Chronic hypoxia compromises repair of DNA double-strand breaks to drive genetic instability

Journal of Cell Science

Volumn 125, Issue 1, 2012, Pages 189-199

  Kumareswaran, Ramya ^a,b   Ludkovski, Olga ^a   Meng, Alice ^a   Sykes, Jenna ^a   Pintilie, Melania ^a   Bristow, Robert G ^a,b  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

H2AX; DNA double strand break sensors; DNA double strand breaks; Genetic instability; Hypoxia; Non homologous end joining

Indexed keywords

ATM PROTEIN; HISTONE H2AX; PROTEIN P53;

ARTICLE; CELL HYPOXIA; CELL SURVIVAL; CHROMOSOME ABERRATION; CLONOGENESIS; COMET ASSAY; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; FIBROBLAST; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; IRRADIATION; PRIORITY JOURNAL; WESTERN BLOTTING;

CELL CYCLE PROTEINS; CELL HYPOXIA; CELL SURVIVAL; CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATIONS; COMET ASSAY; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; FIBROBLASTS; G0 PHASE; G1 PHASE; HISTONES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEINS;

ATAXIA TELANGIECTASIA;

EID: 84858119890     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.092262     Document Type: Article

References (51)

1. Al Rashid, S. T., Dellaire, G., Cuddihy, A., Jalali, F., Vaid, M., Coackley, C., Folkard, M., Xu, Y., Chen, B. P., Chen, D. J. et al. (2005). Evidence for the direct binding of phosphorylated p53 to sites of DNA breaks in vivo. Cancer Res. 65, 10810-10821.
2. Al Rashid, S. T., Harding, S. M., Law, C., Coackley, C. and Bristow, R. G. (2011). Protein-protein interactions occur between p53 phosphoforms and ATM and 53BP1 at sites of exogenous DNA damage. Radiat. Res. 175, 588-598.
3. Banath, J. P., Sinnott, L., Larrivee, B., MacPhail, S. H. and Olive, P. L. (2005). Growth of V79 cells as xenograft tumors promotes multicellular resistance but does not increase spontaneous or radiation-induced mutant frequency. Radiat. Res. 164, 733-744.
4. Bencokova, Z., Kaufmann, M. R., Pires, I. M., Lecane, P. S., Giaccia, A. J. and Hammond, E. M. (2009). ATM activation and signaling under hypoxic conditions. Mol. Cell. Biol. 29, 526-537.
5. Bindra, R. S., Schaffer, P. J., Meng, A., Woo, J., Maseide, K., Roth, M. E., Lizardi, P., Hedley, D. W., Bristow, R. G. and Glazer, P. M. (2004). Down-regulation of Rad51 and decreased homologous recombination in hypoxic cancer cells. Mol. Cell. Biol. 24, 8504-8518.
6. Bindra, R. S., Gibson, S. L., Meng, A., Westermark, U., Jasin, M., Pierce, A. J., Bristow, R. G., Classon, M. K. and Glazer, P. M. (2005). Hypoxia-induced downregulation of BRCA1 expression by E2Fs. Cancer Res. 65, 11597-11604.
7. Bindra, R. S., Crosby, M. E. and Glazer, P. M. (2007). Regulation of DNA repair in hypoxic cancer cells. Cancer Metastasis Rev. 26, 249-260.
8. Bristow, R. G. and Hill, R. P. (2008). Hypoxia and metabolism. Hypoxia, DNA repair and genetic instability. Nat. Rev. Cancer 8, 180-192.
9. Bromfield, G. P., Meng, A., Warde, P. and Bristow, R. G. (2003). Cell death in irradiated prostate epithelial cells: role of apoptotic and clonogenic cell kill. Prostate Cancer Prostatic Dis. 6, 73-85.
10. Brown, J. M. and Wilson, W. R. (2004). Exploiting tumour hypoxia in cancer treatment. Nat. Rev. Cancer 4, 437-447.
11. Celeste, A., Fernandez-Capetillo, O., Kruhlak, M. J., Pilch, D. R., Staudt, D. W., Lee, A., Bonner, R. F., Bonner, W. M. and Nussenzweig, A. (2003). Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol. 5, 675-679.
12. Chan, N. and Bristow, R. G. (2010). "Contextual" synthetic lethality and/or loss of heterozygosity: tumor hypoxia and modification of DNA repair. Clin. Cancer Res. 16, 4553-4560.
13. Chan, N., Koritzinsky, M., Zhao, H., Bindra, R., Glazer, P. M., Powell, S., Belmaaza, A., Wouters, B. and Bristow, R. G. (2008). Chronic hypoxia decreases synthesis of homologous recombination proteins to offset chemoresistance and radioresistance. Cancer Res. 68, 605-614.
