Response to low-dose X-irradiation is p53-dependent in a papillary thyroid carcinoma model system

International Journal of Oncology

Volumn 39, Issue 6, 2011, Pages 1429-1441

  Abou El Ardat, Khalil ^a,b   Derradji, Hanane ^a   De Vos, Winnok ^b   De Meyer, Tim ^b   Bekaert, Sofie ^b   Van Criekinge, Wim ^b   Baatout, Sarah ^a  

^a BELGIAN NUCLEAR RESEARCH CENTRE   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

Apoptosis; p53; p73; Papillary thyroid carcinoma; Radiation; RET PTC1

Indexed keywords

PROTEIN P53;

ARTICLE; CANCER RADIOTHERAPY; CELL AGING; CELL CYCLE S PHASE; CELL MUTANT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; HUMAN; HUMAN CELL; LOW ENERGY RADIATION; PRIORITY JOURNAL; RADIATION DOSE DISTRIBUTION; RADIATION RESPONSE; THYROID PAPILLARY CARCINOMA; X IRRADIATION;

BETA-GALACTOSIDASE; BIOLOGICAL MARKERS; CASPASE 3; CELL CYCLE; CELL DEATH; CELLS, CULTURED; CYTOKINES; DNA BREAKS, DOUBLE-STRANDED; HUMANS; PROTEIN BIOSYNTHESIS; RADIOTHERAPY DOSAGE; THYROID NEOPLASMS; TRANSFORMING GROWTH FACTOR BETA1; TUMOR SUPPRESSOR PROTEIN P53;

EID: 80054820608     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo.2011.1175     Document Type: Article

References (49)

