Cell cycle perturbations and genotoxic effects in human primary fibroblasts induced by low-energy protons and X/γ-rays

Journal of Radiation Research

Volumn 50, Issue 5, 2009, Pages 457-468

  Antoccia, Antonio ^a,b   Sgura, Antonella ^a,b   Berardinelli, Francesco ^a,b   Cavinato, Maria ^c   Cherubini, Roberto ^c   Gerardi, Silvia ^c   Tanzarella, Caterina ^a,b  

^a ROMA TRE UNIVERSITY   (Italy)

^b INFN SEZIONE DI ROMA   (Italy)

^c LABORATORI NAZIONALI DI LEGNARO   (Italy)

Author keywords

CDKN1A; Cell cycle redistribution; Protons; TP53; H2AX

Indexed keywords

ENERGY TRANSFER; FIBROBLASTS; GAMMA RAYS; IRRADIATION;

CDKN1A; CELL CYCLE; CELL-CYCLE REDISTRIBUTION; DNA DAMAGES; GENOTOXIC EFFECTS; LINEAR ENERGY TRANSFER; LOW-ENERGY PROTONS; PERTURBATION EFFECT; TP53; Γ-H2AX;

CELL CULTURE;

CELL CYCLE PROTEIN; PROTON;

ARTICLE; CELL CULTURE; CELL CYCLE; CYTOLOGY; DNA DAMAGE; FIBROBLAST; GAMMA RADIATION; HUMAN; METABOLISM; PHYSIOLOGY; RADIATION DOSE; RADIATION EXPOSURE; RADIATION RESPONSE; X RAY;

CELL CYCLE; CELL CYCLE PROTEINS; CELLS, CULTURED; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, RADIATION; FIBROBLASTS; GAMMA RAYS; HUMANS; PROTONS; RADIATION DOSAGE; X-RAYS;

EID: 71749120165     PISSN: 04493060     EISSN: 13499157     Source Type: Journal    
DOI: 10.1269/jrr.09008     Document Type: Article

References (53)

