telangiectasia heterozygous cell lines by postirradiation cumulative labeling index: Measurements with coded samples. Cancer Res. 47, 398-402 (1987).
20. H. Nagasawa, K. H. Kraemer, Y. Shiloh and J. B. Little, Detection of ataxia telangiectasia heterozygous cell lines by postirradiation cumulative labeling index: Measurements with coded samples. Cancer Res. 47, 398-402 (1987).
21. K. Rothkamm and M. Lobrich, Evidence for a lack of DNA double-strand break repair in human cells exposed to very low x-ray doses. Proc. Natl. Acad. Sci. USA 100, 5057-5062 (2003).
22. S. H. MacPhail, J. P. Banath, T. Y. Yu, E. H. Chu, H. Lambur and P. L. Olive, Expression of phosphorylated histone H2AX in cultured cell lines following exposure to X-rays. Int. J. Radiat. Biol. 79, 351-358 (2003).
23. E. P. Rogakou, D. R. Pilch, A. H. Orr, V. S. Ivanova and W. M. Bonner, DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273, 5858-5868 (1998).
24. D. E. Lea, Actions of Radiations on Living Cells. Cambridge University Press, London, 1955.
25. K. Sax, The time factor in x-ray production of chromosomal aberrations. Proc. Natl. Acad. Sci. USA 25, 225-233 (1939).
26. W. L. Russell, L. B. Russell and E. M. Kelly, Radiation dose rate and mutation frequency. Science 128, 1546-1550 (1958).
27. M. M. Elkind and H. Sutton, X-ray damage and recovery in mammalian cells in culture. Nature 184, 1293-1295 (1959).
28. J. S. Bedford and E. J. Hall, Survival of HeLa cells cultured in vitro and exposed to protracted gamma radiation. Int. J. Radiat. Biol. 7, 377-383 (1963).
29. R. L. Ullrich, M. C. Jernigan, G. E. Cosgrove, L. C. Satterfield, N. D. Bowles and J. B. Storer, The influence of dose and dose rate on the incidence of neoplastic disease in RFM mice after neutron irradiation. Radiat. Res. 68, 115-131 (1976).
30. R. L. Wells and J. S. Bedford, Dose-rate effects in mammalian cells. IV. Repairable and nonrepairable damage in noncycling C3H 10T 1/2 cells. Radiat. Res. 94, 105-134 (1983).
31. R. L. Ullrich and J. B. Storer, Influence of gamma irradiation on the development of neoplastic disease in mice. III. Dose-rate effects. Radiat. Res. 80, 325-342 (1979).
32. R. L. Ullrich, M. C. Jernigan, L. C. Satterfield and N. D. Bowles, Radiation carcinogenesis: Time-dose relationships. Radiat. Res. 111, 179-184 (1987).
33. R. A. Cox, cellular description of the repair defect in ataxia-telangiectasia. In Ataxia-Telangiectasia: A Cellular and Molecular Link Between Cancer, Neuropathology, and Immune Defeciency (B. A. Bridges and D. G. Harnden, Eds.), pp. 141-153. Wiley, Chichester, 1982.
34. M. A. Stackhouse and J. S. Bedford, An ionizing radiation-sensitive mutant of CHO cells: irs-20. II. Dose-rate effects and cellular recovery processes. Radiat. Res. 136, 250-254 (1993).
35. A. Priestley, H. J. Beamish, D. Gell, A. G. Amatucci, M. C. Muhlmann-Diaz, B. K. Singleton, G. C. Smith, T. Blunt, L. C. Schalkwyk and G. E. Taccioli, Molecular and biochemical characterization of DNA-dependent protein kinase-defective rodent mutant irs-20. Nucleic Acids Res. 26, 1965-1973 (1998).
36. H. Nagasawa, D. J. Chen and G. F. Strniste, Response of X-ray-sensitive CHO mutant cells to gamma radiation. I. Effects of low dose rates and the process of repair of potentially lethal damage in G1 phase. Radiat. Res. 118, 559-567 (1989).
37. M. A. Stackhouse and J. S. Bedford, An ionizing radiation-sensitive mutant of CHO cells: irs-20. I. Isolation and initial characterization. Radiat. Res. 136, 241-249 (1993).
38. M. A. Stackhouse and J. S. Bedford, An ionizing radiation-sensitive mutant of CHO cells: irs-20. III. Chromosome aberrations, DNA breaks and mitotic delay. Int. J. Radiat. Biol. 65, 571-582 (1994).
