Regulation of DNA repair in hypoxic cancer cells (original) (raw)

References

  1. Li, C. Y., Little, J. B., Hu, K., Zhang, W., Zhang, L., Dewhirst, M. W., et al. (2001). Persistent genetic instability in cancer cells induced by non-DNA-damaging stress exposures. Cancer Research, 61(2), 428–432.
    PubMed CAS Google Scholar
  2. Paquette, B., & Little, J. B. (1994). In vivo enhancement of genomic instability in minisatellite sequences of mouse C3H/10T1/2 cells transformed in vitro by X-rays. Cancer Research, 54(12), 3173–3178.
    PubMed CAS Google Scholar
  3. Reynolds, T. Y., Rockwell, S., & Glazer, P. M. (1996). Genetic instability induced by the tumor microenvironment. Cancer Research, 56(24), 5754–5757.
    PubMed CAS Google Scholar
  4. Yuan, J., Narayanan, L., Rockwell, S., & Glazer, P. M. (2000). Diminished DNA repair and elevated mutagenesis in mammalian cells exposed to hypoxia and low pH. Cancer Research, 60(16), 4372–4376.
    PubMed CAS Google Scholar
  5. Hammond, E. M., Dorie, M. J., & Giaccia, A. J. (2003). ATR/ATM targets are phosphorylated by ATR in response to hypoxia and ATM in response to reoxygenation. Journal of Biological Chemistry, 278(14), 12207–12213.
    Article PubMed CAS Google Scholar
  6. Coquelle, A., Pipiras, E., Toledo, F., Buttin, G., & Debatisse, M. (1997). Expression of fragile sites triggers intrachromosomal mammalian gene amplification and sets boundaries to early amplicons. Cell, 89(2), 215–225.
    Article PubMed CAS Google Scholar
  7. Coquelle, A., Rozier, L., Dutrillaux, B., & Debatisse, M. (2002). Induction of multiple double-strand breaks within an hsr by meganucleaseI-SceI expression or fragile site activation leads to formation of double minutes and other chromosomal rearrangements. Oncogene, 21(50), 7671–7679.
    Article PubMed CAS Google Scholar
  8. Coquelle, A., Toledo, F., Stern, S., Bieth, A., & 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. Molecular Cell, 2(2), 259–265.
    Article PubMed CAS Google Scholar
  9. Subarsky, P., & Hill, R. P. (2003). The hypoxic tumour microenvironment and metastatic progression. Clinical & Experimental Metastasis, 20(3), 237–250.
    Article CAS Google Scholar
  10. Young, S. D., & Hill, R. P. (1990). Effects of reoxygenation on cells from hypoxic regions of solid tumors: Analysis of transplanted murine tumors for evidence of DNA overreplication. Cancer Research, 50(16), 5031–5038.
    PubMed CAS Google Scholar
  11. Young, S. D., Marshall, R. S., & Hill, R. P. (1988). Hypoxia induces DNA overreplication and enhances metastatic potential of murine tumor cells. Proceedings of the National Academy of Sciences of the United States of America, 85(24), 9533–9537.
    Article PubMed CAS Google Scholar
  12. Mihaylova, V. T., Bindra, R. S., Yuan, J., Campisi, D., Narayanan, L., Jensen, R., et al. (2003). Decreased expression of the DNA mismatch repair gene Mlh1 under hypoxic stress in mammalian cells. Molecular & Cellular Biology, 23(9), 3265–3273.
    Article CAS Google Scholar
  13. Koshiji, M., To, K. K., Hammer, S., Kumamoto, K., Harris, A. L., Modrich, P., et al. (2005). HIF-1alpha induces genetic instability by transcriptionally downregulating MutSalpha expression. Molecular Cell, 17(6), 793–803.
    Article PubMed CAS Google Scholar
  14. Bindra, R. S., & Glazer, P. M. (2007). Co-repression of mismatch repair gene expression by hypoxia in cancer cells: Role of the Myc/Max network. Cancer Letters, (in press).