1. Goodhead, D. T., Thacker, J. and Cox, R. (1993) Effects of radiations of different qualities on cells: molecular mechanisms of damage and repair. Int. J. Radiat. Biol. 63: 543-556.
2. Ward, J. F. (1994) The complexity of DNA damage: relevance to biological consequences. Int. J. Radiat. Biol. 66: 427-432.
3. Belli, M., Cherubini, R., Finotto, S., Moschini, G., Sapora, O., Simone, G. and Tabocchini, M. A. (1989) RBE-LET relationship for the survival of V79 cells irradiated with low energy protons. Int. J. Radiat. Biol. 55: 93-104.
4. Belli, M., Cera, F., Cherubini, R., Ianzini, F., Moschini, G., Sapora, O., Simone, G., Tabocchini, M. A. and Tiveron, P. (1991) Mutation induction and RBE-LET relationship of low-energy protons in V79 cells. Int. J. Radiat. Biol. 59: 459-465.
5. Belli, M., Cera, F., Cherubini, R., Dalla Vecchia, M., Haque, A. M., Ianzini, F., Moschini, G., Sapora, O., Simone, G., Tabocchini, M. A. and Tiveron, P. (1998) RBE-LET relationships for cell inactivation and mutation induced by low energy protons in V79 cells: further results at the LNL facility. Int. J. Radiat. Biol. 74: 501-509.
6. Mognato, M., Bortoletto, E., Ferraro, P., Baggio, L., Cherubini, R., Canova, S., Russo, A. and Celotti, L. (2003) Genetic damage induced by in vitro irradiation of human G0 lymphocytes with low-energy protons (28 keV/microm): HPRT mutations and chromosome aberrations. Radiat. Res. 160: 52-60.
7. Sgura, A., Antoccia, A., Cherubini, R., Dalla Vecchia, M., Tiveron, P., Degrassi, F. and Tanzarella, C. (2000) Micronuclei, CREST-positive micronuclei and cell inactivation induced in Chinese hamster cells by radiation with different quality. Int. J. Radiat. Biol. 76: 367-374.
8. Sgura, A., Antoccia, A., Cherubini, R. and Tanzarella, C. (2001) Chromosome nondisjunction and loss induced by protons and X rays in primary human fibroblasts: role of centromeres in aneuploidy. Radiat. Res. 156: 225-231.
9. Campa, A., Esposito, G., Belli, M., Simone, G. and Tabocchini, M. A. (2004) DNA fragmentation in V79 cells irradiated with light ions as measured by pulsed-field gel electrophoresis. II. Simulation with a generalized broken stick model. Int. J. Radiat. Biol. 80: 229-238.
10. Esposito, G., Belli, M., Campa, A., Cherubini, R., Cuttone, G., Dini, V., Furusawa, Y., Gerardi, S., Simone, G., Sorrentino, E. and Tabocchini, M. A. (2006) DNA fragments induction in human fibroblasts by radiations of different qualities. Radiat. Prot. Dosimetry. 122: 166-168.
11. Ianzini, F. and Mackey, M. A. (1997) Spontaneous premature chromosome condensation and mitotic catastrophe following irradiation of HeLa S3 cells. Int. J. Radiat. Biol. 72: 409-421.
12. Belli, M., Bettega, D., Calzolari, P., Cera, F., Cherubini, R., Dalla Vecchia, M., Durante, M., Favaretto, S., Gialanella, G., Grossi, G., Marchesini, R., Moschini, G., Piazzola, A., Poli, G., Pugliese, M., Sapora, O., Scampoli, P., Simone, G., Sorrentino, E., Tabocchini, M. A., Tallone, L. and Tiveron, P. (2000) Inactivation of human normal and tumour cells irradiated with low energy protons. Int. J. Radiat. Biol. 76: 831-839.
13. Bettega, D., Calzolari, P., Marchesini, R., Noris Chiorda, G. L., Piazzolla, A., Tallone, L., Cera, F., Cherubini, R., Dalla Vecchia, M., Favaretto, S. and Tiveron, P. (1998) Inactivation of C3H10T1/2 cells by low energy protons and deuterons. Int. J. Radiat. Biol. 73: 303-309.
14. Antoccia, A., Sgura, A., Cavinato, M., Cherubini, R. and Tanzarella, C. (2002) Cell cycle perturbations and cytogenetic damage induced by low energy protons in human primary fibroblasts. Radiat. Prot. Dosimetry. 99: 197-198.
15. Terasima, T. and Tolmach, L. J. (1963) Variations in several responses of HeLa cells to x-irradiation during the division cycle. Biophys. J. 3: 11-33.
16. Blakely, E. A. and Kronenberg, A. (1998) Heavy-ion radiobiology: new approaches to delineate mechanisms underlying enhanced biological effectiveness. Radiat. Res. 150: S126-145.
