The TP53 dependence of radiation-induced chromosome instability in human lymphoblastoid cells

Radiation Research

Volumn 159, Issue 6, 2003, Pages 730-736

  Schwartz, Jeffrey L ^a   Jordan, Robert ^a   Evans, Helen H ^b   Lenarczyk, Marek ^c   Liber, Howard ^c  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

CESIUM 137;

ANEUPLOIDY; APOPTOSIS; ARTICLE; CELL CULTURE; CELL CYCLE; CELL ISOLATION; CELL SURVIVAL; CHROMOSOME ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; CULTURE MEDIUM; CYTOGENETICS; DOSE RESPONSE; GENETIC STABILITY; HUMAN; HUMAN CELL; LYMPHOBLASTOID CELL; PRIORITY JOURNAL; RADIATION DOSE; TELOMERE;

NASA DISCIPLINE RADIATION HEALTH; NON-NASA CENTER;

APOPTOSIS; CELLS, CULTURED; CHROMOSOME ABERRATIONS; DOSE-RESPONSE RELATIONSHIP, RADIATION; G1 PHASE; HUMANS; LYMPHOCYTES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0037643491     PISSN: 00337587     EISSN: None     Source Type: Journal    
DOI: 10.1667/RR3005     Document Type: Article

References (56)

1. C. Ducray, J. P. Pommier, L. Martins, F. D. Boussin and L. Sabatier, Telomere dynamics, end-to-end fusions and telomerase activation during the human fibroblast immortalization process. Oncogene 18, 4211-4223 (1999).
2. R. Aledo, A. Aurias, M. F. Avril and B. Dutrillaux, Jumping end-to-end dicentrics in a case of squamous cell carcinoma from a patient with xeroderma pigmentosum. Cancer Genet. Cytogenet. 40, 95-103 (1989).
3. G. Bardi, N. Pandis, N. Mandahl, S. Heim, K. Sfikas, H. Willen, G. Panagiotopoulos, A. Rydholm and F. Mitelman, Chromosomal abnormalities in giant cell tumors of bone. Cancer Genet. Cytogenet. 57, 161-167 (1991).
4. J. P. Park, J. R. Dossu and C. H. Rhodes, Telomere associations in desmoplastic infantile ganglioglioma. Cancer Genet. Cytogenet. 92, 4-7 (1996).
5. M. H. Zheng, P. Siu, J. M. Papadimitriou, D. J. Wood and A. R. Murch, Telomeric fusion is a major cytogenetic aberration of giant cell tumors of bone. Pathology 31, 373-378 (1999).
6. G. L. Nicolson, Tumor cell instability, diversification, and progression to the metastatic phenotype: From oncogene to oncofetal expression. Cancer Res. 47, 1473-1487 (1987).
7. N. J. Duker, Chromosome breakage syndromes and cancer. Am. J. Med. Genet. 115, 125-129 (2002).
8. S. J. Xia, M. A. Shammas and R. J. Shmookler Reis, Reduced telomere length in ataxia-telangiectasia fibroblasts. Mutat. Res. 364, 1-11 (1996).
9. J. A. Metcalfe, J. Parkhill, L. Campbell, M. Stacey, P. Biggs, P. J. Byrd and A. M. Taylor, Accelerated telomere shortening in ataxia telangiectasia. Nat. Genet. 13, 350-353 (1996).
10. W. K. Kaufmann, J. L. Schwartz, J. C. Hurt, L. L. Byrd, D. A. Galloway, E. Levedakou and R. S. Paules, Inactivation of G2 check-point function and chromosomal destabilization are linked in human fibroblasts expressing human papillomavirus type 16 E6. Cell Growth Differ. 8, 1105-1114 (1997).
11. F. A. Ray, J. Meyne and P. M. Kraemer, SV40 T antigen induced chromosomal changes reflect a process that is both clastogenic and aneuploidogenic and is ongoing throughout neoplastic progression of human fibroblasts. Mutat. Res. 284, 265-273 (1992).
12. J. L. Schwartz, R. Jordan, H. Liber, J. P. Murnane and H. H. Evans, Tp53-dependent chromosome instability is associated with transient reductions in telomere length in immortal telomerase-positive cell lines. Genes Chromosomes Cancer 30, 236-244 (2001).
13. L. Sabatier, J. Lebeau and B. Dutrillaux, Chromosomal instability and alterations of telomeric repeats in irradiated human fibroblasts. Int. J. Radiat. Biol. 66, 611-613 (1994).
14. 137Cs gamma radiation. Radiat. Res. 156, 259-271 (2001).
15. J. Campisi, S. H. Kim, C. S. Lim and M. Rubio, Cellular senescence, cancer and aging: The telomere connection. Exp. Gerontol. 36, 1619-1637 (2001).