  15. Chen, H., Yan, Y., Davidson, T. L., Shinkai, Y., & Costa, M. (2006). Hypoxic stress induces dimethylated histone H3 lysine 9 through histone methyltransferase G9a in mammalian cells. Cancer Research, 66(18), 9009–9016.
    Article PubMed CAS Google Scholar
  16. Francia, G., Green, S. K., Bocci, G., Man, S., Emmenegger, U., Ebos, J. M. L., et al. (2005). Down-regulation of DNA mismatch repair proteins in human and murine tumor spheroids: Implications for multicellular resistance to alkylating agents. Molecular Cancer Theraphy, 4(10), 1484–1494.
    Article CAS Google Scholar
  17. Papp-Szabo, E., Josephy, P. D., & Coomber, B. L. (2005). Microenvironmental influences on mutagenesis in mammary epithelial cells. International Journal of Cancer, 116(5), 679–685.
    Article CAS Google Scholar
  18. Shahrzad, S., Quayle, L., Stone, C., Plumb, C., Shirasawa, S., Rak, J. W., et al. (2005). Ischemia-induced K-ras mutations in human colorectal cancer cells: Role of microenvironmental regulation of MSH2 expression. Cancer Research, 65(18), 8134–8141.
    Article PubMed CAS Google Scholar
  19. Bindra, R. S., Gibson, S. L., Meng, A., Westermark, U., Jasin, M., Pierce, A. J., et al. (2005). Hypoxia-induced down-regulation of BRCA1 expression by E2Fs. Cancer Research, 65(24), 11597–11604.
    Article PubMed CAS Google Scholar
  20. Bindra, R. S., & Glazer, P. M. (2006). Repression of RAD51 gene expression by E2F4/p130 complexes in hypoxia. Oncogene, (in press).
  21. Meng, A. X., Jalali, F., Cuddihy, A., Chan, N., Bindra, R. S., Glazer, P. M., et al. (2005). Hypoxia down-regulates DNA double strand break repair gene expression in prostate cancer cells. Radiotherapy and Oncology, 76(2), 168–176.
    Article PubMed CAS Google Scholar
  22. Harris, A. L. (2002). Hypoxia—A key regulatory factor in tumour growth. Nature Reviews Cancer, 2(1), 38–47.
    Article PubMed CAS Google Scholar
  23. Freiberg, R. A., Hammond, E. M., Dorie, M. J., Welford, S. M., & Giaccia, A. M. (2006). DNA damage during reoxygenation elicits a Chk2-dependent checkpoint response. Molecular and Cellular Biology, 26(5), 1598–1609.
    Article PubMed CAS Google Scholar
  24. Freiberg, R. A., Krieg, A. J., Giaccia, A. J., & Hammond, E. M. (2006). Checking in on hypoxia/reoxygenation. Cell Cycle, 5(12), 1304–1307.
    PubMed CAS Google Scholar
  25. Gibson, S. L., Bindra, R. S., & Glazer, P. M. (2005). Hypoxia-induced phosphorylation of Chk2 in an ataxia telangiectasia mutated-dependent manner. Cancer Research, 65(23), 10734–10741.
    Article PubMed CAS Google Scholar
  26. Gibson, S. L., Bindra, R. S., & Glazer, P. M. (2006). CHK2-dependent phosphorylation of BRCA1 in hypoxia. Radiation Research, 166(4), 646–651.
    Article PubMed CAS Google Scholar
  27. Hammond, E. M., Denko, N. C., Dorie, M. J., Abraham, R. T., & Giaccia, A. J. (2002). Hypoxia links ATR and p53 through replication arrest. Molecular & Cellular Biology, 22(6), 1834–1843.
    Article CAS Google Scholar
  28. Hammond, E. M., Dorie, M. J., & Giaccia, A. J. (2004). Inhibition of ATR leads to increased sensitivity to hypoxia/reoxygenation. Cancer Research, 64(18), 6556–6562.
