DNA double-strand breaks induced by mammographic screening procedures in human mammary epithelial cells

International Journal of Radiation Biology

Volumn 87, Issue 11, 2011, Pages 1103-1112

  Colin, Catherine ^a,b   Devic, Clément ^c   Nol, Alain ^d   Rabilloud, Muriel ^e,f   Zabot, Marie Thérse ^e   Pinet Isaac, Sylvie ^a   Giraud, Sophie ^g   Riche, Benjamin ^e,f   Valette, Pierre Jean ^a   Rodriguez Lafrasse, Claire ^a,b   Foray, Nicolas ^c  

^a CENTRE HOSPITALIER LYON SUD   (France)

^b UNIVERSITÉ LYON 1   (France)

^c GRENOBLE INSTITUT DES NEUROSCIENCES   (France)

^d CNRS   (France)

^e HOSPICES CIVILS DE LYON   (France)

^f LABORATOIRE DE BIOMÉTRIE ET BIOLOGIE EVOLUTIVE   (France)

^g EDOUARD HERRIOT HOSPITAL   (France)

Author keywords

DNA damage; DNA double strand break; Ionising radiation; Low dose radiation effect; Mammography

Indexed keywords

DOUBLE STRANDED DNA; HISTONE H2AX;

ADULT; AGED; ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER PATIENT; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE EXACERBATION; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; FEMALE; HIGH RISK PATIENT; HISTONE PHOSPHORYLATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; MAMMOGRAPHY; MICRONUCLEUS; PRIORITY JOURNAL; RADIATION DOSE;

ADULT; AGE FACTORS; AGED; BREAST; DNA BREAKS, DOUBLE-STRANDED; EPITHELIAL CELLS; FEMALE; HISTONES; HUMANS; MAMMOGRAPHY; MICRONUCLEI, CHROMOSOME-DEFECTIVE; MIDDLE AGED;

EID: 80053906135     PISSN: 09553002     EISSN: 13623095     Source Type: Journal    
DOI: 10.3109/09553002.2011.608410     Document Type: Article

References (58)