16. S. M. Bailey, J. Meyne, D. J. Chen, A. Kurimasa, G. C. Li, B. E. Lehnert and E. H. Goodwin, DNA double-strand break repair proteins are required to cap the ends of mammalian chromosomes. Proc. Natl. Acad. Sci. USA 96, 14899-14904 (1999).
17. J. D. Griffith, L. Comeau, S. Rosenfield, R. M. Stansel, A. Bianchi, H. Moss and T. de Lange, Mammalian telomeres end in a large duplex loop. Cell 97, 503-514 (1999).
18. J. Karlseder, D. Broccoli, Y. Dai, S. Hardy and T. de Lange, P53-and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science 283, 1321-1325 (1999).
19. B. van Steensel, A. Smogorzewska and T. de Lange, TRF2 protects human telomeres from end-to-end fusions. Cell 92, 401-413 (1998).
20. R. Riboni, A. Casati, T. Nardo, E. Zaccaro, L. Ferretti, F. Nuzzo and C. Mondello, Telomeric fusions in cultured human fibroblasts as a source of genomic instability. Cancer Genet. Cytogenet. 95, 130-136 (1997).
21. C. M. Counter, A. A. Avilion, C. E. LeFeuvre, N. G. Stewart, C. W. Greider, C. B. Harley and S. Bacchetti, Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J. 11, 1921-1929 (1992).
22. C. B. Harley, Telomere loss: Mitotic clock or genetic time bomb? Mutat. Res. 256, 271-282 (1991).
23. L. Filatov, V. Golubovskaya, J. C. Hurt, L. L. Byrd, J. M. Phillips and W. K. Kaufmann, Chromosomal instability is correlated with telomere erosion and inactivation of G2 checkpoint function in human fibroblasts expressing human papillomavirus type 16 E6 oncoprotein. Oncogene 16, 1825-1838 (1998).
24. L. Chin, S. E. Artandi, Q. Shen, A. Tam, S. L. Lee, G. J. Gottlieb, C. W. Greider and R. A. DePinho, P53 deficiency rescues the adverse effects of telomere loss and cooperates with telomere dysfunction to accelerate carcinogenesis. Cell 97, 527-538 (1999).
25. A. Smogorzewska and T. de Lange, Different telomere damage signaling pathways in human and mouse cells. EMBO J. 21, 4338-4348 (2002).
26. 56Fe particles. Radiat. Res. 159, 737-747 (2003).
27. F. Xia, X. Wang, Y. H. Wang, N. M. Tsang, D. W. Yandell, K. T. Kelsey and H. L. Liber, Altered p53 status correlates with differences in sensitivity to radiation-induced mutation and apoptosis in two closely related human lymphoblast lines. Cancer Res. 55, 12-15 (1995).
28. Y. Peng, Q. Zhang, H. Nagasawa, R. Okayasu, H. L. Liber and J. S. Bedford, Silencing expression of the catalytic subunit of DNA-dependent protein kinase by small interfering RNA sensitizes human cells for radiation-induced chromosome damage, cell killing, and mutation. Cancer Res. 62, 6400-6404 (2002).
29. Y. Y. Chuang, Q. Chen, J. P. Brown, J. M. Sedivy and H. L. Liber, Radiation-induced mutations at the autosomal thymidine kinase locus are not elevated in p53-null cells. Cancer Res. 59 3073-6 (1999).
30. J. A. Levy, M. Virolainen and V. Defendi, Human lymphoblastoid lines from lymph node and spleen. Cancer 22, 517-524 (1968).
31. K. R. Loeb and L. A. Loeb, Significance of multiple mutations in cancer. Carcinogenesis 21, 379-385 (2000).
32. K. C. Cheng and L. A. Loeb, Genomic instability and tumor progression: Mechanistic considerations. Adv. Cancer Res. 60, 121-156 (1993).
33. A. Kronenberg, Radiation-induced genomic instability. Int. J. Radiat. Biol. 66, 603-609 (1994).
34. W. F. Morgan, J. P. Day, M. I. Kaplan, E. M. McGhee and C. L. Limoli, Genomic instability induced by ionizing radiation. Radiat. Res. 146, 247-258 (1996).
35. C. Mothersill and C. Seymour, Lethal mutations and genomic instability. Int. J. Radiat. Biol. 71, 751-758 (1997).
36. E. G. Wright, Radiation-induced genomic instability in haemopoietic cells: Implications for radiation pathology. Radiat. Oncol. Investig. 5, 115-118 (1997).
37. C. Mothersill and C. B. Seymour, Mechanisms and implications of genomic instability and other delayed effects of ionizing radiation exposure. Mutagenesis 13, 421-426 (1998).