39. C. Barlow, S. Hirotsune, R. Paylor, M. Liyanage, M. Eckhaus, F. Collins, Y. Shiloh, J. N. Crawley, T. Ried and A. Wynshaw-Boris, Atm-deficient mice: A paradigm of ataxia telangiectasia. Cell 86, 159-171 (1996).
40. R. A. Tobey and K. D. Ley, Isoleucine-mediated regulation of genome replication in various mammalian cell lines. Cancer Res. 31, 46-51 (1971).
41. T. J. Monroe, M. C. Muhlmann-Diaz, M. J. Kovach, J. O. Carlson, J. S. Bedford and B. J. Beaty, Stable transformation of a mosquito cell-line results in extraordinarily high copy numbers of the plasmid. Proc. Natl. Acad. Sci. USA 89, 5725-5729 (1992).
42. J. S. Bedford and M. C. Muhlmann-Diaz, Damage selectivity in chromosomes. In Radiation Research: A Twentieth Century Perspective (W. C. Dewey, M. Edington, R. J. M. Fry, E. J. Hall and G. F. Whitmore, Eds.), pp. 212-216. Academic Press, San Diego, 1992.
43. T. J. Monroe, M. C. Muhlmann-Díaz, M. J. Kovach, J. O. Carlson, J. S. Bedford and B. J. Beaty, Stable transformation of a mosquito cell line results in extraordinarily high copy numbers of plasmids. Proc. Natl. Acad. Sci. USA 89, 5725-5729 (1992).
44. M. C. Muhlmann-Diaz, R. G. Dullea and J. S. Bedford, Application of 5-bromo-2′deoxyuridine as a label for in situ hybridization in chromosome microdissection and painting, and 3′OH DNA end labeling for apoptosis. BioTechniques 21, 82-86 (1996).
45. 0 cells immediately after exposure to gamma-rays. Int. J. Radiat. Biol. 65, 165-173 (1994).
46. R. J. Amdur and J. S. Bedford, Dose-rate effects between 0.3 and 30 Gy/h in a normal and a malignant human cell line. Int. J. Radiat. Oncol. Biol. Phys. 30, 83-90 (1994).
47. M. R. Raju, Y. Eisen, S. Carpenter and W. C. Inkret, Radiobiology of alpha particles. III. Cell inactivation by alpha-particle traversals of the cell nucleus. Radiat. Res. 128, 204-209 (1991).
48. M. N. Cornforth and J. S. Bedford, X-ray induced breakage and rejoining of human interphase chromosomes. Science 222, 1141-1143 (1983).
49. M. N. Cornforth and J. S. Bedford, On the nature of a defect in cells from individuals with ataxia telangiectasia. Science 227, 1589-1591 (1985).
50. L. Metzger and G. Iliakis, Kinetics of DNA double-strand break repair throughout the cell cycle as assayed by pulsed field gel electrophoresis in CHO cells. Int. J. Radiat. Biol. 59, 1325-1339 (1991).
51. C. Badie, G. Iliakis, N. Foray, G. Alsbeih, B. Cedervall, N. Chavaudra, G. Pantelias, C. Arlett and E. P. Malaise, Induction and rejoining of DNA double-strand breaks and interphase chromosome breaks after exposure to X rays in one normal and two hypersensitive human fibroblast cell lines. Radiat. Res. 144, 26-35 (1995).
52. G. Iliakis, H. Wang, A. R. Perrault, W. Boecker, B. Rosidi, F. Windhofer, W. Wu, J. Guan, G. Terzoudi and G. Pantelias, Mechanisms of DNA double strand break repair and chromosome aberration formation. Cytogenet. Genome Res. 104, 14-20 (2004).
53. M. Lobrich and P. A. Jeggo, The two edges of the ATM sword: Cooperation between repair and checkpoint functions. Radiother. Oncol. 76, 112-118 (2005).
54. P. L. Olive, Detection of DNA damage in individual cells by analysis of histone H2AX phosphorylation. Methods Cell Biol. 75, 355-373 (2004).
55. E. Riballo, M. Kuhne, N. Rief, A. Doherty, G. C. Smith, M. J. Recio, C. Reis, K. Dahm, A. Fricke and M. Lobrich, A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Mol. Cell 16, 715-724 (2004).