1. Andrieu N, Easton DF, Chang-Claude J, Rookus MA, Brohet R, Cardis E, Antoniou AC, Wagner T, Simard J, Evans G, et al. 2006. Effect of chest X-rays on the risk of breast cancer among BRCA1/2 mutation carriers in the international BRCA1/2 carrier cohort study: A report from the EMBRACE, GENEPSO, GEO-HEBON, and IBCCS Collaborators 'Group. Journal of Clinical Oncology 24:3361-3366.
2. Averbeck D. 2010. Non-targeted effects as a paradigm breaking evidence. Mutation Research 687:7-12.
3. Berrington de Gonzalez A, Reeves G. 2005. Mammographic screening before age 50 years in the UK: Comparison of the radiation risks with the mortality benefits. British Journal of Cancer 93:590-596.
4. Berrington de Gonzalez A, Berg CD, Visvanathan K, Robson M. 2009. Estimated risk of radiation-induced breast cancer from mammographic screening for young BRCA mutation carriers. Journal of National Cancer Institute 101:205-209.
5. Beyreuther E, Lessmann E, Pawelke J, Pieck S. 2009a. DNA doublestrand break signalling: X-ray energy dependence of residual co-localised foci of gamma-H2AX and 53BP1. International Journal of Radiation Biology 85:1042-1050.
6. Beyreuther E, Dorr W, Lehnert A, Lessmann E, Pawelke J. 2009b. Relative biological effectiveness of 25 and 10 kV X-rays for the induction of chromosomal aberrations in two human mammary epithelial cell lines. Radiation Environmental Biophysics 48:333-340.
7. Cardis E, Hall J, Tavtigian SV. 2007. Identification of women with an increased risk of developing radiation-induced breast cancer. Breast Cancer Research 9:106.
8. Colin C, Granzotto A, Devic C, Viau M, Maalouf M, Vogin G, Joubert A, Thomas C, Foray N. 2011. MRE11 and H2AX biomarkers in the response to low-dose exposure: Balance between individual susceptibility to radiosensitivity and to genomic instability. International Journal of Low Radiation, in press.
9. Colin C, Prince V. 2007. Radiological screening modalities in patients with an identified family risk of breast cancer. Imagerie de la Femme 17:161-168.
10. Feig SA, Hendrick RE. 1997. Radiation risk from screening mammography of women aged 40-49 years. Journal of National Cancer Institute Monographs 119-124.
11. Fenech M, Morley AA. 1985. Measurement of micronuclei in lymphocytes. Mutation Research 147:29-36.
12. Foray N, Charvet AM, Duchemin D, Favaudon V, Lavalette D. 2005. The repair rate of radiation-induced DNA damage: A stochastic interpretation based on the gamma function. Journal of Theoretical Biology 236:448-458.
13. Foray N, Randrianarison V, Marot D, Perricaudet M, Lenoir G, Feunteun J. 1999. Gamma-rays-induced death of human cells carrying mutations of BRCA1 or BRCA2. Oncogene 18:7334-7342.
14. Foray N, Priestley A, Alsbeih G, Badie C, Capulas EP, Arlett CF, Malaise EP. 1997. Hypersensitivity of ataxia telangiectasia fibroblasts to ionizing radiation is associated with a repair deficiency of DNA double-strand breaks. International Journal of Radiation Biology 72:271-283.
15. Foray N, Marot D, Gabriel A, Randrianarison V, Carr AM, Perricaudet M, Ashworth A, Jeggo P. 2003. A subset of ATM-and ATR-dependent phosphorylation events requires the BRCA1 protein. EMBO Journal 22:2860-2871.
16. Geisel D, Heverhagen JT, Kalinowski M, Wagner HJ. 2008. DNA doublestrand breaks after percutaneous transluminal angioplasty. Radiology 248:852-859.
17. Granzotto A, Devic, C, Viau, M, et al. 2011a. Individual susceptibility to radiosensitivity and to genomic instability; its impact on low doses phenomena. Health Physics 100:282
18. Granzotto A, Joubert A, Viau M, Clément D, Maalouf M, Thomas C, Vogin G, Malek K, Colin C, Balosse J, Foray N. 2011b. Individual response to ionising radiation: What predictive assay(s) to choose? Compte-rendus de l'Académie des Sciences, Biologies 334:140-157.
19. Grudzenski S, Kuefner MA, Heckmann MB, Uder M, Lobrich M. 2009. Contrast medium-enhanced radiation damage caused by CT examinations. Radiology 253:706-714.
