Differences in phosphorylated histone H2AX foci formation and removal of cells exposed to low and high linear energy transfer radiation

Current Genomics

Volumn 13, Issue 6, 2012, Pages 418-425

  Schmid, Thomas Ernst ^a   Zlobinskaya, Olga ^a   Multhoff, Gabriele ^a,b  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

H2AX foci; DNA double strand breaks; Linear energy transfer; Radiation

Indexed keywords

HEAVY ION; HISTONE H2AX;

ACCURACY; ARTICLE; CARCINOGENESIS; CELL DEATH; CHROMOSOME ABERRATION; COMET ASSAY; DNA DAMAGE; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; GENE MUTATION; GENOMIC INSTABILITY; HUMAN; IONIZING RADIATION; LINEAR ENERGY TRANSFER; MICRONUCLEUS TEST; NICK END LABELING; PROTEIN PHOSPHORYLATION; RADIATION BEAM; RADIATION EXPOSURE;

EID: 84866680950     PISSN: 13892029     EISSN: 18755488     Source Type: Journal    
DOI: 10.2174/138920212802510501     Document Type: Article

References (68)

1. Ramaekers, B.L.; Pijls-Johannesma, M.; Joore, M.A.; van den Ende, P.; Langendijk, J.A.; Lambin, P.; Kessels, A.G.; Grutters, J.P. Systematic review and meta-analysis of radiotherapy in various head and neck cancers: comparing photons, carbon-ions and protons. Cancer Treat. Rev. 2011, 37 185-201.
2. Nakano, T.; Suzuki, M.; Abe, A.; Suzuki, Y.; Morita, S.; Mizoe, J.; Sato, S.; Miyamoto, T.; Kamada, T.; Kato, H.; Tsujii, H. The phase I/II clinical study of carbon ion therapy for cancer of the uterine cervix. Cancer J. Sci. Am. 1999, 5 362-369.
3. Weyrather, W.K.; Kraft, G. RBE of carbon ions: experimental data and the strategy of RBE calculation for treatment planning. Radiother. Oncol. 2004, 73 (Suppl 2) S161-169.
4. Kramer, M.; Scholz, M. Rapid calculation of biological effects in ion radiotherapy. Phys. Med. Biol. 2006, 51 1959-1970.
5. Wenzl, T.; Wilkens, J.J. Modelling of the oxygen enhancement ratio for ion beam radiation therapy. Phys. Med. Biol. 2011, 56 3251-3268.
6. Nomiya, T.; Tsuji, H.; Hirasawa, N.; Kato, H.; Kamada, T.; Mizoe, J.; Kishi, H.; Kamura, K.; Wada, H.; Nemoto, K.; Tsujii, H. Carbon Ion Radiation Therapy for Primary Renal Cell Carcinoma: Initial Clinical Experience. Int. J. Radiat. Oncol. Biol. Phys. 2008.
7. Kobayashi, J.; Iwabuchi, K.; Miyagawa, K.; Sonoda, E.; Suzuki, K.; Takata, M.; Tauchi, H. Current topics in DNA double-strand break repair. J. Radiat. Res. (Tokyo) 2008, 49 93-103.
8. Rothkamm, K.; Horn, S. gamma-H2AX as protein biomarker for radiation exposure. Ann Ist Super Sanita 2009, 45 265-271.
9. Wyman, C.; Kanaar, R. DNA double-strand break repair: all's well that ends well. Annu. Rev. Genet. 2006, 40 363-383.
10. Prise, K.M.; Pinto, M.; Newman, H.C.; Michael, B.D. A review of studies of ionizing radiation-induced double-strand break clustering. Radiat. Res. 2001, 156 572-576.
11. Hada, M.; Georgakilas, A.G. Formation of clustered DNA damage after high-LET irradiation: a review. J. Radiat. Res. (Tokyo) 2008, 49 203-210.
12. Jeggo, P.A.; Geuting, V.; Lobrich, M. The role of homologous recombination in radiation-induced double-strand break repair. Radiother. Oncol. 2011.
13. Rothkamm, K.; Balroop, S.; Shekhdar, J.; Fernie, P.; Goh, V. Leukocyte DNA damage after multi-detector row CT: a quantitative biomarker of low-level radiation exposure. Radiology 2007, 242 244-251.
14. Golfier, S.; Jost, G.; Pietsch, H.; Lengsfeld, P.; Eckardt-Schupp, F.; Schmid, E.; Voth, M. Dicentric chromosomes and gamma-H2AX foci formation in lymphocytes of human blood samples exposed to a CT scanner: a direct comparison of dose response relationships. Radiat. Prot. Dosimetry 2009, 134 55-61.
15. Lobrich, M.; Rief, N.; Kuhne, M.; Heckmann, M.; Fleckenstein, J.; Rube, C.; Uder, M. In vivo formation and repair of DNA doublestrand breaks after computed tomography examinations. Proc. Natl. Acad. Sci. U S A 2005, 102 8984-8989.
