Combined low initial DNA damage and high radiation-induced apoptosis confers clinical resistance to long-term toxicity in breast cancer patients treated with high-dose radiotherapy

Radiation Oncology

Volumn 6, Issue 1, 2011, Pages

  Henríquez Hernández, Luis A ^a,b,c   Carmona Vigo, Ruth ^a   Pinar, Beatriz ^a,b,c   Bordón, Elisa ^a,b,c   Lloret, Marta ^a,b,c   Núñez, María I ^d   Rodríguez Gallego, Carlos ^a,b   Lara, Pedro C ^a,b,c  

^a HOSPITAL UNIVERSITARIO DE GRAN CANARIA DR NEGRÍN   (Spain)

^b Madrid Spain   (Spain)

^c UNIVERSITY OF LAS PALMAS DE GRAN CANARIA   (Spain)

^d HOSPITAL UNIVERSITARIO SAN CECILIO   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOCORTIN 5; PROPIDIUM IODIDE; DNA;

ADULT; ADVANCED CANCER; AGED; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER PATIENT; CANCER RADIOTHERAPY; CANCER SURVIVOR; CLINICAL ARTICLE; CYTOTOXICITY; DOUBLE STRANDED DNA BREAK; FEMALE; FLOW CYTOMETRY; FOLLOW UP; HUMAN; PERIPHERAL LYMPHOCYTE; RADIATION DOSE FRACTIONATION; RADIATION HAZARD; RADIATION INJURY; RADIOSENSITIVITY; STATISTICAL ANALYSIS; BREAST TUMOR; DNA DAMAGE; LYMPHOCYTE; MIDDLE AGED; RADIATION DOSE; RADIATION EXPOSURE; RADIATION RESPONSE; RADIOTHERAPY; TREATMENT OUTCOME;

ADULT; AGED; AGED, 80 AND OVER; APOPTOSIS; BREAST NEOPLASMS; DNA; DNA DAMAGE; DOSE FRACTIONATION; DOSE-RESPONSE RELATIONSHIP, RADIATION; FEMALE; HUMANS; LYMPHOCYTES; MIDDLE AGED; RADIATION TOLERANCE; RADIOTHERAPY; TREATMENT OUTCOME;

EID: 79957908254     PISSN: None     EISSN: 1748717X     Source Type: Journal    
DOI: 10.1186/1748-717X-6-60     Document Type: Article

References (52)

