Homologous recombination and prostate cancer: A model for novel DNA repair targets and therapies

Radiotherapy and Oncology

Volumn 83, Issue 3, 2007, Pages 220-230

  Bristow, Robert G ^a,b   Ozcelik, Hilmi ^c   Jalali, Farid ^a   Chan, Norman ^a   Vesprini, Danny ^b  

^a Department of Medical Biophysics ^*  (Canada)

^b PRINCESS MARGARET HOSPITAL   (Canada)

^c MOUNT SINAI HOSPITAL   (Canada)

Author keywords

Androgen deprivation; ATM; ATR; Biomarkers; Carcinogenesis; Cell cycle; Chemotherapy; DNA double strand breaks; DNA repair; End joining; Homologous recombination; Hypoxia; Prostate cancer; RAD51; Radiotherapy

Indexed keywords

8 HYDROXY 2 METHYL 4(3H) QUINAZOLINONE; AG 14361; BLEOMYCIN; CAMPTOTHECIN; CISPLATIN; ETOPOSIDE; GEMCITABINE; IMATINIB; KU 0058684; KU 55953; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; NU 7026; PROTEIN SERINE THREONINE KINASE INHIBITOR; SU 11752; UNCLASSIFIED DRUG; VANILLIN;

APOPTOSIS; CANCER RADIOTHERAPY; CANCER RISK; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; HOMOLOGOUS RECOMBINATION; HUMAN; IONIZING RADIATION; MICROENVIRONMENT; PRIORITY JOURNAL; PROGNOSIS; PROSTATE CANCER; RADIOSENSITIZATION; REVIEW;

BIOLOGICAL MARKERS; DNA REPAIR; HUMANS; MALE; PROSTATIC NEOPLASMS; RECOMBINATION, GENETIC; RISK FACTORS; SEQUENCE HOMOLOGY;

EID: 34250343422     PISSN: 01678140     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.radonc.2007.04.016     Document Type: Review

References (86)