17. Dulic, V., Kaufmann, W. K., Wilson, S. J., Tlsty, T. D., Lees, E., Harper, J. W., Elledge, S. J. and Reed, S. I. (1994) p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell 76: 1013-1023.
18. Harper, J. W., Adami, G. R., Wei, N., Keyomarsi, K. and Elledge, S. J. (1993) The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75: 805-816.
19. El-Deiry, W. S., Harper, J. W., O'Connor, P. M., Velculescu, V. E., Canman, C. E., Jackman, J., Pietenpol, J. A., Burrell, M., Hill, D. E., Wang, Y., Wiman, K. G., Mercer, W. E., Kastan, M. B., Khon, K. W., Elledge, S. J., Kinzler, K. W. and Vogelstein, B. (1994) WAF1/CIP1 is induced in p53-mediated G1 arrest and apoptosis. Cancer Res. 54: 1169-1174.
20. Lucke-Huhle, C., Blakely, E. A., Chang, P. Y. and Tobias, C. A. (1979) Drastic G2 arrest in mammalian cells after irradiation with heavy-ion beams. Radiat. Res. 79: 97-112.
21. Scholz, M., Kraft-Weyrather, W., Ritter, S. and Kraft, G. (1994) Cell cycle delays induced by heavy ion irradiation of synchronous mammalian cells. Int. J. Radiat. Biol. 66: 59-75.
22. Iwadate, Y., Mizoe, J., Osaka, Y., Yamaura, A. and Tsujii, H. (2001) High linear energy transfer carbon radiation effectively kills cultured glioma cells with either mutant or wild-type p53. Int. J. Radiat. Oncol. Biol. Phys. 50: 803-808.
23. Fournier, C. and Taucher-Scholz, G. (2004) Radiation induced cell cycle arrest: an overview of specific effects following high-LET exposure. Radiother. Oncol. 73 Suppl 2: S119-S122.
24. Agarwal, M. L., Agarwal, A., Taylor, W. R. and Stark, G. R. (1995) p53 controls both the G2/M and the G1 cell cycle checkpoints and mediates reversible growth arrest in human fibroblasts. Proc. Natl. Acad. Sci. U. S. A. 92: 8493-8497.
25. Nasonova, E. A. and Ritter, S. (2004) Cytogenetic effects of densely ionising radiation in human lymphocytes: impact of cell cycle delays. Cytogenet. Genome Res. 104: 216-220.
26. Tenhumberg, S., Gudowska-Nowak, E., Nasonova, E. and Ritter, S. (2007) Cell cycle arrest and aberration yield in normal human fibroblasts. II: Effects of 11 MeV u-1 C ions and 9. 9 MeV u-1 Ni ions. Int. J. Radiat. Biol. 83: 501-513.
27. Gadbois, D. M., Crissman, H. A., Nastasi, A., Habbersett, R., Wang, S. K., Chen, D. and Lehnert, B. E. (1996) Alterations in the progression of cells through the cell cycle after exposure to alpha particles or gamma rays. Radiat. Res. 146: 414-424.
28. Azzam, E. I., de Toledo, S. M., Waker, A. J. and Little, J. B. (2000) High and low fluences of alpha-particles induce a G1 checkpoint in human diploid fibroblasts. Cancer Res. 60: 2623-2631.
29. Di Leonardo, A., Linke, S. P., Clarkin, K. and Wahl, G. M. (1994) DNA damage triggers a prolonged p53-dependent G1 arrest and long-term induction of Cip1 in normal human fibro-blasts. Genes Dev. 8: 2540-2551.
30. Linke, S. P., Clarkin, K. C. and Wahl, G. M. (1997) p53 mediates permanent arrest over multiple cell cycles in response to gamma-irradiation. Cancer Res. 57: 1171-1179.
31. Suzuki, K., Mori, I., Nakayama, Y., Miyakoda, M., Kodama, S. and Watanabe, M. (2001) Radiation-induced senescence-like growth arrest requires TP53 function but not telomere shortening. Radiat. Res. 155: 248-253.
32. Fournier, C., Winter, M., Zahnreich, S., Nasonova, E., Melnikova, L. and Ritter, S. (2007) Interrelation amongst differentiation, senescence and genetic instability in long-term cultures of fibroblasts exposed to different radiation qualities. Radiother. Oncol. 83: 277-282.
33. Goto, S., Watanabe, M. and Yatagai, F. (2002) Delayed cell cycle progression in human lymphoblastoid cells after exposure to high-LET radiation correlates with extremely localized DNA damage. Radiat. Res. 158: 678-686.
34. Desai, N., Davis, E., O'Neill, P., Durante, M., Cucinotta, F. A. and Wu, H. (2005) Immunofluorescence detection of clustered gamma-H2AX foci induced by HZE-particle radiation. Radiat. Res. 164: 518-522.
35. Rogakou, E. P., Pilch, D. R., Orr, A. H., Ivanova, V. S. and Bonner, W. M. (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273: 5858-5868.