16. Cucinotta, F.A.; Pluth, J.M.; Anderson, J.A.; Harper, J.V.; O'Neill, P. Biochemical kinetics model of DSB repair and induction of gamma-H2AX foci by non-homologous end joining. Radiat Res 2008, 169 214-222.
17. Costes, S.V.; Chiolo, I.; Pluth, J.M.; Barcellos-Hoff, M.H.; Jakob, B. Spatiotemporal characterization of ionizing radiation induced DNA damage foci and their relation to chromatin organization. Mutat Res 2007, 704 78-87.
18. 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.
19. Jakob, B.; Splinter, J.; Conrad, S.; Voss, K.O.; Zink, D.; Durante, M.; Lobrich, M.; Taucher-Scholz, G. DNA double-strand breaks in heterochromatin elicit fast repair protein recruitment, histone H2AX phosphorylation and relocation to euchromatin. Nucleic Acids Res 2011.
20. Rothkamm, K.; Lobrich, M. Evidence for a lack of DNA doublestrand break repair in human cells exposed to very low x-ray doses. Proc Natl Acad Sci U S A 2003, 100 5057-5062.
21. Rogakou, E.P.; Boon, C.; Redon, C.; Bonner, W.M. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 1999, 146 905-916.
22. Asaithamby, A.; Hu, B.; Chen, D.J. Unrepaired clustered DNA lesions induce chromosome breakage in human cells. Proc Natl Acad Sci U S A 2011, 108 8293-8298.
23. Lees-Miller, S.P.; Meek, K. Repair of DNA double strand breaks by non-homologous end joining. Biochimie 2003, 85 1161-1173.
24. Ferguson, D.O.; Sekiguchi, J.M.; Chang, S.; Frank, K.M.; Gao, Y.; DePinho, R.A.; Alt, F.W. The nonhomologous end-joining pathway of DNA repair is required for genomic stability and the suppression of translocations. Proc Natl Acad Sci U S A 2000, 97 6630-6633.
25. Mladenov, E.; Kalev, P.; Anachkova, B. The complexity of doublestrand break ends is a factor in the repair pathway choice. Radiat. Res. 2009, 171 397-404.
26. Ismail, I.H.; Wadhra, T.I.; Hammarsten, O. An optimized method for detecting gamma-H2AX in blood cells reveals a significant interindividual variation in the gamma-H2AX response among humans. Nucleic Acids Re. s 2007, 35 e36.
27. Bocker, W.; Iliakis, G. Computational Methods for analysis of foci: validation for radiation-induced gamma-H2AX foci in human cells. Radiat. Res. 2006, 165 113-124.
28. MacPhail, S.H.; Banath, J.P.; Yu, T.Y.; Chu, E.H.; Lambur, H.; Olive, P.L. Expression of phosphorylated histone H2AX in cultured cell lines following exposure to X-rays. Int. J. Radiat. Biol. 2003, 79 351-358.
29. Yu, T.; MacPhail, S.H.; Banath, J.P.; Klokov, D.; Olive, P.L. Endogenous expression of phosphorylated histone H2AX in tumors in relation to DNA double-strand breaks and genomic instability. DNA Repair (Amst) 2006, 5 935-946.
30. Chowdhury, D.; Keogh, M.C.; Ishii, H.; Peterson, C.L.; Buratowski, S.; Lieberman, J. gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol. Cell 2005, 20 801-809.
31. Speit, G.; Hartmann, A. The comet assay (single-cell gel test). A sensitive genotoxicity test for the detection of DNA damage and repair. Methods Mol. Biol. 1999, 113 203-212.
32. Huang, X.; Kurose, A.; Tanaka, T.; Traganos, F.; Dai, W.; Darzynkiewicz, Z. Sequential phosphorylation of Ser-10 on histone H3 and ser-139 on histone H2AX and ATM activation during premature chromosome condensation: relationship to cell-cycle phase and apoptosis. Cytometry A 2006, 69 222-229.
33. Darzynkiewicz, Z.; Huang, X.; Okafuji, M. Detection of DNA strand breaks by flow and laser scanning cytometry in studies of apoptosis and cell proliferation (DNA replication). Methods Mol. Biol. 2006, 314 81-93.