1. Al Rashid S.T., Dellaire G., Cuddihy A., et al. Evidence for the direct binding of phosphorylated p53 to sites of DNA breaks in vivo. Cancer Res 65 (2005) 10810-10821
2. Angele S., Falconer A., Foster C.S., Taniere P., Eeles R.A., and Hall J. ATM protein overexpression in prostate tumors: possible role in telomere maintenance. Am J Clin Pathol 121 (2004) 231-236
3. Bartek J., and Lukas J. DNA damage checkpoints: from initiation to recovery or adaptation. Curr Opin Cell Biol 19 (2007) 238-245
4. Bartkova J., Horejsi Z., Koed K., et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434 (2005) 864-870
5. Bindra R.S., Gibson S.L., Meng A., et al. Hypoxia-induced down-regulation of BRCA1 expression by E2Fs. Cancer Res 65 (2005) 11597-11604
6. Bindra R.S., Schaffer P.J., Meng A., et al. Down-regulation of Rad51 and decreased homologous recombination in hypoxic cancer cells. Mol Cell Biol 24 (2004) 8504-8518
7. Boisvert F.M., Hendzel M.J., Masson J.Y., and Richard S. Methylation of MRE11 regulates its nuclear compartmentalization. Cell Cycle 4 (2005) 981-989
8. Bradshaw P.S., Stavropoulos D.J., and Meyn M.S. Human telomeric protein TRF2 associates with genomic double-strand breaks as an early response to DNA damage. Nat Genet 37 (2005) 193-197
9. Bristow R.G., and Hill R. Molecular and cellular radiobiology. In: Tannock I.F.H.R., Harrington L., and Bristow R.G. (Eds). The basic science of oncology. 4th ed. (2005), McGraw-Hill Ltd, New York 261-288 Chapter 14
10. Bristow RG., and Harrington L. Genetic instability and DNA repair. In: Tannock I.F.H.R., Harrington L., and Bristow R.G. (Eds). The basic science of oncology. 4th ed. (2005), McGraw-Hill Ltd, New York 77-99 Chapter 5
11. Bromfield G.P., Meng A., Warde P., and Bristow R.G. Cell death in irradiated prostate epithelial cells: role of apoptotic and clonogenic cell kill. Prostate Cancer Prostatic Dis 6 (2003) 73-85
12. Brown J.M., and Wilson W.R. Exploiting tumour hypoxia in cancer treatment. Nat Rev Cancer 4 (2004) 437-447
13. Brunner T.B., Gupta A.K., Shi Y., et al. Farnesyltransferase inhibitors as radiation sensitizers. Int J Radiat Biol 79 (2003) 569-576
14. Bryant H.E., Schultz N., Thomas H.D., et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434 (2005) 913-917
15. Cairns R.A., and Hill R.P. Acute hypoxia enhances spontaneous lymph node metastasis in an orthotopic murine model of human cervical carcinoma. Cancer Res 64 (2004) 2054-2061
16. Camphausen K., Burgan W., Cerra M., et al. Enhanced radiation-induced cell killing and prolongation of gammaH2AX foci expression by the histone deacetylase inhibitor MS-275. Cancer Res 64 (2004) 316-321
17. Camphausen K., Cerna D., Scott T., et al. Enhancement of in vitro and in vivo tumor cell radiosensitivity by valproic acid. Int J Cancer 114 (2005) 380-386
18. Carnell D.M., Smith R.E., Daley F.M., Saunders M.I., Bentzen S.M., and Hoskin P.J. An immunohistochemical assessment of hypoxia in prostate carcinoma using pimonidazole: implications for radioresistance. Int J Radiat Oncol Biol Phys 65 (2006) 91-99
19. Cesaretti J.A., Stock R.G., Lehrer S., et al. ATM sequence variants are predictive of adverse radiotherapy response among patients treated for prostate cancer. Int J Radiat Oncol Biol Phys 61 (2005) 196-202
20. Chan N, Bristow R, Milosevic M. Tumor hypoxia, DNA repair and prostate cancer progression: new targets and new therapies. Future Oncol 2007; (in press).
21. Chang I.Y., Youn C.K., Kim H.B., et al. Oncogenic H-Ras up-regulates expression of Ku80 to protect cells from gamma-ray irradiation in NIH3T3 cells. Cancer Res 65 (2005) 6811-6819
22. Charlesworth P.J., and Harris A.L. Mechanisms of disease: angiogenesis in urologic malignancies. Nat Clin Pract Urol 3 (2006) 157-169
23. Chen L., Elahi A., Pow-Sang J., Lazarus P., and Park J. Association between polymorphism of human oxoguanine glycosylase 1 and risk of prostate cancer. J Urol 170 (2003) 2471-2474
24. Chinnaiyan P., Vallabhaneni G., Armstrong E., Huang S.M., and Harari P.M. Modulation of radiation response by histone deacetylase inhibition. Int J Radiat Oncol Biol Phys 62 (2005) 223-229
25. Choudhury A, Zhao H, Jalali F, Kiltie A, R B. Targeting RAD 51-dependent homologous recombination using imatinib results in enhancement of effects of chemoradiation. Mol Cancer Therap, 2007 (unpublished).
26. Choudhury A., Cuddihy A., and Bristow R.G. Radiation and new molecular agents part I: targeting ATM-ATR checkpoints, DNA repair, and the proteasome. Semin Radiat Oncol 16 (2006) 51-58
27. Collis S.J., Sangar V.K., Tighe A., et al. Development of a novel rapid assay to assess the fidelity of DNA double-strand-break repair in human tumour cells. Nucleic Acids Res 30 (2002) E1