20. Grudzenski S, Raths A, Conrad S, Rube CE, Lobrich M. 2010. Inducible response required for repair of low-dose radiation damage in human fibroblasts. Proceedings of the National Academy of Sciences of the USA 107:14205-14210.
21. Harrigan JA, Belotserkovskaya R, Coates J, Dimitrova DS, Polo SE, Bradshaw CR, Fraser P, Jackson SP. 2011. Replication stress induces 53BP1-containing OPT domains in G1 cells. Journal of Cell Biology 193:97-108.
22. Hendrick RE, Pisano ED, Averbukh A, Moran C, Berns EA, Yaffe MJ, Herman B, Acharyya S, Gatsonis C. 2010. Comparison of acquisition parameters and breast dose in digital mammography and screenfilm mammography in the american college of radiology imaging network digital mammographic imaging screening trial. American Journal of Roentgenology 194:362-369.
23. Heyes GJ, Mill AJ. 2004. The neoplastic transformation potential of mammography X-rays and atomic bomb spectrum radiation. Radiation Research 162:120-127.
24. Heyes GJ, Mill AJ, Charles MW. 2009. Mammography-oncogenecity at low doses. Journal of Radiology Protocols 29:A123-132.
25. Iliakis G. 1991. The role of DNA double strand breaks in ionizing radiation-induced killing of eukaryotic cells. Bioessays 13:641-648.
26. Jansen-van der Weide MC, Greuter MJ, Jansen L, Oosterwijk JC, Pijnappel RM, de Bock GH. 2010. Exposure to low-dose radiation and the risk of breast cancer among women with a familial or genetic predisposition: A meta-analysis. European Radiology 20:2547-2556.
27. Jeggo PA, Lobrich M. 2006. Contribution of DNA repair and cell cycle checkpoint arrest to the maintenance of genomic stability. DNA Repair (Amst) 5:1192-1198.
28. Joubert A, Zimmerman KM, Bencokova Z, Gastaldo J, Chavaudra N, Favaudon V, Arlett CF, Foray N. 2008. DNA double-strand break repair defects in syndromes associated with acute radiation response: At least two different assays to predict intrinsic radiosensitivity? International Journal of Radiation Biology 84:107-125.
29. Ko SJ, Liao XY, Molloi S, Elmore E, Redpath JL. 2004. Neoplastic transformation in vitro after exposure to low doses of mammographicenergy X-rays: Quantitative and mechanistic aspects. Radiation Research 162:646-654.
30. Kriege M, Brekelmans CT, Boetes C, Besnard PE, Zonderland HM, Obdeijn IM, Manoliu RA, Kok T, Peterse H, Tilanus-Linthorst MM, et al. 2004. Efficacy of MRI and mammography for breast-cancer screening in women with a familial or genetic predisposition. New England Journal of Medicine 351:427-437.
31. Kuhl CK, Schrading S, Leutner CC, Morakkabati-Spitz N, Wardelmann E, Fimmers R, Kuhn W, Schild HH. 2005. Mammography, breast ultrasound, and magnetic resonance imaging for surveillance of women at high familial risk for breast cancer. Journal of Clinical Oncology 23:8469-8476.
32. Law J. 1997. Cancers detected and induced in mammographic screening: New screening schedules and younger women with family history. British Journal of Radiology 70:62-69.
33. Leach MO, Boggis CR, Dixon AK, Easton DF, Eeles RA, Evans DG, Gilbert FJ, Griebsch I, HoffRJ, Kessar P, et al. 2005. Screening with magnetic resonance imaging and mammography of a UK population at high familial risk of breast cancer: A prospective multicentre cohort study (MARIBS). The Lancet 365:1769-1778.
34. Lee C, Kim JS, Waldman T. 2004. PTEN gene targeting reveals a radiation-induced size checkpoint in human cancer cells. Cancer Research 64:6906-6914.
35. Lehnert A, Lessmann E, Pawelke J, Dorr W. 2006. RBE of 25 kV X-rays for the survival and induction of micronuclei in the human mammary epithelial cell line MCF-12A. Radiation Environmental Biophysics 45:253-260.
36. Lehnert A, Dorr W, Lessmann E, Pawelke J. 2008. RBE of 10 kV X-rays determined for the human mammary epithelial cell line MCF-12A. Radiation Research 169:330-336.
37. Lobrich M, Rief N, Kuhne M, Heckmann M, Fleckenstein J, Rube C, Uder M. 2005. In vivo formation and repair of DNA double-strand breaks after computed tomography examinations. Proceedings of National Academy of Sciences of the USA 102:8984-8989.