1. Little JB: Cellular, molecular, and carcinogenic effects of radiation. Hematol Oncol Clin North Am 7: 337-352, 1993.
2. Hooker AM, Bhat M, Day TK, Lane JM, Swinburne SJ, Morley AA and Sykes PJ: The linear no-threshold model does not hold for low-dose ionizing radiation. Radiat Res 162: 447-452, 2004. (Pubitemid 39388167)
3. Averbeck D: Does scientific evidence support a change from the LNT model for low-dose radiation risk extrapolation? Health Phys 97: 493-504, 2009.
4. Rothkamm K and Löbrich M: 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. (Pubitemid 36542657)
5. Jin YW, Na YJ, Lee YJ, An S, Lee J, Jung M, Kim H, Nam S, Kim C, Yang K, Kim S, Kim W, Park WY, Yoo KY, Kim C and Kim J: Comprehensive analysis of time- and dose-dependent patterns of gene expression in a human mesenchymal stem cell line exposed to low-dose ionizing radiation. Oncol Rep 19: 135-144, 2008. (Pubitemid 351176141)
6. Bonner WM: Low-dose radiation: thresholds, bystander effects, and adaptive responses. Proc Natl Acad Sci USA 100: 4973-4975, 2003.
7. Cardis E, Howe G, Bebeshko V, Bogdanova T, Bouville A, Carr Z, Chumak V, Davis S, Demidchik Y, Zvonova I, et al.: Cancer consequences of the chernobyl accident: 20 years on. J Radiol Prot 26: 127-140, 2006. (Pubitemid 43861071)
8. Hatch M, Ron E, Bouville A, Zablotska L and Howe G: The chernobyl disaster: cancer following the accident at the chernobyl nuclear power plant. Epidemiol Rev 27: 56-66, 2005. (Pubitemid 40885066)
9. Christov K: Thyroid cell proliferation in rats and induction of tumors by X-rays. Cancer Res 35: 1256-1262, 1975.
10. Melillo RM, Castellone MD, Guarino V, De Falco V, Cirafici AM, Salvatore G, Caiazzo F, Basolo F, Giannini R, Kruhoffer M, Orntoft T, Fusco A and Santoro M: The RET/PTC-RAS-BRAF linear signaling cascade mediates the motile and mitogenic pheno- type of thyroid cancer cells. J Clin Invest 115: 1068-1081, 2005. (Pubitemid 40489412)
11. Meireles AM, Preto A, Rocha AS, Rebocho AP, Màximo V, Pereira-Castro I, Moreira S, Feijão T, Botelho T, Marques R, Trovisco V, Cirnes L, Alves C, Velho S, Soares P and Sobrinho-Simões M: Molecular and genotypic characterization of human thyroid follicular cell carcinoma-derived cell lines. Thyroid 17: 707-715, 2007.
12. De Vos WH, Van Neste L, Dieriks B, Joss GH and Van Oostveldt P: High content image cytometry in the context of subnuclear organization. Cytometry A 77: 64-75, 2010.
13. Gary RK and Kindell SM: Quantitative assay of senescence-associated â-galactosidase activity in mammalian cell extracts. Anal Biochem 343: 329-334, 2005. (Pubitemid 41074047)
14. Dieriks B, De Vos WH, Derradji H, Baatout S and Van Oostveldt P: Medium-mediated DNA repair response after ionizing radiation is correlated with the increase of specific cytokines in human fibroblasts. Mutat Res 687: 40-48, 2010.
15. Bache M, Pigorsch S, Dunst J, Würl P, Meye A, Bartel F, Schmidt H, Rath FW and Taubert H: Loss of G2/M arrest correlates with radiosensitization in two human sarcoma cell lines with mutant p53. Int J Cancer 96: 110-117, 2001. (Pubitemid 32291431)
16. Cichowski K and Hahn WC: Unexpected pieces to the senescence puzzle. Cell 133: 958-961, 2008. (Pubitemid 351787750)
17. Rodier F, Coppé JP, Patil CK, Hoejimakers WAM, Muñoz DP, Raza SR, Freund A, Campeau E, Davalos AR and Campisi J: Persistent DNA damage signalling triggers senescence-associated inflammatory cytokine secretion. Nat Cell Biol 11: 973-981, 2009.
18. Sengupta S and Harris CC: p53: Traffic cop at the crossroads of DNA repair and recombination. Nat Rev Mol Cell Biol 6: 44-55, 2005. (Pubitemid 40064898)
19. Severino J, Allen RG, Balin S, Balin A and Cristofalo VJ: Is beta-galactosidase staining a marker of senescence in vitro and in vivo? Exp Cell Res 257: 162-171, 2000. (Pubitemid 30324654)
20. Boice JD Jr: Radiation-induced thyroid cancer - What's new? J Natl Cancer Inst 97: 703-705, 2005.
21. Tucker MA, Jones PH, Boice JD, Jr., Robison LL, Stone BJ, Stovall M, Jenkin RD, Lubin JH, Baum ES, Siegel SE, Meadows AT, Hoover RN and Fraumeni JF Jr: Therapeutic radiation at a young age is linked to secondary thyroid cancer. Cancer Res 51: 2885-2888, 1991.
22. Schneider AB, Ron E, Lubin J, Stovall M and Gierlowski TC: Dose-response relationships for radiation-induced thyroid cancer and thyroid nodules: evidence for the prolonged effects of radiation on the thyroid. J Clin Endocrinol Metab 77: 362-369, 1993. (Pubitemid 23230041)
23. Cardis E, Vrijheid M, Blettner M, Gilbert E, Hakama M, Hill C, Howe G, Kaldor J, Muirhead CR, Schubauer-Berigan M, Yoshimura T, et al.: Risk of cancer after low doses of ionising radiation: retrospective cohort study in 15 countries. BMJ 331: 77, 2005.
24. Kesminiene A, Evrard AS, Ivanov VK, Malakhova IV, Kurtinaitis J, Stengrevics A, Tekkel M, Anspaugh LR, Bouville A, Chekin S, Chumak VV, Drozdovitch V, Gapanovich V, Golovanov I, Hubert P, Illichev SV, Khait SE, Kryuchkov VP, Maceika E, Maksyoutov M, Mirkhaidarov AK, Polyakov S, Shchukina N, Tenet V, Tserakhovich TI, Tsykalo A, Tukov AR and Cardis E: Risk of hematological malignancies among Chernobyl liquidators. Radiat Res 170: 721-735, 2008.