28. Collis S.J., Swartz M.J., Nelson W.G., and DeWeese T.L. Enhanced radiation and chemotherapy-mediated cell killing of human cancer cells by small inhibitory RNA silencing of DNA repair factors. Cancer Res 63 (2003) 1550-1554
29. Collis S.J., Tighe A., Scott S.D., Roberts S.A., Hendry J.H., and Margison G.P. Ribozyme minigene-mediated RAD51 down-regulation increases radiosensitivity of human prostate cancer cells. Nucleic Acids Res 29 (2001) 1534-1538
30. Cuddihy A.R., and Bristow R.G. The p53 protein family and radiation sensitivity: yes or no?. Cancer Metastasis Rev 23 (2004) 237-257
31. Cybulski C., Gorski B., Debniak T., et al. NBS1 is a prostate cancer susceptibility gene. Cancer Res 64 (2004) 1215-1219
32. Damaraju S., Murray D., Dufour J., et al. Association of DNA repair and steroid metabolism gene polymorphisms with clinical late toxicity in patients treated with conformal radiotherapy for prostate cancer. Clin Cancer Res 12 (2006) 2545-2554
33. Dittmann K., Mayer C., Fehrenbacher B., et al. Radiation-induced epidermal growth factor receptor nuclear import is linked to activation of DNA-dependent protein kinase. J Biol Chem 280 (2005) 31182-31189
34. Dittmann K., Mayer C., and Rodemann H.P. Inhibition of radiation-induced EGFR nuclear import by C225 (Cetuximab) suppresses DNA-PK activity. Radiother Oncol 76 (2005) 157-161
35. Dong J.T. Prevalent mutations in prostate cancer. J Cell Biochem 97 (2006) 433-447
36. El-Awady R.A., Dikomey E., and Dahm-Daphi J. Radiosensitivity of human tumour cells is correlated with the induction but not with the repair of DNA double-strand breaks. Br J Cancer 89 (2003) 593-601
37. Erkko H., Xia B., Nikkila J., et al. A recurrent mutation in PALB2 in Finnish cancer families. Nature 446 (2007) 316-319
38. Fan C., Quan R., Feng X., et al. ATM activation is accompanied with earlier stages of prostate tumorigenesis. Biochim Biophys Acta 1763 (2006) 1090-1097
39. Fan R., Kumaravel T.S., Jalali F., Marrano P., Squire J.A., and Bristow R.G. Defective DNA strand break repair after DNA damage in prostate cancer cells: implications for genetic instability and prostate cancer progression. Cancer Res 64 (2004) 8526-8533
40. Farmer H., McCabe N., Lord C.J., et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434 (2005) 917-921
41. Faulhaber O, Bristow RG. Basis of cell kill following clinical radiotherapy. Chapter in application of apoptosis to cancer treatment (Sluyser, Mels, editors). Dordrecht, NL: Springer Publishing; 2005.
42. Fowler J.F., Nahum A.E., and Orton C.G. Point/counterpoint. The best radiotherapy for the treatment of prostate cancer involves hypofractionation. Med Phys 33 (2006) 3081-3084
43. Green M.M., Hiley C.T., Shanks J.H., et al. Expression of vascular endothelial growth factor (VEGF) in locally invasive prostate cancer is prognostic for radiotherapy outcome. Int J Radiat Oncol Biol Phys 67 (2007) 84-90
44. Hall E.J., Schiff P.B., Hanks G.E., et al. A preliminary report: frequency of A-T heterozygotes among prostate cancer patients with severe late responses to radiation therapy. Cancer J Sci Am 4 (1998) 385-389
45. Harris A.L. Hypoxia - a key regulatory factor in tumour growth. Nat Rev Cancer 2 (2002) 38-47
46. Jain R.K., Duda D.G., Clark J.W., and Loeffler J.S. Lessons from phase III clinical trials on anti-VEGF therapy for cancer. Nat Clin Pract Oncol 3 (2006) 24-40
47. Jeggo P.A., and Lobrich M. Contribution of DNA repair and cell cycle checkpoint arrest to the maintenance of genomic stability. DNA Repair (Amsterdam) 5 (2006) 1192-1198
48. Koritzinsky M., Magagnin M.G., van den Beucken T., et al. Gene expression during acute and prolonged hypoxia is regulated by distinct mechanisms of translational control. EMBO J (2006)
49. Koritzinsky M., Wouters B.G., Amellem O., and Pettersen E.O. Cell cycle progression and radiation survival following prolonged hypoxia and re-oxygenation. Int J Radiat Biol 77 (2001) 319-328
50. Levy-Lahad E., and Friedman E. Cancer risks among BRCA1 and BRCA2 mutation carriers. Br J Cancer 96 (2007) 11-15
51. Ma B.B., Bristow R.G., Kim J., and Siu L.L. Combined-modality treatment of solid tumors using radiotherapy and molecular targeted agents. J Clin Oncol 21 (2003) 2760-2776
52. McBride W.H., Iwamoto K.S., Syljuasen R., Pervan M., and Pajonk F. The role of the ubiquitin/proteasome system in cellular responses to radiation. Oncogene 22 (2003) 5755-5773
53. Meng A.X., Jalali F., Cuddihy A., et al. Hypoxia down-regulates DNA double strand break repair gene expression in prostate cancer cells. Radiother Oncol 76 (2005) 168-176
54. Meng A.X., Jalali F., Cuddihy A., et al. Hypoxia down-regulates DNA double strand break repair gene expression in prostate cancer cells. Radiother Oncol 76 (2005) 168-176