    Article PubMed CAS Google Scholar
  29. Hammond, E. M., Green, S. L., & Giaccia, A. J. (2003). Comparison of hypoxia-induced replication arrest with hydroxyurea and aphidicolin-induced arrest. Mutation Research, 532(1–2), 205–213.
    PubMed CAS Google Scholar
  30. Yao, X., Buermeyer, A. B., Narayanan, L., Tran, D., Baker, S. M., Prolla, T. M., et al. (1999). Different mutator phenotypes in Mlh1-versus Pms2-deficient mice. Proceedings of the National Academy of Sciences of the United States of America, 96(12), 6850–6855.
    Article PubMed CAS Google Scholar
  31. Salnikow, K., Blagosklonny, M. V., Ryan, H., Johnson, R., & Costa, M. (2000). Carcinogenic nickel induces genes involved with hypoxic stress. Cancer Research, 60(1), 38–41.
    PubMed CAS Google Scholar
  32. Mueller-Klieser, W., Freyer, J. P., & Sutherland, R. M. (1986). Influence of glucose and oxygen supply conditions on the oxygenation of multicellular spheroids. British Journal of Cancer, 53(3), 345–353.
    PubMed CAS Google Scholar
  33. Corn, P. G., Ricci, M. S., Scata, K. A., Arsham, A. M., Simon, M. C., Dicker, D. T., et al. (2005). Mxi1 is induced by hypoxia in a HIF-1-dependent manner and protects cells from c-Myc-induced apoptosis. Cancer Biological Therapy, 4(11), 1285–1294.
    CAS Google Scholar
  34. Kaidi, A., Williams, A. C., & Paraskeva, C. (2007). Interaction between beta-catenin and HIF-1 promotes cellular adaptation to hypoxia. Nature Cell Biology, 9(2), 210–217.
    Article PubMed CAS Google Scholar
  35. Khaitan, D., Chandna, S., Arya, M. B., & Dwarakanath, B. S. (2006). Establishment and characterization of multicellular spheroids from a human glioma cell line; Implications for tumor therapy. Journal of Translation Med, 4, 12.
    Article Google Scholar
  36. Krieg, A. J., Hammond, E. M., & Giaccia, A. J. (2006). Functional analysis of p53 binding under differential stresses. Molecular and Cellular Biology, 26(19), 7030–7045.
    Article PubMed CAS Google Scholar
  37. Adhikary, S., & Eilers, M. (2005). Transcriptional regulation and transformation by Myc proteins. Naturalist Review of Molecular and Cellular Biology, 6(8), 635–645.
    Article CAS Google Scholar
  38. Kim, J. W., Zeller, K. I., Wang, Y., Jegga, A. G., Aronow, B. J., O’Donnell, K. A., et al. (2004). Evaluation of myc E-box phylogenetic footprints in glycolytic genes by chromatin immunoprecipitation assays. Molecular Cellular Biology, 24(13), 5923–5936.
    Article PubMed CAS Google Scholar
  39. Nilsson, J. A., & Cleveland, J. L. (2004). Mnt: Master regulator of the Max network. Cell Cycle, 3(5), 588–590.
    PubMed CAS Google Scholar
  40. Bindra, R. S., Schaffer, P. J., Meng, A., Woo, J., Maseide, K., Roth, M. E., et al. (2004). Down-regulation of Rad51 and decreased homologous recombination in hypoxic cancer cells. Molecular and Cellular Biology, 24(19), 8504–8518.
    Article PubMed CAS Google Scholar
  41. Thompson, L. H., & Schild, D. (2002). Recombinational DNA repair and human disease. Mutation Research, 509(1–2), 49–78.
    PubMed CAS Google Scholar
  42. Classon, M., & Dyson, N. (2001). p107 and p130: Versatile proteins with interesting pockets. Experimental Cell Research, 264(1), 135–147.
    Article PubMed CAS Google Scholar
  43. Cobrinik, D. (2005). Pocket proteins and cell cycle control. Oncogene, 24(17), 2796–2809.
    Article PubMed CAS Google Scholar
  44. Zhu, W., Giangrande, P. H., & Nevins, J. R. (2004). E2Fs link the control of G1/S and G2/M transcription. European Molecular Biology Organization Journal, 23(23), 4615–4626.
