H2AX phosphorylation screen of cells from radiosensitive cancer patients reveals a novel DNA double-strand break repair cellular phenotype

British Journal of Cancer

Volumn 102, Issue 10, 2010, Pages 1511-1518

  Vasireddy, R S ^a,b   Sprung, C N ^a,b,c   Cempaka, N L ^a,b   Chao, M ^a,d   McKay, M J ^a,b,e,f  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d Radiation Oncology Victoria   (Australia)

^e CANBERRA HOSPITAL   (Australia)

^f AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

; H2AX; Ionising radiation; Radiosensitivity

Indexed keywords

DNA; DOUBLE STRANDED DNA; HISTONE H2AX;

ADULT; AGED; ARTICLE; CANCER CELL CULTURE; CANCER LOCALIZATION; CANCER PATIENT; CANCER RADIOTHERAPY; CANCER SCREENING; CELL REGENERATION; CLINICAL ARTICLE; CONTROLLED STUDY; DNA STRAND BREAKAGE; FEMALE; HUMAN; HUMAN CELL; IONIZING RADIATION; LYMPHOBLAST; MALE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RADIATION RESPONSE;

ADULT; AGED; AGED, 80 AND OVER; CELL LINE, TUMOR; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GENETIC TECHNIQUES; HISTONES; HUMANS; MALE; MIDDLE AGED; NEOPLASMS; PHENOTYPE; PHOSPHORYLATION; RADIATION TOLERANCE; TUMOR MARKERS, BIOLOGICAL;

EID: 77952116482     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6605666     Document Type: Article

References (57)