14. Chan, N., Pires, I. M., Bencokova, Z., Coackley, C., Luoto, K. R., Bhogal, N., Lakshman, M., Gottipati, P., Oliver, F. J., Helleday, T. et al. (2010). Contextual synthetic lethality of cancer cell kill based on the tumor microenvironment. Cancer Res. 70, 8045-8054.
15. Chowdhury, D., Keogh, M. C., Ishii, H., Peterson, C. L., Buratowski, S. and Lieberman, J. (2005). gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol. Cell 20, 801-809.
16. Christensen, E., Pintilie, M., Evans, K. R., Lenarduzzi, M., Menard, C., Catton, C. N., Diamandis, E. P. and Bristow, R. G. (2009). Longitudinal cytokine expression during IMRT for prostate cancer and acute treatment toxicity. Clin. Cancer Res. 15, 5576-5583.
17. Coquelle, A., Toledo, F., Stern, S., Bieth, A. and Debatisse, M. (1998). A new role for hypoxia in tumor progression: induction of fragile site triggering genomic rearrangements and formation of complex DMs and HSRs. Mol. Cell 2, 259-265.
18. Falck, J., Coates, J. and Jackson, S. P. (2005). Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434, 605-611.
19. Fan, R., Kumaravel, T. S., Jalali, F., Marrano, P., Squire, J. A. and Bristow, R. G. (2004). Defective DNA strand break repair after DNA damage in prostate cancer cells: implications for genetic instability and prostate cancer progression. Cancer Res. 64, 8526-8533.
20. Fischer, U., Radermacher, J., Mayer, J., Mehraein, Y. and Meese, E. (2008). Tumor hypoxia: Impact on gene amplification in glioblastoma. Int. J. Oncol. 33, 509-515.
21. Fraser, M., Harding, S. M., Zhao, H., Coackley, C., Durocher, D. and Bristow, R. G. (2011). MRE11 promotes AKT phosphorylation in direct response to DNA doublestrand breaks. Cell Cycle 10, 2218-2232.
22. Freiberg, R. A., Hammond, E. M., Dorie, M. J., Welford, S. M. and Giaccia, A. J. (2006). DNA damage during reoxygenation elicits a Chk2-dependent checkpoint response. Mol. Cell. Biol. 26, 1598-1609.
23. Gibson, S. L., Bindra, R. S. and Glazer, P. M. (2005). Hypoxia-induced phosphorylation of Chk2 in an ataxia telangiectasia mutated-dependent manner. Cancer Res. 65, 10734-10741.
24. Hammond, E. M., Dorie, M. J. and Giaccia, A. J. (2003). ATR/ATM targets are phosphorylated by ATR in response to hypoxia and ATM in response to reoxygenation. J. Biol. Chem. 278, 12207-12213.
25. Hammond, E. M., Dorie, M. J. and Giaccia, A. J. (2004). Inhibition of ATR leads to increased sensitivity to hypoxia/reoxygenation. Cancer Res. 64, 6556-6562.
26. Hardin, J. W. and Hilbe, J. (2003). Generalized Estimating Equations. London: Chapman and Hall/CRC.
27. Helleday, T., Lo, J., van Gent, D. C. and Engelward, B. P. (2007). DNA double-strand break repair: from mechanistic understanding to cancer treatment. DNA Repair (Amst.) 6, 923-935.
28. Hickson, I., Zhao, Y., Richardson, C. J., Green, S. J., Martin, N. M., Orr, A. I., Reaper, P. M., Jackson, S. P., Curtin, N. J. and Smith, G. C. (2004). Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res. 64, 9152-9159.
29. Huang, L. E., Bindra, R. S., Glazer, P. M. and Harris, A. L. (2007). Hypoxia-induced genetic instability - a calculated mechanism underlying tumor progression. J. Mol. Med. 85, 139-148.
30. Jackman, R. P., Utter, G. H., Heitman, J. W., Hirschkorn, D. F., Law, J. P., Gefter, N., Busch, M. P. and Norris, P. J. (2011). Effects of blood sample age at time of separation on measured cytokine concentrations in human plasma. Clin. Vaccine Immunol. 18, 318-326.
31. Jeggo, P. A. and Lobrich, M. (2007). DNA double-strand breaks: their cellular and clinical impact? Oncogene 26, 7717-7719.
32. Kaspler, P., Pintilie, M. and Hill, R. P. (2009). Dynamics of micronuclei in rat skin fibroblasts after X irradiation. Radiat. Res. 172, 106-113.