    CAS Google Scholar
  45. Cam, H., Balciunaite, E., Blais, A., Spektor, A., Scarpulla, R. C., Young, R., et al. (2004). A common set of gene regulatory networks links metabolism and growth inhibition. Molecular Cell, 16(3), 399–411.
    Article PubMed CAS Google Scholar
  46. Cam, H., & Dynlacht, B. D. (2003). Emerging roles for E2F: Beyond the G1/S transition and DNA replication. Cancer Cell, 3(4), 311–316.
    Article PubMed CAS Google Scholar
  47. Lin, W. C., Lin, F. T., & Nevins, J. R. (2001). Selective induction of E2F1 in response to DNA damage, mediated by ATM-dependent phosphorylation. Genes & Development, 15(14), 1833–1844.
    CAS Google Scholar
  48. Pediconi, N., Ianari, A., Costanzo, A., Belloni, L., Gallo, R., Cimino, L., et al. (2003). Differential regulation of E2F1 apoptotic target genes in response to DNA damage. Nature Cell Biology, 5(6), 552–558.
    Article PubMed CAS Google Scholar
  49. Stevens, C., & La Thangue, N. B. (2003). A new role for E2F-1 in checkpoint control. Cell Cycle, 2(5), 435–437.
    PubMed CAS Google Scholar
  50. Stevens, C., & La Thangue, N. B. (2004). The emerging role of E2F-1 in the DNA damage response and checkpoint control. DNA Repair (Amst), 3(8–9), 1071–1079.
    Article CAS Google Scholar
  51. Stevens, C., Smith, L., & La Thangue, N. B. (2003). Chk2 activates E2F-1 in response to DNA damage. Nature Cell Biology, 5(5), 401–409.
    Article PubMed CAS Google Scholar
  52. Koshiji, M., Kageyama, Y., Pete, A., Horikawa, I., Barrett, J. C., Huang, L. E., et al. (2004). HIF-1alpha induces cell cycle arrest by functionally counteracting Myc. European Molecular Biology Organization Journal, 23(9), 1949–1956.
    CAS Google Scholar
  53. Helt, A. M., & Galloway, D. A. (2001). Destabilization of the retinoblastoma tumor suppressor by human papillomavirus type 16 E7 is not sufficient to overcome cell cycle arrest in human keratinocytes. Journal of Virology, 75(15), 6737–6747.
    Article PubMed CAS Google Scholar
  54. Crook, T., & Vousden, K. H. (1994). Interaction of HPV E6 with p53 and associated proteins. Biochemical Society Transactions, 22(1), 52–55.
    PubMed CAS Google Scholar
  55. Dimitrov, S., Brennerova, M., & Forejt, J. (2001). Expression profiles and intergenic structure of head-to-head oriented Brca1 and Nbr1 genes. Gene, 262(1–2), 89–98.
    Article PubMed CAS Google Scholar
  56. Xu, C. F., Brown, M. A., Nicolai, H., Chambers, J. A., Griffiths, B. L., & Solomon, E. (1997). Isolation and characterisation of the NBR2 gene which lies head to head with the human BRCA1 gene. Human Molecular Genetics, 6(7), 1057–1062.
    Article PubMed CAS Google Scholar
  57. Weinmann, A. S., Yan, P. S., Oberley, M. J., Huang, T. H., & Farnham, P. J. (2002). Isolating human transcription factor targets by coupling chromatin immunoprecipitation and CpG island microarray analysis. Genes & Development, 16(2), 235–244.
    Article CAS Google Scholar
  58. Wells, J., & Farnham, P. J. (2002). Characterizing transcription factor binding sites using formaldehyde crosslinking and immunoprecipitation. Methods, 26(1), 48–56.