1. Alsner J, Andreassen CN, Overgaard J (2008) Genetic markers for prediction of normal tissue toxicity after radiotherapy. Semin Radiat Oncol 18: 126-135
2. Banath JP, Macphail SH, Olive PL (2004) Radiation sensitivity, H2AX phosphorylation, and kinetics of repair of DNA strand breaks in irradiated cervical cancer cell lines. Cancer Res 64: 7144-7149
3. Bassing CH, Alt FW (2004) H2AX may function as an anchor to hold broken chromosomal DNA ends in close proximity. Cell Cycle 3: 149-153
4. Bassing CH, Chua KF, Sekiguchi J, Suh H, Whitlow SR, Fleming JC, Monroe BC, Ciccone DN, Yan C, Vlasakova K, Livingston DM, Ferguson DO, Scully R, Alt FW (2002) Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc Natl Acad Sci USA 99: 8173-8178
5. Bouquet F, Muller C, Salles B (2006) The loss of gammaH2AX signal is a marker of DNA double strand breaks repair only at low levels of DNA damage. Cell Cycle 5: 1116-1122
6. Brammer I, Zoller M, Dikomey E (2001) Relationship between cellular radiosensitivity and DNA damage measured by comet assay in human normal, NBS and AT fibroblasts. Int J Radiat Biol 77: 929-938
7. Brock WA, Tucker SL, Geara FB, Turesson I, Wike J, Nyman J, Peters LJ (1995) Fibroblast radiosensitivity versus acute and late normal skin responses in patients treated for breast cancer. Int J Radiat Oncol Biol Phys 32: 1371-1379
8. Burma S, Chen DJ (2004) Role of DNA-PK in the cellular response to DNA double-strand breaks. DNA Repair (Amst) 3: 909-918
9. Celeste A, Fernandez-Capetillo O, Kruhlak MJ, Pilch DR, Staudt DW, Lee A, Bonner RF, Bonner WM, Nussenzweig A (2003) Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat Cell Biol 5: 675-679
10. Chowdhury D, Keogh MC, Ishii H, Peterson CL, Buratowski S, Lieberman J (2005) gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol Cell 20: 801-809
11. Distel L, Neubauer S, Varon R, Holter W, Grabenbauer G (2003) Fatal toxicity following radio-and chemotherapy of medulloblastoma in a child with unrecognized Nijmegen breakage syndrome. Med Pediatr Oncol 41: 44-48
12. Distel LV, Neubauer S, Keller U, Sprung CN, Sauer R, Grabenbauer GG (2006) Individual differences in chromosomal aberrations after in vitro irradiation of cells from healthy individuals, cancer and cancer susceptibility syndrome patients. Radiother Oncol 81: 257-263
13. Gurska S, Farkasova T, Gabelova A (2007) Radiosensitivity of cervical cancer cell lines: the impact of polymorphisms in DNA repair genes. Neoplasma 54: 195-201
14. Ismail IH, Wadhra TI, Hammarsten O (2007) An optimized method for detecting gamma-H2AX in blood cells reveals a significant interindivi-dual variation in the gamma-H2AX response among humans. Nucleic Acids Res 35: e36
15. Ismail SM, Puppi M, Prithivirajsingh S, Munshi A, Raju U, Meyn RE, Buchholz TA, Story MD, Brock WA, Milas L, Thames HD, Stevens CW (2004) Predicting radiosensitivity using DNA end-binding complex analysis. Clin Cancer Res 10: 1226-1234
16. Keogh MC, Kim JA, Downey M, Fillingham J, Chowdhury D, Harrison JC, Onishi M, Datta N, Galicia S, Emili A, Lieberman J, Shen X, Buratowski S, Haber JE, Durocher D, Greenblatt JF, Krogan NJ (2006) A phosphatase complex that dephosphorylates gammaH2AX regulates DNA damage checkpoint recovery. Nature 439: 497-501
17. Klokov D, MacPhail SM, Banath JP, Byrne JP, Olive PL (2006) Phosphorylated histone H2AX in relation to cell survival in tumor cells and xenografts exposed to single and fractionated doses of X-rays. Radiother Oncol 80: 223-229
18. Kuhne M, Riballo E, Rief N, Rothkamm K, Jeggo PA, Lobrich M (2004) A double-strand break repair defect in ATM-deficient cells contributes to radiosensitivity. Cancer Res 64: 500-508
19. Kusch T, Florens L, Macdonald WH, Swanson SK, Glaser RL, Yates III JR, Abmayr SM, Washburn MP, Workman JL (2004) Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 306: 2084-2087
20. Leong T, Whitty J, Keilar M, Mifsud S, Ramsay J, Birrell G, Venter D, Southey M, McKay M (2000) Mutation analysis of BRCA1 and BRCA2 cancer predisposition genes in radiation hypersensitive cancer patients. Int J Radiat Oncol Biol Phys 48: 959-965
21. Lovelock PK, Wong EM, Sprung CN, Marsh A, Hobson K, French JD, Southey M, Sculley T, Pandeya N, Brown MA, Chenevix-Trench G, Spurdle AB, kConFab Investigators, McKay MJ (2007) Prediction of BRCA1 and BRCA2 mutation status using post-irradiation assays of lymphoblastoid cell lines is compromised by inter-cell-line phenotypic variability. Breast Cancer Res Treat 104(3): 257-266
22. MacPhail SH, Banath JP, Yu TY, Chu EH, Lambur H, Olive PL (2003) Expression of phosphorylated histone H2AX in cultured cell lines following exposure to X-rays. Int J Radiat Biol 79: 351-358
23. Mahrhofer H, Burger S, Oppitz U, Flentje M, Djuzenova CS (2006) Radiation induced DNA damage and damage repair in human tumor and fibroblast cell lines assessed by histone H2AX phosphorylation. Int J Radiat Oncol Biol Phys 64: 573-580
24. McGowan CH, Russell P (2004) The DNA damage response: sensing and signaling. Curr Opin Cell Biol 16: 629-633
25. McIlrath J, Bouffler SD, Samper E, Cuthbert A, Wojcik A, Szumiel I, Bryant PE, Riches AC, Thompson A, Blasco MA, Newbold RF, Slijepcevic P (2001) Telomere length abnormalities in mammalian radiosensitive cells. Cancer Res 61: 912-915
26. McKay MJ, Kefford RF (1995) The spectrum of in vitro radiosensitivity in four human melanoma cell lines is not accounted for by differential induction or rejoining of DNA double strand breaks. Int J Radiat Oncol Biol Phys 31: 345-352
27. Morgan G, Ward R, Barton M (2004) The contribution of cytotoxic chemotherapy to 5-year survival in adult malignancies. Clin Oncol (R Coll Radiol) 16: 549-560