34. Schmid, T.E.; Dollinger, G.; Beisker, W.; Hable, V.; Greubel, C.; Auer, S.; Mittag, A.; Tarnok, A.; Friedl, A.A.; Molls, M.; Roper, B. Differences in the kinetics of gamma-H2AX fluorescence decay after exposure to low and high LET radiation. Int. J. Radiat. Biol. 2010, 86 682-691.
35. Huang, X.; Okafuji, M.; Traganos, F.; Luther, E.; Holden, E.; Darzynkiewicz, Z. Assessment of histone H2AX phosphorylation induced by DNA topoisomerase I and II inhibitors topotecan and mitoxantrone and by the DNA cross-linking agent cisplatin. Cytometry A 2004, 58 99-110.
36. Whalen, M.K.; Gurai, S.K.; Zahed-Kargaran, H.; Pluth, J.M. Specific ATM-mediated phosphorylation dependent on radiation quality. Radiat. Res. 2008, 170 353-364.
37. Olive, P.L.; Banath, J.P. Detection of DNA double-strand breaks through the cell cycle after exposure to X-rays, bleomycin, etoposide and 125IdUrd. Int. J. Radiat. Biol. 1993, 64 349-358.
38. Banath, J.P.; Macphail, S.H.; Olive, P.L. Radiation sensitivity, H2AX phosphorylation, and kinetics of repair of DNA strand breaks in irradiated cervical cancer cell lines. Cancer Res. 2004, 64 7144-7149.
39. Hauptner, A.; Friedland, W.; Dietzel, S.; Drexler, G.A.; Greubel, C.; Hable, V.; Strickfaden, H.; Cremer, T.; Friedl, A.A.; Krücken, R.; Paretzke, H.G.; Dollinger, G., Spatial distribution of DNA double-strand breaks from ion tracks. In Ion Beam Science: Solved and Unsolved Problems Sigmund, P., Ed. Danish Academy of Sciences and Letters: Copenhagen, 2006; pp 59-85.
40. Desai, N.; Davis, E.; O'Neill, P.; Durante, M.; Cucinotta, F.A.; Wu, H. Immunofluorescence detection of clustered gamma-H2AX foci induced by HZE-particle radiation. Radiat. Res. 2005, 164 518-522.
41. Goodarzi, A.A.; Jeggo, P.; Lobrich, M. The influence of heterochromatin on DNA double strand break repair: Getting the strong, silent type to relax. DNA Repair (Amst) 2010, 9 1273-1282.
42. Zafar, F.; Seidler, S.B.; Kronenberg, A.; Schild, D.; Wiese, C. Homologous recombination contributes to the repair of DNA double-strand breaks induced by high-energy iron ions. Radiat. Res. 2010, 173 27-39.
43. Karlsson, K.H.; Stenerlow, B. Focus formation of DNA repair proteins in normal and repair-deficient cells irradiated with high-LET ions. Radiat. Res. 2004, 161 517-527.
44. Leatherbarrow, E.L.; Harper, J.V.; Cucinotta, F.A.; O'Neill, P. Induction and quantification of gamma-H2AX foci following low and high LET-irradiation. Int. J. Radiat. Biol. 2006, 82 111-118.
45. Jenner, T.J.; deLara, C.M.; O'Neill, P.; Stevens, D.L. Induction and rejoining of DNA double-strand breaks in V79-4 mammalian cells following gamma-and alpha-irradiation. Int. J. Radiat. Biol. 1993, 64 265-273.
46. Hofman-Huther, H.; Scholz, M.; Rave-Frank, M.; Virsik-Kopp, P. Induction of reproductive cell death and chromosome aberrations in radioresistant tumour cells by carbon ions. Int. J. Radiat. Biol. 2004, 80 423-435.
47. Durante, M.; Furusawa, Y.; George, K.; Gialanella, G.; Greco, O.; Grossi, G.; Matsufuji, N.; Pugliese, M.; Yang, T.C. Rejoining and misrejoining of radiation-induced chromatin breaks. IV. Charged particles. Radiat. Res. 1998, 149 446-454.
48. Loucas, B.D.; Cornforth, M.N. Complex chromosome exchanges induced by gamma rays in human lymphocytes: an mFISH study. Radiat. Res. 2001, 155 660-671.
49. Darroudi, F.; Bezrookove, V.; Fomina, J.; Mesker, W.E.; Wiegant, J.C.; Raap, A.K.; Tanke, H.J. Insights into the sites of X ray and neutron induced chromosomal aberrations in human lymphocytes using COBRA-MFISH. Radiat. Prot. Dosimetry 2002, 99 189-192.
50. Durante, M.; George, K.; Wu, H.; Cucinotta, F.A. Karyotypes of human lymphocytes exposed to high-energy iron ions. Radiat. Res. 2002, 158 581-590.