1. Haagensen CD, Stout AP. Carcinoma of the Breast. II-Criteria of Operability. Ann Surg 1943, 118:1032-1051. 10.1097/00000658-194312000-00010, 1617775, 17858324.
2. Haagensen CD, Stout AP. Carcinoma of the Breast: Ii. Criteria of Operability. Ann Surg 1943, 118:859-870. 1617728, 17858315.
3. Toonkel LM, Fix I, Jacobson LH, Bamberg N, Wallach CB. Locally advanced breast carcinoma: results with combined regional therapy. Int J Radiat Oncol Biol Phys 1986, 12:1583-1587. 10.1016/0360-3016(86)90281-6, 3759583.
4. Therasse P, Mauriac L, Welnicka-Jaskiewicz M, Bruning P, Cufer T, Bonnefoi H, Tomiak E, Pritchard KI, Hamilton A, Piccart MJ. Final results of a randomized phase III trial comparing cyclophosphamide, epirubicin, and fluorouracil with a dose-intensified epirubicin and cyclophosphamide + filgrastim as neoadjuvant treatment in locally advanced breast cancer: an EORTC-NCIC-SAKK multicenter study. J Clin Oncol 2003, 21:843-850. 10.1200/JCO.2003.05.135, 12610183.
5. Shenkier T, Weir L, Levine M, Olivotto I, Whelan T, Reyno L. Clinical practice guidelines for the care and treatment of breast cancer: 15. Treatment for women with stage III or locally advanced breast cancer. CMAJ 2004, 170:983-994. 359433, 15023926.
6. Budach W, Hehr T, Budach V, Belka C, Dietz K. A meta-analysis of hyperfractionated and accelerated radiotherapy and combined chemotherapy and radiotherapy regimens in unresected locally advanced squamous cell carcinoma of the head and neck. BMC Cancer 2006, 6:28. 10.1186/1471-2407-6-28, 1379652, 16448551.
7. Baumann M, Bentzen SM, Ang KK. Hyperfractionated radiotherapy in head and neck cancer: a second look at the clinical data. Radiother Oncol 1998, 46:127-130. 10.1016/S0167-8140(97)00173-4, 9510039.
8. Burnet NG, Johansen J, Turesson I, Nyman J, Peacock JH. Describing patients' normal tissue reactions: concerning the possibility of individualising radiotherapy dose prescriptions based on potential predictive assays of normal tissue radiosensitivity. Steering Committee of the BioMed2 European Union Concerted Action Programme on the Development of Predictive Tests of Normal Tissue Response to Radiation Therapy. Int J Cancer 1998, 79:606-613. 10.1002/(SICI)1097-0215(19981218)79:6<606::AID-IJC9>3.0.CO;2-Y, 9842969.
9. Turesson I, Nyman J, Holmberg E, Oden A. Prognostic factors for acute and late skin reactions in radiotherapy patients. Int J Radiat Oncol Biol Phys 1996, 36:1065-1075. 10.1016/S0360-3016(96)00426-9, 8985028.
10. Meyn MS. Ataxia-telangiectasia and cellular responses to DNA damage. Cancer Res 1995, 55:5991-6001.
11. Ozsahin M, Ozsahin H, Shi Y, Larsson B, Wurgler FE, Crompton NE. Rapid assay of intrinsic radiosensitivity based on apoptosis in human CD4 and CD8 T-lymphocytes. Int J Radiat Oncol Biol Phys 1997, 38:429-440. 10.1016/S0360-3016(97)00038-2, 9226332.
12. Moody AM, Mayles WP, Bliss JM, A'Hern RP, Owen JR, Regan J, Broad B, Yarnold JR. The influence of breast size on late radiation effects and association with radiotherapy dose inhomogeneity. Radiother Oncol 1994, 33:106-112. 10.1016/0167-8140(94)90063-9, 7708953.
13. McMillan TJ, Tobi S, Mateos S, Lemon C. The use of DNA double-strand break quantification in radiotherapy. Int J Radiat Oncol Biol Phys 2001, 49:373-377. 10.1016/S0360-3016(00)01467-X, 11173130.
14. Crompton NE, Miralbell R, Rutz HP, Ersoy F, Sanal O, Wellmann D, Bieri S, Coucke PA, Emery GC, Shi YQ, et al. Altered apoptotic profiles in irradiated patients with increased toxicity. Int J Radiat Oncol Biol Phys 1999, 45:707-714. 10.1016/S0360-3016(99)00256-4, 10524426.