    Article PubMed CAS Google Scholar
  59. Iwanaga, R., Komori, H., & Ohtani, K. (2004). Differential regulation of expression of the mammalian DNA repair genes by growth stimulation. Oncogene, 23(53), 8581–8590.
    Article PubMed CAS Google Scholar
  60. Kel, A. E., Kel-Margoulis, O. V., Farnham, P. J., Bartley, S. M., Wingender, E., & Zhang, M. Q. (2001). Computer-assisted identification of cell cycle-related genes: New targets for E2F transcription factors. Journal of Molecular Biology, 309(1), 99–120.
    Article PubMed CAS Google Scholar
  61. Garriga, J., Limon, A., Mayol, X., Rane, S. G., Albrecht, J. H., Reddy, E. P., et al. (1998). Differential regulation of the retinoblastoma family of proteins during cell proliferation and differentiation. Biochemical Journal, 333(Pt 3), 645–654.
    PubMed CAS Google Scholar
  62. Barrientes, S., Cooke, C., & Goodrich, D. W. (2000). Glutamic acid mutagenesis of retinoblastoma protein phosphorylation sites has diverse effects on function. Oncogene, 19(4), 562–570.
    Article PubMed CAS Google Scholar
  63. Krucher, N. A., Rubin, E., Tedesco, V. C., Roberts, M. H., Sherry, T. C., & De Leon, G. (2006). Dephosphorylation of Rb (Thr-821) in response to cell stress. Experimental Cell Research, 312(15), 2757–2763.
    Article PubMed CAS Google Scholar
  64. Lonergan, K. M., Iliopoulos, O., Ohh, M., Kamura, T., Conaway, R. C., Conaway, J. W., et al. (1998). Regulation of hypoxia-inducible mRNAs by the von Hippel–Lindau tumor suppressor protein requires binding to complexes containing elongins B/C and Cul2. Molecular and Cellular Biology, 18(2), 732–741.
    PubMed CAS Google Scholar
  65. Hartman, A. R., & Ford, J. M. (2003). BRCA1 and p53: Compensatory roles in DNA repair. Journal of Molecular Medecine, 81(11), 700–707.
    Article CAS Google Scholar
  66. Moynahan, M. E., Chiu, J. W., Koller, B. H., & Jasin, M. (1999). Brca1 controls homology-directed DNA repair. Molecular Cell, 4(4), 511–518.
    Article PubMed CAS Google Scholar
  67. Scully, R., Chen, J., Plug, A., Xiao, Y., Weaver, D., Feunteun, J., et al. (1997). Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell, 88(2), 265–275.
    Article PubMed CAS Google Scholar
  68. Zhang, J., Willers, H., Feng, Z., Ghosh, J. C., Kim, S., Weaver, D. T., et al. (2004). Chk2 phosphorylation of BRCA1 regulates DNA double-strand break repair. Molecular and Cellular Biology, 24(2), 708–718.
    Article PubMed CAS Google Scholar
  69. Valerie, K., & Povirk, L. F. (2003). Regulation and mechanisms of mammalian double-strand break repair. Oncogene, 22(37), 5792–5812.
    Article PubMed CAS Google Scholar
  70. Pierce, A. J., Johnson, R. D., Thompson, L. H., & Jasin, M. (1999). XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes & Development, 13(20), 2633–2638.
    Article CAS Google Scholar
  71. Um, J. H., Kang, C. D., Bae, J. H., Shin, G. G., Kim, D. W., Kim, D. W., et al. (2004). Association of DNA-dependent protein kinase with hypoxia inducible factor-1 and its implication in resistance to anticancer drugs in hypoxic tumor cells. Experimental and Molecular Medicine, 36(3), 233–242.
    PubMed CAS Google Scholar
  72. Unruh, A., Ressell, A., Mohamed, H. G., Johnson, R. S., Nadrowitz, R., Richter, E., et al. (2003). The hypoxia-inducible factor-1 alpha is a negative factor for tumor therapy. Oncogene, 22(21), 3213–3220.