51. Yamamoto, N.; Ikeda, C.; Yakushiji, T.; Nomura, T.; Katakura, A.; Shibahara, T.; Mizoe, J.E. Genetic effects of X-ray and carbon ion irradiation in head and neck carcinoma cell lines. Bull. Tokyo Dent. Coll. 2007, 48 177-185.
52. Fowler, J.F. Is repair of DNA strand break damage from ionizing radiation second-order rather than first-order? A simpler explanation of apparently multiexponential repair. Radiat. Res. 1999, 152 124-136.
53. Haines, G.A.; Hendry, J.H.; Daniel, C.P.; Morris, I.D. Germ cell and dose-dependent DNA damage measured by the comet assay in murine spermatozoaa after testicular X-irradiation. Biol. Reprod. 2002, 67 854-861.
54. Rössler, U.; Hornhardt, S.; Seidl, C.; Müller-Laue, E.; Walsh, L.; Panzer, W.; Schmid, E.; Senekowitsch-Schmidtke, R.; Gomolka, M. The sensitivity of the alkaline comet assay in detecting DNA lesions induced by X rays, gamma rays and alpha particles. Radiation protection dosimetry 2006, 122 154-159.
55. Menz, R.; Andres, R.; Larsson, B.; Ozsahin, M.; Trott, K.; Crompton, N.E. Biological dosimetry: the potential use of radiation-induced apoptosis in human T-lymphocytes. Radiat. Environ. Biophys. 1997, 36 175-181.
56. Charriaut-Marlangue, C.; Ben-Ari, Y. A cautionary note on the use of the TUNEL stain to determine apoptosis. Neuroreport. 1995, 7 61-64.
57. Huerta, S.; Goulet, E.J.; Huerta-Yepez, S.; Livingston, E.H. Screening and Detection of Apoptosis. Journal of Surgical Research 2007, 139 143-156.
58. Franken, N.A.P.; Rodermond, H.M.; Stap, J.; Haveman, J.; van Bree, C. Clonogenic assay of cells in vitro. Nat. Protocols 2006, 1 2315-2319.
59. West, C.M.; Davidson, S.E.; Roberts, S.A.; Hunter, R.D. The independence of intrinsic radiosensitivity as a prognostic factor for patient response to radiotherapy of carcinoma of the cervix. Br. J. Cancer. 1997, 76 1184-1190.
60. Haikonen, J.; Rantanen, V.; Pekkola, K.; Kulmala, J.; Grenman, R. Does skin fibroblast radiosensitivity predict squamous cancer cell radiosensitivity of the same individual? Int. J. Cancer 2003, 103 784-788.
61. Oppitz, U.; Schulte, S.; Stopper, H.; Baier, K.; Muller, M.; Wulf, J.; Schakowski, R.; Flentje, M. In vitro radiosensitivity measured in lymphocytes and fibroblasts by colony formation and comet assay: comparison with clinical acute reactions to radiotherapy in breast cancer patients. Int. J. Radiat. Biol. 2002, 78 611-616.
62. Lindstrom, M.J.; Kunugi, K.A.; Kinsella, T.J. Global comparison of radiation and chemotherapy dose-response curves with a test for interaction. Radiat. Res. 1993, 135 269-277.
63. Span, L.F.; Pennings, A.H.; Vierwinden, G.; Boezeman, J.B.; Raymakers, R.A.; de Witte, T. The dynamic process of apoptosis analyzed by flow cytometry using Annexin-V/propidium iodide and a modified in situ end labeling technique. Cytometry 2002, 47 24-31.
64. Kern, P.; Keilholz, L.; Forster, C.; Seegenschmiedt, M.H.; Sauer, R.; Herrmann, M. In vitro apoptosis in peripheral blood mononuclear cells induced by low-dose radiotherapy displays a discontinuous dose-dependence. Int. J. Radiat. Biol. 1999, 75 995-1003.
65. Willems, P.; August, L.; Slabbert, J.; Romm, H.; Oestreicher, U.; Thierens, H.; Vral, A. Automated micronucleus (MN) scoring for population triage in case of large scale radiation events. Int. J. Radiat. Biol. 2010, 86 2-11.
66. Vral, A.; Fenech, M.; Thierens, H. The micronucleus assay as a biological dosimeter of in vivo ionising radiation exposure. Mutagenesis 2011, 26 11-17.
67. Leonard, A.; Rueff, J.; Gerber, G.B.; Leonard, E.D. Usefulness and limits of biological dosimetry based on cytogenetic methods. Radiat. Prot. Dosimetry 2005, 115 448-454.
68. Bonner, W.M.; Redon, C.E.; Dickey, J.S.; Nakamura, A.J.; Sedelnikova, O.A.; Solier, S.; Pommier, Y. [gamma]H2AX and cancer. Nat. Rev. Cancer 2008, 8 957-967.