15. Henriquez Hernandez LA, Lara PC, Pinar B, Bordon E, Rodriguez Gallego C, Bilbao C, Fernandez Perez L, Flores Morales A. Constitutive gene expression profile segregates toxicity in locally advanced breast cancer patients treated with high-dose hyperfractionated radical radiotherapy. Radiat Oncol 2009, 4:17. 10.1186/1748-717X-4-17, 2698866, 19497124.
16. Rodningen OK, Borresen-Dale AL, Alsner J, Hastie T, Overgaard J. Radiation-induced gene expression in human subcutaneous fibroblasts is predictive of radiation-induced fibrosis. Radiother Oncol 2008, 86:314-320. 10.1016/j.radonc.2007.09.013, 17963910.
17. Pinar B, Lara PC, Lloret M, Bordon E, Nunez MI, Villalobos M, Guerrero R, Luna JD, Ruiz de Almodovar JM. Radiation-induced DNA damage as a predictor of long-term toxicity in locally advanced breast cancer patients treated with high-dose hyperfractionated radical radiotherapy. Radiat Res 2007, 168:415-422. 10.1667/RR0746.1, 17903032.
18. Ruiz de Almodovar JM, Guirado D, Isabel Nunez M, Lopez E, Guerrero R, Valenzuela MT, Villalobos M, del Moral R. Individualization of radiotherapy in breast cancer patients: possible usefulness of a DNA damage assay to measure normal cell radiosensitivity. Radiother Oncol 2002, 62:327-333. 10.1016/S0167-8140(01)00490-X, 12175564.
19. Barber JB, West CM, Kiltie AE, Roberts SA, Scott D. Detection of individual differences in radiation-induced apoptosis of peripheral blood lymphocytes in normal individuals, ataxia telangiectasia homozygotes and heterozygotes, and breast cancer patients after radiotherapy. Radiat Res 2000, 153:570-578. 10.1667/0033-7587(2000)153[0570:DOIDIR]2.0.CO;2, 10790278.
20. Ozsahin M, Crompton NE, Gourgou S, Kramar A, Li L, Shi Y, Sozzi WJ, Zouhair A, Mirimanoff RO, Azria D. CD4 and CD8 T-lymphocyte apoptosis can predict radiation-induced late toxicity: a prospective study in 399 patients. Clin Cancer Res 2005, 11:7426-7433. 10.1158/1078-0432.CCR-04-2634, 16243816.
21. Bordon E, Henriquez Hernandez LA, Lara PC, Pinar B, Fontes F, Rodriguez Gallego C, Lloret M. Prediction of clinical toxicity in localized cervical carcinoma by radio-induced apoptosis study in peripheral blood lymphocytes (PBLs). Radiat Oncol 2009, 4:58. 10.1186/1748-717X-4-58, 2787528, 19941649.
22. Bordon E, Henriquez-Hernandez LA, Lara PC, Ruiz A, Pinar B, Rodriguez-Gallego C, Lloret M. Prediction of clinical toxicity in locally advanced head and neck cancer patients by radio-induced apoptosis in peripheral blood lymphocytes (PBLs). Radiat Oncol 2010, 5:4. 10.1186/1748-717X-5-4, 2827476, 20109191.
23. Pinar B, Henriquez-Hernandez LA, Lara PC, Bordon E, Rodriguez-Gallego C, Lloret M, Nunez MI, De Almodovar MR. Radiation induced apoptosis and initial DNA damage are inversely related in locally advanced breast cancer patients. Radiat Oncol 2010, 5:85. 10.1186/1748-717X-5-85, 2956713, 20868468.
24. Nunez MI, Guerrero MR, Lopez E, del Moral MR, Valenzuela MT, Siles E, Villalobos M, Pedraza V, Peacock JH, Ruiz de Almodovar JM. DNA damage and prediction of radiation response in lymphocytes and epidermal skin human cells. Int J Cancer 1998, 76:354-361. 10.1002/(SICI)1097-0215(19980504)76:3<354::AID-IJC12>3.0.CO;2-B, 9579572.
25. Bordon E, Henriquez-Hernandez LA, Lara PC, Pinar B, Rodriguez-Gallego C, Lloret M. Role of CD4 and CD8 T-lymphocytes, B-lymphocytes and Natural Killer cells in the prediction of radiation-induced late toxicity in cervical cancer patients. Int J Radiat Biol 2011, 87:424-431. 10.3109/09553002.2010.537433, 21142701.