33. Lara, P. C., Lloret, M., Clavo, B., Apolinario, R. M., Bordon, E., Rey, A., Falcon, O., Alonso, A. R. and Belka, C. (2008). Hypoxia downregulates Ku70/80 expression in cervical carcinoma tumors. Radiother. Oncol. 89, 222-226.
34. Lee, J. H., Choi, I. J., Song, D. K. and Kim, D. K. (2010). Genetic instability in the human lymphocyte exposed to hypoxia. Cancer Genet. Cytogenet. 196, 83-88.
35. Liang, K. and Zeger, S. L. (1986). Longitudinal data analysis using generalized linear models. Biometrika 73, 13-22.
36. Little, J. B. and Nagasawa, H. (1985). Effect of confluent holding on potentially lethal damage repair, cell cycle progression, and chromosomal aberrations in human normal and ataxia-telangiectasia fibroblasts. Radiat. Res. 101, 81-93.
37. Little, J. B., Nagasawa, H., Dahlberg, W. K., Zdzienicka, M. Z., Burma, S. and Chen, D. J. (2002). Differing responses of Nijmegen breakage syndrome and ataxia telangiectasia cells to ionizing radiation. Radiat. Res. 158, 319-326.
38. Liu, S. K., Coackley, C., Krause, M., Jalali, F., Chan, N. and Bristow, R. G. (2008). A novel poly(ADP-ribose) polymerase inhibitor, ABT-888, radiosensitizes malignant human cell lines under hypoxia. Radiother. Oncol. 88, 258-268.
39. Marconi, V. C., Grandits, G., Okulicz, J. F., Wortmann, G., Ganesan, A., Crum-Cianflone, N., Polis, M., Landrum, M., Dolan, M. J., Ahuja, S. K. et al. (2011). Cumulative viral load and virologic decay patterns after antiretroviral therapy in HIVinfected subjects influence CD4 recovery and AIDS. PLoS ONE 6, e17956.
40. Meng, A. X., Jalali, F., Cuddihy, A., Chan, N., Bindra, R. S., Glazer, P. M. and Bristow, R. G. (2005). Hypoxia down-regulates DNA double strand break repair gene expression in prostate cancer cells. Radiother. Oncol. 76, 168-176.
41. O'Driscoll, M. and Jeggo, P. A. (2006). The role of double-strand break repair - insights from human genetics. Nat. Rev. Genet. 7, 45-54.
42. Olive, P. L. and Banath, J. P. (2004). Phosphorylation of histone H2AX as a measure of radiosensitivity. Int. J. Radiat. Oncol. Biol. Phys. 58, 331-335.
43. Ozeri-Galai, E., Schwartz, M., Rahat, A. and Kerem, B. (2008). Interplay between ATM and ATR in the regulation of common fragile site stability. Oncogene 27, 2109-2117.
44. Paull, T. T., Rogakou, E. P., Yamazaki, V., Kirchgessner, C. U., Gellert, M. and Bonner, W. M. (2000). A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10, 886-895.
45. Revai, K., Patel, J. A., Grady, J. J., Nair, S., Matalon, R. and Chonmaitree, T. (2009). Association between cytokine gene polymorphisms and risk for upper respiratory tract infection and acute otitis media. Clin. Infect. Dis. 49, 257-261.
46. Rogakou, E. P., Pilch, D. R., Orr, A. H., Ivanova, V. S. and Bonner, W. M. (1998). DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273, 5858-5868.
47. Sprong, D., Janssen, H. L., Vens, C. and Begg, A. C. (2006). Resistance of hypoxic cells to ionizing radiation is influenced by homologous recombination status. Int. J. Radiat. Oncol. Biol. Phys. 64, 562-572.
48. Stiff, T., O'Driscoll, M., Rief, N., Iwabuchi, K., Lobrich, M. and Jeggo, P. A. (2004). ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res. 64, 2390-2396.
49. Um, J. H., Kang, C. D., Bae, J. H., Shin, G. G., Kim, D. W., Kim, D. W., Chung, B. S. and Kim, S. H. (2004). Association of DNA-dependent protein kinase with hypoxia inducible factor-1 and its implication in resistance to anticancer drugs in hypoxic tumor cells. Exp. Mol. Med. 36, 233-242.
50. Weichselbaum, R. R., Withers, H. R., Tomkinson, K. and Little, J. (1983). Potentially lethal damage repair (PLDR) in X-irradiated cultures of a normal human diploid fibroblast cell strain. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med. 43, 313-319.
51. Wu, W., Wang, M., Wu, W., Singh, S. K., Mussfeldt, T. and Iliakis, G. (2008). Repair of radiation induced DNA double strand breaks by backup NHEJ is enhanced in G2. DNA Repair (Amst.) 7, 329-338.