    Article PubMed CAS Google Scholar
  73. Bekker-Jensen, S., Lukas, C., Kitagawa, R., Melander, F., Kastan, M. B., Bartek, J., et al. (2006). Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. Journal of Cell Biology, 173(2), 195–206.
    Article PubMed CAS Google Scholar
  74. Shiloh, Y. (2003). ATM and related protein kinases: Safeguarding genome integrity. Nature Reviews Cancer, 3(3), 155–168.
    Article PubMed CAS Google Scholar
  75. Abraham, R. T. (2004). PI 3-kinase related kinases: ‘Big’ players in stress-induced signaling pathways. DNA Repair (Amst), 3(8–9), 883–887.
    Article CAS Google Scholar
  76. Abraham, R. T. (2004). The ATM-related kinase, hSMG-1, bridges genome and RNA surveillance pathways. DNA Repair (Amst), 3(8–9), 919–925.
    Article CAS Google Scholar
  77. Stiff, T., Walker, S. A., Cerosaletti, K., Goodarzi, A. A., Petermann, E., Concannon, P., et al. (2006). ATR-dependent phosphorylation and activation of ATM in response to UV treatment or replication fork stalling. European Molecular Biology Organization Journal, 25(24), 5775–5782.
    CAS Google Scholar
  78. Bakkenist, C. J., & Kastan, M. B. (2003). DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature, 421(6922), 499–506.
    Article PubMed CAS Google Scholar
  79. Cortez, D., Guntuku, S., Qin, J., & Elledge, S. J. (2001). ATR and ATRIP: partners in checkpoint signaling. Science, 294(5547), 1713–1716.
    Article PubMed CAS Google Scholar
  80. Cortez, D., Wang, Y., Qin, J., & Elledge, S. J. (1999). Requirement of ATM-dependent phosphorylation of brca1 in the DNA damage response to double-strand breaks. Science, 286(5442), 1162–1166.
    Article PubMed CAS Google Scholar
  81. Helt, C. E., Cliby, W. A., Keng, P. C., Bambara, R. A., & O’Reilly, M. A. (2005). Ataxia telangiectasia mutated (ATM) and ATM and Rad3-related protein exhibit selective target specificities in response to different forms of DNA damage. Journal of Biological Chemistry, 280(2), 1186–1192.
    Article PubMed CAS Google Scholar
  82. Green, S. L., Freiberg, R. A., & Giaccia, A. J. (2001). p21(Cip1) and p27(Kip1) regulate cell cycle reentry after hypoxic stress but are not necessary for hypoxia-induced arrest. Molecular & Cellular Biology, 21(4), 1196–1206.
    Article CAS Google Scholar
  83. Foray, N., Marot, D., Gabriel, A., Randrianarison, V., Carr, A. M., Perricaudet, M., et al. (2003). A subset of ATM- and ATR-dependent phosphorylation events requires the BRCA1 protein. European Molecular Biology Organization Journal, 22(11), 2860–2871.
    CAS Google Scholar
  84. Hammond, E. M., Mandell, D. J., Salim, A., Krieg, A. J., Johnson, T. M., Shirazi, H. A., et al. (2006). Genome-wide analysis of p53 under hypoxic conditions. Molecular and Cellar Biology, 26(9), 3492–3504.
    Article PubMed CAS Google Scholar
  85. Zhang, X., Succi, J., Feng, Z., Prithivirajsingh, S., Story, M. D., Legerski, R. J. (2004). Artemis is a phosphorylation target of ATM and ATR and is involved in the G2/M DNA damage checkpoint response. Molecular and Cellular Biology, 24(20), 9207–9220.
    Article PubMed CAS Google Scholar
  86. Li, S., Ting, N. S., Zheng, L., Chen, P. L., Ziv, Y., Shiloh, Y., et al. (2000). Functional link of BRCA1 and ataxia telangiectasia gene product in DNA damage response. Nature, 406(6792), 210–215.