38. C. L. Limoli, M. I. Kaplan, E. Giedzinski and W. F. Morgan, Attenuation of radiation-induced genomic instability by free radical scavengers and cellular proliferation. Free Radic. Biol. Med. 31, 10-19 (2001).
39. C. L. Limoli, B. Ponnaiya, J. J. Corcoran, E. Giedzinski and W. F. Morgan, Chromosomal instability induced by heavy ion irradiation. Int. J. Radiat. Biol. 76, 1599-1606 (2000).
40. C. L. Limoli, J. J. Corcoran, J. R. Milligan, J. F. Ward and W. F. Morgan, Critical target and dose and dose-rate responses for the induction of chromosomal instability by ionizing radiation. Radiat. Res. 151, 677-685 (1999).
41. J. B. Little, H. Nagasawa, T. Pfenning and H. Vetrovs, Radiation-induced genomic instability: Delayed mutagenic and cytogenetic effects of X rays and alpha particles. Radiat. Res. 148, 299-307 (1997).
42. R. L. Ullrich and C. M. Davis, Radiation-induced cytogenetic instability in vivo. Radiat. Res. 152, 170-173 (1999).
43. H. L. Liber and W. G. Thilly, Mutation assay at the thymidine kinase locus in diploid human lymphoblasts. Mutat. Res. 94, 467-485 (1982).
44. J. L. Schwartz, R. Jordan, B. A. Sedita, M. J. Swenningson, J. P. Banath and P. L. Olive, Different sensitivity to cell killing and chromosome mutation induction by gamma rays in two human lymphoblastoid cell lines derived from a single donor: Possible role of apoptosis. Mutagenesis 10, 227-233 (1995).
45. J. L. Schwartz and R. Jordan, Selective elimination of human lymphoid cells with unstable chromosome aberrations by p53-dependent apoptosis. Carcinogenesis 18, 201-205 (1997).
46. A. Grosovsky, H. Bethel, K. Parks, L. Ritter, C. Giver, S. Gauny, C. Wiese and A. Kronenberg, Genomic instability in human lymphoid cells exposed to 1 GeV/amu Fe ions. Phys. Med. 17, 238-240 (2001).
47. L. E. Smith and A. J. Grosovsky, Genetic instability on chromosome 16 in a human b lymphoblastoid cell line. Somat. Cell Mol. Genet. 19, 515-527 (1993).
48. C. Y. Li, D. W. Yandell and J. B. Little, Elevated frequency of microsatellite mutations in tk6 human lymphoblast clones selected for mutations at the thymidine kinase locus. Mol. Cell Biol. 14, 4373-4379 (1994).
49. J. D. Tucker, J. W. Breneman, J. F. Briner, G. G. Eveleth, R. G. Langlois and D. H. Moore, 2nd, Persistence of radiation-induced translocations in rat peripheral blood determined by chromosome painting. Environ. Mol. Mutagen. 30, 264-272 (1997).
50. S. A. Amundson, M. Bittner, P. Meltzer, J. Trent and A. J. Fornace, Jr., Induction of gene expression as a monitor of exposure to ionizing radiation. Radiat. Res. 156, 657-561 (2001).
51. D. E. MacCallum, P. A. Hall and E. G. Wright, The TRP53 pathway is induced in vivo by low doses of gamma radiation. Radiat. Res. 156, 324-347 (2001).
52. R. E. Rugo, M. B. Secretan and R. H. Schiestl, X radiation causes a persistent induction of reactive oxygen species and a delayed reinduction of TP53 in normal human diploid fibroblasts. Radiat. Res. 158, 210-219 (2002).
53. W. G. Nelson and M. B. Kastan, DNA strand breaks: The DNA template alterations that trigger p53-dependent DNA damage response pathways. Mol. Cell Biol. 14, 1815-1823 (1994).
54. A. A. Sablina, L. S. Agapova, P. M. Chumakov and B. P. Kopnin, P53 does not control the spindle assembly cell cycle checkpoint but mediates G1 arrest in response to disruption of microtubule system. Cell. Biol. Int. 23, 323-334 (1999).
55. S. M. Cross, C. A. Sanchez, C. A. Morgan, M. K. Schimke, S. Ramel, R. L. Idzerda, W. H. Raskind and B. J. Reid, A p53-dependent mouse spindle checkpoint. Science 267, 1353-1356 (1995).
56. P. L. Olive, J. P. Banath and R. E. Durand, Development of apoptosis and polyploidy in human lymphoblast cells as a function of position in the cell cycle at the time of irradiation. Radiat. Res. 146, 595-602 (1996).