36. Paull, T. T., Rogakou, E. P., Yamazaki, V., Kirchgessner, C. U., Gellert, M. and Bonner, W. M. (2000) A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10: 886-895.
37. Antonelli, F., Belli, M., Cuttone, G., Dini, V., Esposito, G., Simone, G., Sorrentino, E. and Tabocchini, M. A. (2005) Induction and repair of DNA double-strand breaks in human cells: dephosphorylation of histone H2AX and its inhibition by calyculin A. Radiat. Res. 164: 514-517.
38. Mukherjee, B., Camacho, C. V., Tomimatsu, N., Miller, J., Burma, S. (2008) Modulation of the DNA-damage response to HZE particles by shielding. DNA Repair 7: 1717-1730.
39. MacPhail, S. H., Banath, J. P., Yu, T. Y., Chu, E. H., Lambur, H. and Olive, P. L. (2003) Expression of phosphorylated histone H2AX in cultured cell lines following exposure to X-rays. Int. J. Radiat. Biol. 79: 351-358.
40. Fenech, M. and Morley, A. A. (1985) Measurement of micro-nuclei in lymphocytes. Mutat. Res. 147: 29-36.
41. Belli, M., Cherubini, R., Galeazzi, G., Mazzucato, S., Moschini, G., Sapora, O., Simone, G. and Tabacchini, M. A. (1987) Proton irradiation facility for radiobiological studies at a 7 MV Van de Graaff accelerator. Nucl. Instr. and Meth. A. 256: 576-580.
42. Belli, M., Cera, F., Cherubini, R., Haque, A. M., Ianzini, F., Moschini, G., Sapora, O., Simone, G., Tabocchini, M. A. and Tiveron, P. (1993) Inactivation and mutation-inducton in V79 cells by low-energy protons re-evaluation of the results at LNL-facility. Int. J. Radiat. Biol. 63: 331-337.
43. Belli, M., Bettega, D., Calzolari, P., Cherubini, R., Cuttone, G., Durante, M., Esposito, G., Furusawa, Y., Gerardi, S., Gialanella, G., Grossi, G., Manti, L., Marchesini, R., Pugliese, M., Scampoli, P., Simone, G., Sorrentino, E., Tabocchini, M. A., Tallone, L. (2008) Effectiveness of monoenergetic and spread-out Bragg peak carbon-ions for inactivation of various normal and tumour human cell lines. J. Radiat. Res. 49: 597-607.
44. Fournier, C., Wiese, C. and Taucher-Scholz, G. (2004) Accumulation of the cell cycle regulators TP53 and CDKN1A (p21) in human fibroblasts after exposure to low- and high-LET radiation. Radiat. Res. 161: 675-684.
45. Lucke-Huhle, C. (1982) Alpha-irradiation-induced G2 delay: a period of cell recovery. Radiat. Res. 89: 298-308.
46. Noda, A., Ning, Y., Venable, S. F., Pereira-Smith, O. M. and Smith, J. R. (1994) Cloning of senescent cell-derived inhibitors of DNA synthesis using an expression screen. Exp. Cell Res. 211: 90-98.
47. Zhou, T., Chou, J. W., Simpson, D. A., Zhou, Y., Mullen, T. E., Medeiros, M., Bushel, P. R., Paules, R. S., Yang, X., Hurban, P., Lobenhofer, E. K. and Kaufmann, W. K. (2006) Profiles of global gene expression in ionizing-radiation-damaged human diploid fibroblasts reveal synchronization behind the G1 checkpoint in a G0-like state of quiescence. Environ. Health Perspect. 114: 553-559.
48. Rodemann, H. P., Peterson, H. P., Schwenke, K. and von Wangenheim, K. H. (1991) Terminal differentiation of human fibroblasts is induced by radiation. Scanning Microsc. 5: 1135-1142.
49. Stein, G. H., Drullinger, L. F., Soulard, A. and Dulic, V. (1999) Differential roles for cyclin-dependent kinase inhibitors p21 and p16 in the mechanisms of senescence and differentiation in human fibroblasts. Mol. Cell Biol. 19: 2109-2117.
50. Fournier, C., Scholz, M., Weyrather, W. K., Rodemann, H. P. and Kraft, G. (2001) Changes of fibrosis-related parameters after high- and low-LET irradiation of fibroblasts. Int. J. Radiat. Biol. 77: 713-722.
51. Kegel, P., Riballo, E., Kühne, M., Jeggo, P. A., Löbrich, M. (2007) X-irradiation of cells on glass slides has a dose doubling impact. DNA Repair 6: 1692-1697.
52. Kinner, A., Wu, W., Staudt, C., Iliakis, G. (2008) Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 36: 5678-5694.
53. Wu, H., Hada, M., Meador, J., Hu, X., Rusek, A. and Cucinotta, F. A. (2006) Induction of micronuclei in human fibroblasts across the Bragg curve of energetic heavy ions. Radiat. Res. 166: 583-589.