25. Luster M, Lassmann M, Freudenberg LS and Reiners C: Thyroid cancer in childhood: management strategy, including dosimetry and long-term results. Hormones (Athens) 6: 269-278, 2007.
26. Haas RL: Low dose radiotherapy in indolent lymphomas, enough is enough. Hematol Oncol 27: 71-81, 2009.
27. Cuttler JM and Pollycove M: Can cancer be treated with low doses of radiation? J Am Phys Surg 8: 108-111, 2003.
28. Mallick U, Harmer C and Hackshaw A: The HiLo trial: a multi- centre randomised trial of high- versus low-dose radioiodine, with or without recombinant human thyroid stimulating hormone, for remnant ablation after surgery for differentiated thyroid cancer. Clin Oncol 20: 325-326, 2008. (Pubitemid 351636017)
29. Frasca F, Vella V, Aloisi A, Mandarino A, Mazzon E, Vigneri R and Vigneri P: p73 tumor-suppressor activity is impaired in human thyroid cancer. Cancer Res 63: 5829-5837, 2003. (Pubitemid 37187481)
30. Garner E and Raj K: Protective mechanisms of p53-p21-pRb proteins against DNA damage-induced cell death. Cell Cycle 7: 277-282, 2008. (Pubitemid 351366487)
31. Namba H, Hara T, Tukazaki T, Migita K, Ishikawa N, Ito K, Nagataki S and Yamashita S: Radiation-induced G1 arrest is selectively mediated by the p53-WAF1/Cip1 pathway in human thyroid cells. Cancer Res 55: 2075-2080, 1995.
32. Rosenbluth JM and Pietenpol JA: The jury is in: p73 is a tumor suppressor after all. Genes Dev 22: 2591-2595, 2008.
33. Levrero M, De Laurenzi V, Costanzo A, Sabatini S, Gong J, Wang JY and Melino G: The p53/p63/p73 family of transcription factors: overlapping and distinct functions. J Cell Sci 113: 1661-1670, 2000.
34. Soussi T and Hjortsberg L: When mutant p53 plays hide and seek: a new challenge for diagnosis and therapy? Trends Mol Med 15: 1-4, 2009.
35. Leong WF, Chau JF and Li B: p53 Deficiency leads to compen- satory up-regulation of p16INK4a. Mol Cancer Res 7: 354-360, 2009
36. Yamakoshi K, Takahashi A, Hirota F, Nakayama R, Ishimaru N, Kubo Y, Mann DJ, Ohmura M, Hirao A, Saya H, Arase S, Hayashi Y, Nakao K, Matsumoto M, Ohtani N and Hara E: Real-time in vivo imaging of p16Ink4a reveals cross talk with p53. J Cell Biol 186: 393-407, 2009.
37. Stein GH, Drullinger LF, Soulard A and Duliæ V: 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, 1999. (Pubitemid 29098269)
38. Abd Elmageed ZY, Gaur RL, Williams M, Abdraboh ME, Rao PN, Raj MH, Ismail FM and Ouhtit A: Characterization of coordinated immediate responses by p16INK4A and p53 pathways in UVB-irradiated human skin cells. J Invest Dermatol 129: 175-183, 2009.
39. Short SC, Bourne S, Martindale C, Woodcock M and Jackson SP: DNA damage responses at low radiation doses. Radiat Res 164: 292-302, 2005. (Pubitemid 41233783)
40. McCubrey JA, Steelman LS, Abrams SL, Lee JT, Chang F, Bertrand FE, Navolanic M, Terrian DM, Franklin RA, Libra M, et al.: Roles of the RAF/MEK/ERK and PI3K/PTEN/AKT pathways in malignant transformation and drug resistance. Adv Enzyme Regul 46: 249-279, 2006. (Pubitemid 44301348)
41. Antonsson B and Martinou JC: The Bcl-2 protein family. Exp Cell Res 256: 50-57, 2000. (Pubitemid 30211166)
42. Wang Y, Hou P, Yu H, Wang W, Ji M, Zhao S, Yan S, Sun X, Liu D, Xing M, et al.: High prevalence and mutual exclusivity of genetic alterations in the phosphatidylinositol-3-kinase/akt pathway in thyroid tumors. J Clin Endocrinol Metab 92: 2387-2390, 2007. (Pubitemid 46997152)
43. Krueger SA, Joiner MC, Weinfeld M, Piasentin E and Marples B: Role of apoptosis in low-dose hyper-radiosensitivity. Radiat Res 167: 260-267, 2007. (Pubitemid 351292537)
44. Enns L, Bogen KT, Wizniak J, Murtha AD and Weinfeld M: Low-dose radiation hypersensitivity is associated with p53- dependent apoptosis. Mol Cancer Res 2: 557-566, 2004. (Pubitemid 39403384)
45. Tsai KK, Stuart J, Chuang YY, Little JB and Yuan ZM: Low-dose radiation-induced senescent stromal fibroblasts render nearby breast cancer cells radioresistant. Radiat Res 172: 306-313, 2009.
46. Acosta JC, O'Loghlen A, Banito A, Guijarro MV, Augert A, Raguz S, Fumagalli M, Da Costa M, Brown C, Popov N, Takatsu Y, Melamed J, d'Adda di Fagagna F, Bernard D, Hernando E and Gil J: Chemokine signaling via the CXCR2 receptor reinforces senescence. Cell 133: 1006-1018, 2008. (Pubitemid 351795610)
47. Orjalo AV, Bhaumik D, Gengler BK, Scott GK and Campisi J: Cell surface-bound IL-1alpha is an upstream regulator of the senescence-associated IL-6/IL-8 cytokine network. Proc Natl Acad Sci USA 106: 17031-17036, 2009.
48. Matsuo SE, Leoni SG, Colquhoun A and Kimura ET: Transforming growth factor-beta1 and activin A generate antiproliferative signaling in thyroid cancer cells. J Endocrinol 190: 141-150, 2006. (Pubitemid 44161069)
49. Coppé JP, Patil CK, Rodier F, Sun Y, Muñoz DP, Goldstein J, Nelson PS, Desprez PY and Campisi J: Senescence-associated secretory phenotypes reveal cell-nonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol 6: 2853-2868, 2008.