28. Nachtrab U, Oppitz U, Flentje M, Stopper H (1998) Radiation-induced micronucleus formation in human skin fibroblasts of patients showing severe and normal tissue damage after radiotherapy. Int J Radiat Biol 73: 279-287
29. Neitzel H (1986) A routine method for the establishment of permanent growing lymphoblastoid cell lines. Hum Genet 73: 320-326
30. Nelms BE, Maser RS, MacKay JF, Lagally MG, Petrini JH (1998) In situ visualization of DNA double-strand break repair in human fibroblasts. Science 280: 590-592
31. Neubauer S, Arutyunyan R, Stumm M, Dork T, Bendix R, Bremer M, Varon R, Sauer R, Gebhart E (2002) Radiosensitivity of ataxia telangiectasia and Nijmegen breakage syndrome homozygotes and heterozygotes as determined by three-color FISH chromosome painting. Radiat Res 157: 312-321
32. Neubauer S, Dunst J, Gebhart E (1997) The impact of complex chromosomal rearrangements on the detection of radiosensitivity in cancer patients. Radiother Oncol 43: 189-195
33. Olive PL, Banath JP (2004) Phosphorylation of histone H2AX as a measure of radiosensitivity. Int J Radiat Oncol Biol Phys 58: 331-335
34. Olive PL, Banath JP, Keyes M (2008) Residual gammaH2AX after irradiation of human lymphocytes and monocytes in vitro and its relation to late effects after prostate brachytherapy. Radiother Oncol 86: 336-346
35. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, Bonner WM (2000) A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 10: 886-895
36. Petersen S, Casellas R, Reina-San-Martin B, Chen HT, Difilippantonio MJ, Wilson PC, Hanitsch L, Celeste A, Muramatsu M, Pilch DR, Redon C, Ried T, Bonner WM, Honjo T, Nussenzweig MC, Nussenzweig A (2001) AID is required to initiate Nbs1/gamma-H2AX focus formation and mutations at sites of class switching. Nature 414: 660-665
37. Qvarnström OF, Simonsson M, Johansson KA, Nyman J, Turesson I (2004) DNA double strand break quantification in skin biopsies. Radiother Oncol 72: 311-317
38. Rieger KE, Hong WJ, Tusher VG, Tang J, Tibshirani R, Chu G (2004) Toxicity from radiation therapy associated with abnormal transcriptional responses to DNA damage. Proc Natl Acad Sci USA 101: 6635-6640
39. Rogakou EP, Boon C, Redon C, Bonner WM (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146: 905-916
40. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858-5868
41. Sedelnikova OA, Rogakou EP, Panyutin IG, Bonner WM (2002) Quantitative detection of (125)IdU-induced DNA double-strand breaks with gamma-H2AX antibody. Radiat Res 158: 486-492
42. Severin DM, Leong T, Cassidy B, Elsaleh H, Peters L, Venter D, Southey M, McKay M (2001) Novel DNA sequence variants in the hHR21 DNA repair gene in radiosensitive cancer patients. Int J Radiat Oncol Biol Phys 50: 1323-1331
43. Shiloh Y (2001) ATM and ATR: networking cellular responses to DNA damage. Curr Opin Genet Dev 11: 71-77
44. Shiloh Y (2003) ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 3: 155-168
45. Sprung CN, Chao M, Leong T, McKay MJ (2005) Chromosomal radio-sensitivity in two cell lineages derived from clinically radiosensitive cancer patients. Clin Cancer Res 11: 6352-6358
46. Sprung CN, Davey DS, Withana NP, Distel LV, McKay MJ (2008) Telomere length in lymphoblast cell lines derived from clinically radiosensitive cancer patients. Cancer Biol Ther 7: 1-7
47. Sprung CN, Mathews LJ, McKay MJ (2002) DNA repair deficiencies: connecting carcinogenesis and sensitivity to ionising radiation. Today's Life Science 14: 40-44
48. Spycher C, Miller ES, Townsend K, Pavic L, Morrice NA, Janscak P, Stewart GS, Stucki M (2008) Constitutive phosphorylation of MDC1 physically links the MRE11-RAD50-NBS1 complex to damaged chromatin. J Cell Biol 181: 227-240
49. Stucki M, Jackson SP (2006) gammaH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair (Amst) 5: 534-543
50. Svensson JP, Stalpers LJ, Esveldt-van Lange RE, Franken NA, Haveman J, Klein B, Turesson I, Vrieling H, Giphart-Gassler M (2006) Analysis of gene expression using gene sets discriminates cancer patients with and without late radiation toxicity. PLoS Med 3: e422
51. Svetlova M, Solovjeva L, Nishi K, Nazarov I, Siino J, Tomilin N (2007) Elimination of radiation-induced gamma-H2AX foci in mammalian nucleus can occur by histone exchange. Biochem Biophys Res Commun 358: 650-654
52. Taneja N, Davis M, Choy JS, Beckett MA, Singh R, Kron SJ, Weichselbaum RR (2004) Histone H2AX phosphorylation as a predictor of radio-sensitivity and target for radiotherapy. J Biol Chem 279: 2273-2280
53. Vilenchik MM, Knudson AG (2003) Endogenous DNA double-strand breaks: production, fidelity of repair, and induction of cancer. Proc Natl Acad Sci USA 100: 12871-12876
54. West CM, Davidson SE, Elyan SA, Swindell R, Roberts SA, Orton CJ, Coyle CA, Valentine H, Wilks DP, Hunter RD, Hendry JH (1998) The intrinsic radiosensitivity of normal and tumour cells. Int J Radiat Biol 73: 409-413
55. Wilding CS, Curwen GB, Tawn EJ, Sheng X, Winther JF, Chakraborty R, Boice Jr JD (2007) Influence of polymorphisms at loci encoding DNA repair proteins on cancer susceptibility and G2 chromosomal radio-sensitivity. Environ Mol Mutagen 48: 48-57
56. Wurm R, Burnet NG, Duggal N, Yarnold JR, Peacock JH (1994) Cellular radiosensitivity and DNA damage in primary human fibroblasts. Int J Radiat Oncol Biol Phys 30: 625-633
57. Zhou PK, Sproston AR, Marples B, West CM, Margison GP, Hendry JH (1998) The radiosensitivity of human fibroblast cell lines correlates with residual levels of DNA double-strand breaks. Radiother Oncol 47: 271-276