    Article PubMed CAS Google Scholar
  87. Chehab, N. H., Malikzay, A., Appel, M., & Halazonetics, T. D. (2000). Chk2/hCds1 functions as a DNA damage checkpoint in G(1) by stabilizing p53. Genes Development, 14(3), 278–288.
    PubMed CAS Google Scholar
  88. Matsuoka, S., Rotman, G., Ogawa, A., Shiloh, J., Tamai, K., & Eledge, S. J. (2000). Ataxia telangiectasia-mutated phosphorylates Chk2 in vivo and in vitro. Proceedings of the National Academy of Sciences of the United States of America, 97(19), 10389–10394.
    Article PubMed CAS Google Scholar
  89. Au, W. W., & Henderson, B. R. (2005). The BRCA1 RING and BRCT domains cooperate in targeting BRCA1 to ionizing radiation-induced nuclear foci. Journal of Biological Chemistry, 280(8), 6993–7001.
    Article PubMed CAS Google Scholar
  90. Thomas, J. E., Smith, M., Tonkinson, J. L., Rubinfeld, B., & Polakis, P. (1997). Induction of phosphorylation on BRCA1 during the cell cycle and after DNA damage. Cell Growth Differ, 8(7), 801–809.
    PubMed CAS Google Scholar
  91. Chen, G. C., Guan, L. S., Yu, J. H., Choi Kim, H. R., & Wang, Z. Y. (2001). Rb-associated protein 46 (RbAp46) inhibits transcriptional transactivation mediated by BRCA1. Biochemical and Biophysical Research Communications, 284(2), 507–514.
    Article PubMed CAS Google Scholar
  92. Mullan, P. B., Quinn, J. E., & Harkin, D. P. (2006). The role of BRCA1 in transcriptional regulation and cell cycle control. Oncogene, 25(43), 5854–5863.
    Article PubMed CAS Google Scholar
  93. Gatei, M., Scott, S. P., Filippovitch, I., Soronika, N., Lavin, M. F., Weber, B., et al. (2000). Role for ATM in DNA damage-induced phosphorylation of BRCA1. Cancer Research, 60(12), 3299–3304.
    PubMed CAS Google Scholar
  94. Lee, J. S., Collins, K. M., Brown, A. L., Lee, C. H., & Chung, J. H. (2000). hCds1-mediated phosphorylation of BRCA1 regulates the DNA damage response. Nature, 404(6774), 201–204.
    Article PubMed CAS Google Scholar
  95. Okada, S., & Ouchi, T. (2003). Cell cycle differences in DNA damage-induced BRCA1 phosphorylation affect its subcellular localization. Journal of Biological Chemistry, 278(3), 2015–2020.
    Article PubMed CAS Google Scholar
  96. Venkitaraman, A. R. (2002). Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell, 108(2), 171–182.
    Article PubMed CAS Google Scholar
  97. Kang, H. J., Kim, H. J., Rin, J.-K., Mattson, T. L., Kim, K. W., Cho, C.-H., et al. (2006). BRCA1 plays a role in the hypoxic response by regulating HIF-1alpha stability and by modulating vascular endothelial growth factor expression. Journal of Biological Chemistry, 281(19), 13047–13056.
    Article PubMed CAS Google Scholar
  98. Flygare, J., Benson, F., & Hellgren, D. (1996). Expression of the human RAD51 gene during the cell cycle in primary human peripheral blood lymphocytes. Biochimica et Biophysica acta, 1312(3), 231–236.
    PubMed Google Scholar
  99. Gudas, J. M., Li, T., Nguyen, H., Jensen, D., Rauscher, F. J. 3rd, Cowan, K. H. (1996). Cell cycle regulation of BRCA1 messenger RNA in human breast epithelial cells. Cell Growth Differ, 7(6), 717–723.
    PubMed CAS Google Scholar
  100. Hammond, E. M., Dorie, M. J., & Giaccia, A. J. (2003). ATR/ATM targets are phosphorylated by ATR in response to hypoxia and ATM in response to reoxygenation. Journal of Biological Chemistry, 278(14), 12207–12213.
    Article PubMed CAS Google Scholar

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