26. Johansson S, Svensson H, Denekamp J. Dose response and latency for radiation-induced fibrosis, edema, and neuropathy in breast cancer patients. Int J Radiat Oncol Biol Phys 2002, 52:1207-1219. 10.1016/S0360-3016(01)02743-2, 11955731.
27. Coles CE, Moody AM, Wilson CB, Burnet NG. Reduction of radiotherapy-induced late complications in early breast cancer: the role of intensity-modulated radiation therapy and partial breast irradiation. Part II--Radiotherapy strategies to reduce radiation-induced late effects. Clin Oncol (R Coll Radiol) 2005, 17:98-110.
28. Dickson J, Magee B, Stewart A, West CM. Relationship between residual radiation-induced DNA double-strand breaks in cultured fibroblasts and late radiation reactions: a comparison of training and validation cohorts of breast cancer patients. Radiother Oncol 2002, 62:321-326. 10.1016/S0167-8140(01)00432-7, 12175563.
29. Hoeller U, Borgmann K, Bonacker M, Kuhlmey A, Bajrovic A, Jung H, Alberti W, Dikomey E. Individual radiosensitivity measured with lymphocytes may be used to predict the risk of fibrosis after radiotherapy for breast cancer. Radiother Oncol 2003, 69:137-144. 10.1016/j.radonc.2003.10.001, 14643950.
30. Zhou PK, Sproston AR, Marples B, West CM, Margison GP, Hendry JH. The radiosensitivity of human fibroblast cell lines correlates with residual levels of DNA double-strand breaks. Radiother Oncol 1998, 47:271-276. 10.1016/S0167-8140(97)00200-4, 9681890.
31. Geara FB, Peters LJ, Ang KK, Wike JL, Sivon SS, Guttenberger R, Callender DL, Malaise EP, Brock WA. Intrinsic radiosensitivity of normal human fibroblasts and lymphocytes after high-and low-dose-rate irradiation. Cancer Res 1992, 52:6348-6352.
32. O'Driscoll MC, Scott D, Orton CJ, Kiltie AE, Davidson SE, Hunter RD, West CM. Radiation-induced micronuclei in human fibroblasts in relation to clonogenic radiosensitivity. Br J Cancer 1998, 78:1559-1563. 10.1038/bjc.1998.723, 2063244, 9862564.
33. Belyaev IY. Radiation-induced DNA repair foci: spatio-temporal aspects of formation, application for assessment of radiosensitivity and biological dosimetry. Mutat Res 2010, 704:132-141. 10.1016/j.mrrev.2010.01.011, 20096808.
34. Belyaev IY, Eriksson S, Nygren J, Torudd J, Harms-Ringdahl M. Effects of ethidium bromide on DNA loop organisation in human lymphocytes measured by anomalous viscosity time dependence and single cell gel electrophoresis. Biochim Biophys Acta 1999, 1428:348-356.
35. Torudd J, Protopopova M, Sarimov R, Nygren J, Eriksson S, Markova E, Chovanec M, Selivanova G, Belyaev IY. Dose-response for radiation-induced apoptosis, residual 53BP1 foci and DNA-loop relaxation in human lymphocytes. Int J Radiat Biol 2005, 81:125-138. 10.1080/09553000500077211, 16019922.
36. Kiltie AE, Orton CJ, Ryan AJ, Roberts SA, Marples B, Davidson SE, Hunter RD, Margison GP, West CM, Hendry JH. A correlation between residual DNA double-strand breaks and clonogenic measurements of radiosensitivity in fibroblasts from preradiotherapy cervix cancer patients. Int J Radiat Oncol Biol Phys 1997, 39:1137-1144. 10.1016/S0360-3016(97)00545-2, 9392556.
37. Lopez E, Guerrero R, Nunez MI, del Moral R, Villalobos M, Martinez-Galan J, Valenzuela MT, Munoz-Gamez JA, Oliver FJ, Martin-Oliva D, Ruiz de Almodovar JM. Early and late skin reactions to radiotherapy for breast cancer and their correlation with radiation-induced DNA damage in lymphocytes. Breast Cancer Res 2005, 7:R690-698. 10.1186/bcr1277, 1242135, 16168114.