38. Lukas C, Savic V, Bekker-Jensen S, Doil C, Neumann B, Pedersen RS, Grofte M, Chan KL, Hickson ID, Bartek J, et al. 2011. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nature Cell Biology 13:243-253.
39. Panteleeva A, Slonina D, Brankovic K, Spekl K, Pawelke J, Hoinkis C, Dorr W. 2003. Clonogenic survival of human keratinocytes and rodent fibroblasts after irradiation with 25 kV x-rays. Radiation Environmental Biophysics 42:95-100.
40. Powell SN, Kachnic LA. 2003. Roles of BRCA1 and BRCA2 in homologous recombination, DNA replication fidelity and the cellular response to ionizing radiation. Oncogene 22:5784-5791.
41. Puc J, Keniry M, Li HS, Pandita TK, Choudhury AD, Memeo L, Mansukhani M, Murty VV, Gaciong Z, Meek SE, et al. 2005. Lack of PTEN sequesters CHK1 and initiates genetic instability. Cancer Cell 7: 193-204.
42. Redpath JL, Lu Q, Lao X, Molloi S, Elmore E. 2003. Low doses of diagnostic energy X-rays protect against neoplastic transformation in vitro. International Journal of Radiation Biology 79:235-240.
43. Ripperger T, Gadzicki D, Meindl A, Schlegelberger B. 2009. Breast cancer susceptibility: Current knowledge and implications for genetic counselling. European Journal of Human Genetics 17:722-731.
44. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. 1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. Journal of Biology Chemistry 273:5858-5868.
45. Rothkamm K, Lobrich M. 2003. Evidence for a lack of DNA double-strand break repair in human cells exposed to very low x-ray doses. Proceedings of National Academy of Sciences of the USA 100:5057-5062.
46. Rothkamm K, Balroop S, Shekhdar J, Fernie P, Goh V. 2007. Leukocyte DNA damage after multi-detector row CT: A quantitative biomarker of low-level radiation exposure. Radiology 242:244-251.
47. Sardanelli F, Boetes C, Borisch B, Decker T, Federico M, Gilbert FJ, Helbich T, Heywang-Kobrunner SH, Kaiser WA, Kerin MJ, et al. 2010. Magnetic resonance imaging of the breast: Recommendations from the EUSOMA working group. European Journal of Cancer 46:1296-1316.
48. Saslow D, Boetes C, Burke W, Harms S, Leach MO, Lehman CD, Morris E, Pisano E, Schnall M, Sener S, et al. 2007. American Cancer Society guidelines for breast screening with MRI as an adjunct to mammography. Cancer Journal for Clinicians 57:75-89.
49. Schmid E, Regulla D, Kramer HM, Harder D. 2002. The effect of 29 kV X-rays on the dose response of chromosome aberrations in human lymphocytes. Radiation Research 158:771-777.
50. Scully R, Livingston DM. 2000. In search of the tumour-suppressor functions of BRCA1 and BRCA2. Nature 408:429-432.
51. Slonina D, Spekl K, Panteleeva A, Brankovic K, Hoinkis C, Dorr W. 2003.Induction of micronuclei in human fibroblasts and keratinocytes by 25 kV X-rays. Radiation Environmental Biophysics 42:55-61.
52. Smathers RL, Boone JM, Lee LJ, Berns EA, Miller RA, Wright AM. 2007. Radiation dose reduction for augmentation mammography. American Journal od Roentgenology 188:1414-1421.
53. Swift M, Morrell D, Massey RB, Chase CL. 1991. Incidence of cancer in 161 families affected by ataxia-telangiectasia. New England Journal of Medecine 325:1831-1836.
54. Thierens H, Vral A. 2009. The micronucleus assay in radiation accidents. Annali dell'Istituto Superiore di Sanità 45:260-264.
55. Thomas C, Charrier J, Massart C, Cherel M, Fertil B, Barbet J, Foray N. 2008. Low-dose hyper-radiosensitivity of progressive and regressive cells isolated from a rat colon tumour: Impact of DNA repair. International Journal of Radiation Biology 84:533-548.
56. Walsh T, King MC. 2007. Ten genes for inherited breast cancer. Cancer Cell 11:103-105.
57. Warner E, Plewes DB, Hill KA, Causer PA, Zubovits JT, Jong RA, Cutrara MR, DeBoer G, Yaffe MJ, Messner SJ, et al. 2004. Surveillance of BRCA1 and BRCA2 mutation carriers with magnetic resonance imaging, ultrasound, mammography, and clinical breast examination. Journal of the American Medical Association 292:1317-1325.
58. Yaffe MJ, Mainprize JG. 2011. Risk of radiation-induced breast cancer from mammographic screening. Radiology 258:98-105.