Endogenous expression of phosphorylated histone H2AX in tumors in relation to DNA double-strand breaks and genomic instability

DNA Repair

Volumn 5, Issue 8, 2006, Pages 935-946

  Yu, T ^a   MacPhail, S H ^a   Banath J P ^a   Klokov, D ^a   Olive, P L ^a  

^a BRITISH COLUMBIA CANCER RESEARCH CENTRE   (Canada)

Author keywords

H2AX; Comet assay; DSB; Genome instability; Ionizing radiation

Indexed keywords

DOUBLE STRANDED DNA; HISTONE H2AX; PROTEIN P53;

ARTICLE; CANCER CELL CULTURE; CELL LINE; CHROMOSOME REARRANGEMENT; CHROMOSOME STRUCTURE; COMPARATIVE STUDY; CONTROLLED STUDY; DNA REPAIR; DNA STRAND BREAKAGE; DRUG SCREENING; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; HUMAN TISSUE; KARYOTYPE; LUNG FIBROBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SENESCENCE; TELOMERE; UTERINE CERVIX CARCINOMA; WILD TYPE;

CELL LINE, TUMOR; COMET ASSAY; DNA DAMAGE; FLOW CYTOMETRY; GENES, P53; GENOMIC INSTABILITY; HISTONES; HUMANS; IMMUNOHISTOCHEMISTRY; NEOPLASMS; PHOSPHORYLATION;

EID: 33746721468     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2006.05.040     Document Type: Article

References (39)

1. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., and Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273 (1998) 5858-5868
2. Paull T.T., Rogakou E.P., Yamazaki V., Kirchgessner C.U., Gellert M., and Bonner W.M. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10 (2000) 886-895
3. Rothkamm K., and Lobrich 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. U.S.A. 100 (2003) 5057-5062
4. Sedelnikova O.A., Rogakou E.P., Panyutin I.G., and Bonner W.M. Quantitative detection of (125)IdU-induced DNA double-strand breaks with gamma-H2AX antibody. Radiat. Res. 158 (2002) 486-492
5. Keogh M.C., Kim J.A., Downey M., Fillingham J., Chowdhury D., Harrison J.C., Onishi M., Datta N., Galicia S., Emili A., Lieberman J., Shen X., Buratowski S., Haber J.E., Durocher D., Greenblatt J.F., and Krogan N.J. A phosphatase complex that dephosphorylates gammaH2AX regulates DNA damage checkpoint recovery. Nature 439 (2006) 497-501
6. MacPhail S.H., Banath J.P., Yu T.Y., Chu E.H., Lambur H., and Olive P.L. Expression of phosphorylated histone H2AX in cultured cell lines following exposure to X-rays. Int. J. Radiat. Biol. 79 (2003) 351-358
7. Taneja N., Davis M., Choy J.S., Beckett M.A., Singh R., Kron S.J., and Weichselbaum R.R. Histone H2AX phosphorylation as a predictor of radiosensitivity and target for radiotherapy. J. Biol. Chem. 279 (2004) 2273-2280
8. Banath J.P., MacPhail S.H., and Olive P.L. Radiation sensitivity, H2AX phosphorylation, and kinetics of repair of DNA strand breaks in irradiated cervical cancer cell lines. Cancer Res. 64 (2004) 7144-7149
9. Limoli C.L., Giedzinski E., Bonner W.M., and Cleaver J.E. UV-induced replication arrest in the xeroderma pigmentosum variant leads to DNA double-strand breaks, gamma-H2AX formation, and Mre11 relocalization. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 233-238
10. Rogakou E.P., Boon C., Redon C., and Bonner W.M. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146 (1999) 905-916
11. Chen H.T., Bhandoola A., Difilippantonio M.J., Zhu J., Brown M.J., Tai X., Rogakou E.P., Brotz T.M., Bonner W.M., Ried T., and Nussenzweig A. Response to RAG-mediated VDJ cleavage by NBS1 and gamma-H2AX. Science 290 (2000) 1962-1965
12. Hunter N., Borner G.V., Lichten M., and Kleckner N. Gamma-H2AX illuminates meiosis. Nat. Genet. 27 (2001) 236-238
13. Sedelnikova O.A., Horikawa I., Zimonjic D.B., Popescu N.C., Bonner W.M., and Barrett J.C. Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks. Nat. Cell Biol. 6 (2004) 168-170
14. McManus K.J., and Hendzel M.J. ATM-dependent DNA damage-independent mitotic phosphorylation of H2AX in normally growing mammalian cells. Mol. Biol. Cell. 16 (2005) 5013-5025
15. Bartkova J., Horejsi Z., Koed K., Kramer A., Tort F., Zieger K., Guldberg P., Sehested M., Nesland J.M., Lukas C., Orntoft T., Lukas J., and Bartek J. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434 (2005) 864-870
16. Gorgoulis V.G., Vassiliou L.V., Karakaidos P., Zacharatos P., Kotsinas A., Liloglou T., Venere M., Ditullio Jr. R.A., Kastrinakis N.G., Levy B., Kletsas D., Yoneta A., Herlyn M., Kittas C., and Halazonetis T.D. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434 (2005) 907-913
17. A. Celeste, S. Petersen, P.J. Romanienko, O. Fernandez-Capetillo, H.T. Chen, O.A. Sedelnikova, B. Reina-San-Martin, V. Coppola, E. Meffre, M.J. Difilippantonio, C. Redon, D.R. Pilch, A. Olaru, M. Eckhaus, R.D., L. Tessarollo, F. Livak, K. Manova, W.M. Bonner, M.C. Nussenzweig, A. Nussenzweig. Genomic instability in mice lacking histone H2AX, Science 296 (2002) 922-927.
18. Warters R.L., Adamson P.J., Pond C.D., and Leachman S.A. Melanoma cells express elevated levels of phosphorylated histone H2AX foci. J. Invest. Dermatol. 124 (2005) 807-817
19. Roschke A.V., Tonon G., Gehlhaus K.S., McTyre N., Bussey K.J., Lababidi S., Scudiero D.A., Weinstein J.N., and Kirsch I.R. Karyotypic complexity of the NCI-60 drug-screening panel. Cancer Res. 63 (2003) 8634-8647
20. Blumenthal R.D., Leone E., Goldenberg D.M., Rodriguez M., and Modrak D. An in vitro model to optimize dose scheduling of multimodal radioimmunotherapy and chemotherapy: effects of p53 expression. Int. J. Cancer 108 (2004) 293-300
21. MacPhail S.H., Banath J.P., Yu Y., Chu E., and Olive P.L. Cell cycle-dependent expression of phosphorylated histone H2AX: reduced expression in unirradiated but not X-irradiated G(1)-phase cells. Radiat. Res. 159 (2003) 759-767
22. Olive P.L., and Banáth J.P. Detection of DNA double-strand breaks through the cell cycle after exposure to X-rays, bleomycin, etoposide and 125IdUrd. Int. J. Radiat. Biol. 64 (1993) 349-358
23. Johnston P.J., Olive P.L., and Bryant P.E. Higher-order chromatin structure-dependent repair of DNA double-strand breaks: modeling the elution of DNA from nucleoids. Radiat. Res. 148 (1997) 561-567
24. Raderschall E., Stout K., Freier S., Suckow V., Schweiger S., and Haaf T. Elevated levels of Rad51 recombination protein in tumor cells. Cancer Res. 62 (2002) 219-225
25. Ward I.M., Minn K., van D.J., and Chen J. p53 Binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice. Mol. Cell Biol. 23 (2003) 2556-2563
26. O'Connor P.M., Jackman J., Bae I., Myers T.G., Fan S., Mutoh M., Scudiero D.A., Monks A., Sausville E.A., Weinstein J.N., Friend S., Fornace A.J.J., and Kohn K.W. Characterization of the p53 tumor suppressor pathway in cell lines of the National Cancer Institute anticancer drug screen and correlations with the growth-inhibitory potency of 123 anticancer agents. Cancer Res. 57 (1997) 4285-4300
27. Dahm-Daphi J. p53: biology and role for cellular radiosensitivity, Strahlenther. Onkology 176 (2000) 278-285
28. Nishizuka S., Charboneau L., Young L., Major S., Reinhold W.C., Waltham M., Kouros-Mehr H., Bussey K.J., Lee J.K., Espina V., Munson P.J., Petricoin E.3rd., Liotta L.A., and Weinstein J.N. Proteomic profiling of the NCI-60 cancer cell lines using new high-density reverse-phase lysate microarrays. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 14229-14234
29. Ross D.T., Scherf U., Eisen M.B., Perou C.M., Rees C., Spellman P., Iyer V., Jeffrey S.S., Van de R.M., Waltham M., Pergamenschikov A., Lee J.C., Lashkari D., Shalon D., Myers T.G., Weinstein J.N., Botstein D., and Brown P.O. Systematic variation in gene expression patterns in human cancer cell lines. Nat. Genet. 24 (2000) 227-235
30. Torres-Roca J.F., Eschrich S., Zhao H., Bloom G., Sung J., McCarthy S., Cantor A.B., Scuto A., Li C., Zhang S., Jove R., and Yeatman T. Prediction of radiation sensitivity using a gene expression classifier. Cancer Res. 65 (2005) 7169-7176
31. Al-Wahiby S., and Slijepcevic P. Chromosomal aberrations involving telomeres in BRCA1 deficient human and mouse cell lines. Cytogenet. Genome Res. 109 (2005) 491-496
32. Duensing S., and Munger K. The human papillomavirus type 16 E6 and E7 oncoproteins independently induce numerical and structural chromosome instability. Cancer Res. 62 (2002) 7075-7082
33. Soler D., Genesca A., Arnedo G., Egozcue J., and Tusell L. Telomere dysfunction drives chromosomal instability in human mammary epithelial cells. Genes Chromosomes Cancer 44 (2005) 339-350
34. de Lange T., Shiue L., Myers R.M., Cox D.R., Naylor S.L., Killery A.M., and Varmus H.E. Structure and variability of human chromosome ends. Mol. Cell Biol. 10 (1990) 518-527
35. Schwartz J.L., Jordan R., Liber H., Murnane J.P., and Evans H.H. TP53-dependent chromosome instability is associated with transient reductions in telomere length in immortal telomerase-positive cell lines. Genes Chromosomes Cancer 30 (2001) 236-244
36. Artandi S.E., and Attardi L.D. Pathways connecting telomeres and p53 in senescence, apoptosis, and cancer. Biochem. Biophys. Res. Commun. 331 (2005) 881-890
37. S.T. Al Rashid, G. Dellaire, A. Cuddihy, F. Jalali, M. Vaid, C. Coackley, M. Folkard, Y. Xu, B.P. Chen, D.J. Chen, L. Lilge, K.M. Prise, D.P., R.G. Bristow. Evidence for the direct binding of phosphorylated p53 to sites of DNA breaks in vivo, Cancer Res. 65 (2005) 10810-10821.
38. Bertrand P., Saintigny Y., and Lopez B.S. p53's double life: transactivation-independent repression of homologous recombination. Trends Genet. 20 (2004) 235-243
39. Roemer K. Mutant p53: gain-of-function oncoproteins and wild-type p53 inactivators. Biol. Chem. 380 (1999) 879-887