38. Bourton EC, Plowman PN, Smith D, Arlett CF, Parris CN. Prolonged expression of the gamma-H2AX DNA repair biomarker correlates with excess acute and chronic toxicity from radiotherapy treatment. Int J Cancer 2011,
39. Saavedra MM, Henriquez-Hernandez LA, Lara PC, Pinar B, Rodriguez-Gallego C, Lloret M. Amifostine modulates radio-induced apoptosis of peripheral blood lymphocytes in head and neck cancer patients. J Radiat Res (Tokyo) 2010, 51:603-607.
40. Dikomey E, Brammer I, Johansen J, Bentzen SM, Overgaard J. Relationship between DNA double-strand breaks, cell killing, and fibrosis studied in confluent skin fibroblasts derived from breast cancer patients. Int J Radiat Oncol Biol Phys 2000, 46:481-490. 10.1016/S0360-3016(99)00335-1, 10661357.
41. Greve B, Dreffke K, Rickinger A, Konemann S, Fritz E, Eckardt-Schupp F, Amler S, Sauerland C, Braselmann H, Sauter W, et al. Multicentric investigation of ionising radiation-induced cell death as a predictive parameter of individual radiosensitivity. Apoptosis 2009, 14:226-235. 10.1007/s10495-008-0294-6, 19142732.
42. Wistop A, Keller U, Sprung CN, Grabenbauer GG, Sauer R, Distel LV. Individual radiosensitivity does not correlate with radiation-induced apoptosis in lymphoblastoid cell lines or CD3+ lymphocytes. Strahlenther Onkol 2005, 181:326-335. 10.1007/s00066-005-1372-0, 15900430.
43. McKay BC, Ljungman M, Rainbow AJ. Persistent DNA damage induced by ultraviolet light inhibits p21waf1 and bax expression: implications for DNA repair, UV sensitivity and the induction of apoptosis. Oncogene 1998, 17:545-555. 10.1038/sj.onc.1201963, 9704920.
44. Dumaz N, Duthu A, Ehrhart JC, Drougard C, Appella E, Anderson CW, May P, Sarasin A, Daya-Grosjean L. Prolonged p53 protein accumulation in trichothiodystrophy fibroblasts dependent on unrepaired pyrimidine dimers on the transcribed strands of cellular genes. Mol Carcinog 1997, 20:340-347. 10.1002/(SICI)1098-2744(199712)20:4<340::AID-MC3>3.0.CO;2-N, 9433478.
45. Story MD, Voehringer DW, Malone CG, Hobbs ML, Meyn RE. Radiation-induced apoptosis in sensitive and resistant cells isolated from a mouse lymphoma. Int J Radiat Biol 1994, 66:659-668.
46. Sionov RV, Haupt Y. The cellular response to p53: the decision between life and death. Oncogene 1999, 18:6145-6157. 10.1038/sj.onc.1203130, 10557106.
47. Duchaud E, Ridet A, Delic Y, Cundari E, Moustacchi E, Rosselli F. Changes in the radiation-induced apoptotic response in homozygotes and heterozygotes for the ataxia-telangiectasia gene. C R Acad Sci III 1994, 317:983-989.
48. Mori M, Benotmane MA, Tirone I, Hooghe-Peters EL, Desaintes C. Transcriptional response to ionizing radiation in lymphocyte subsets. Cell Mol Life Sci 2005, 62:1489-1501. 10.1007/s00018-005-5086-3, 15971001.
49. Rosselli F, Ridet A, Soussi T, Duchaud E, Alapetite C, Moustacchi E. p53-dependent pathway of radio-induced apoptosis is altered in Fanconi anemia. Oncogene 1995, 10:9-17.
50. Cann KL, Hicks GG. Regulation of the cellular DNA double-strand break response. Biochem Cell Biol 2007, 85:663-674. 10.1139/O07-135, 18059525.
51. Crompton NE, Shi YQ, Emery GC, Wisser L, Blattmann H, Maier A, Li L, Schindler D, Ozsahin H, Ozsahin M. Sources of variation in patient response to radiation treatment. Int J Radiat Oncol Biol Phys 2001, 49:547-554. 10.1016/S0360-3016(00)01477-2, 11173153.
52. Svensson JP, Stalpers LJ, Esveldt-van Lange RE, Franken NA, Haveman J, Klein B, Turesson I, Vrieling H, Giphart-Gassler M. Analysis of gene expression using gene sets discriminates cancer patients with and without late radiation toxicity. PLoS Med 2006, 3:e422. 10.1371/journal.pmed.0030422, 1626552, 17076557.