55. Milosevic MRB. Androgen withdrawal in patients reduces prostate cancer hypoxia: implications for disease progression and radiation response. Cancer Res 2007; (in press).
56. 2 ratio predicts for biochemical failure in patients with prostate cancer: preliminary findings. Urology 60 (2002) 634-639
57. Munshi A., Kurland J.F., Nishikawa T., et al. Histone deacetylase inhibitors radiosensitize human melanoma cells by suppressing DNA repair activity. Clin Cancer Res 11 (2005) 4912-4922
58. Nahum A.E., Movsas B., Horwitz E.M., Stobbe C.C., and Chapman J.D. Incorporating clinical measurements of hypoxia into tumor local control modeling of prostate cancer: implications for the alpha/beta ratio. Int J Radiat Oncol Biol Phys 57 (2003) 391-401
59. Nichol A.M., Warde P., and Bristow R.G. Optimal treatment of intermediate-risk prostate carcinoma with radiotherapy: clinical and translational issues. Cancer 104 (2005) 891-905
60. Norris A.M., Woodruff R.D., D'Agostino Jr. R.B., Clodfelter J.E., and Scarpinato K.D. Elevated levels of the mismatch repair protein PMS2 are associated with prostate cancer. Prostate 67 (2007) 214-225
61. Parker C., Milosevic M., Toi A., et al. Polarographic electrode study of tumor oxygenation in clinically localized prostate cancer. Int J Radiat Oncol Biol Phys 58 (2004) 750-757
62. Peng Y., Woods R.G., Beamish H., et al. Deficiency in the catalytic subunit of DNA-dependent protein kinase causes down-regulation of ATM. Cancer Res 65 (2005) 1670-1677
63. Prtilo A., Leach F.S., Markwalder R., et al. Tissue microarray analysis of hMSH2 expression predicts outcome in men with prostate cancer. J Urol 174 (2005) 1814-1818 discussion p. 18.
64. Qvarnstrom O.F., Simonsson M., Johansson K.A., Nyman J., and Turesson I. DNA double strand break quantification in skin biopsies. Radiother Oncol 72 (2004) 311-317
65. 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
66. Rochester M.A., Riedemann J., Hellawell G.O., Brewster S.F., and Macaulay V.M. Silencing of the IGF1R gene enhances sensitivity to DNA-damaging agents in both PTEN wild-type and mutant human prostate cancer. Cancer Gene Ther 12 (2005) 90-100
67. Russell J.S., Brady K., Burgan W.E., et al. Gleevec-mediated inhibition of Rad51 expression and enhancement of tumor cell radiosensitivity. Cancer Res 63 (2003) 7377-7383
68. Rybicki B.A., Conti D.V., Moreira A., Cicek M., Casey G., and Witte J.S. DNA repair gene XRCC1 and XPD polymorphisms and risk of prostate cancer. Cancer Epidemiol Biomark Prev 13 (2004) 23-29
69. Serafin A.M., Akudugu J.M., and Bohm L. Studies on the influence of DNA repair on radiosensitivity in prostate cell lines. Urol Res 31 (2003) 227-231
70. Shen W.H., Balajee A.S., Wang J., et al. Essential role for nuclear PTEN in maintaining chromosomal integrity. Cell 128 (2007) 157-170
71. Slupianek A., Schmutte C., Tombline G., et al. BCR/ABL regulates mammalian RecA homologs, resulting in drug resistance. Mol Cell 8 (2001) 795-806
72. Soldatenkov V.A., and Potaman V.N. DNA-binding properties of poly(ADP-ribose) polymerase: a target for anticancer therapy. Curr Drug Targets 5 (2004) 357-365
73. Sprong D., Janssen H.L., Vens C., and Begg A.C. Resistance of hypoxic cells to ionizing radiation is influenced by homologous recombination status. Int J Radiat Oncol Biol Phys 64 (2006) 562-572
74. Stucki M., and Jackson S.P. gammaH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair (Amsterdam) 5 (2006) 534-543
75. Sun X., Chen C., Vessella R.L., and Dong J.T. Microsatellite instability and mismatch repair target gene mutations in cell lines and xenografts of prostate cancer. Prostate 66 (2006) 660-666
76. Syljuasen R.G., Sorensen C.S., Hansen L.T., et al. Inhibition of human Chk1 causes increased initiation of DNA replication, phosphorylation of ATR targets, and DNA breakage. Mol Cell Biol 25 (2005) 3553-3562
77. Teicher B.A., Ara G., Herbst R., Palombella V.J., and Adams J. The proteasome inhibitor PS-341 in cancer therapy. Clin Cancer Res 5 (1999) 2638-2645
78. Trotman L.C., Niki M., Dotan Z.A., et al. Pten dose dictates cancer progression in the prostate. PLoS Biol 1 (2003) E59
79. Trzeciak A.R., Nyaga S.G., Jaruga P., Lohani A., Dizdaroglu M., and Evans M.K. Cellular repair of oxidatively induced DNA base lesions is defective in prostate cancer cell lines, PC-3 and DU-145. Carcinogenesis 25 (2004) 1359-1370
80. Woodward W.A., Wachsberger P., Burd R., and Dicker A.P. Effects of androgen suppression and radiation on prostate cancer suggest a role for angiogenesis blockade. Prostate Cancer Prostatic Dis 8 (2005) 127-132
81. Wyman C., Ristic D., and Kanaar R. Homologous recombination-mediated double-strand break repair. DNA Repair (Amsterdam) 3 (2004) 827-833
82. Xu J., Zheng S.L., Turner A., et al. Associations between hOGG1 sequence variants and prostate cancer susceptibility. Cancer Res 62 (2002) 2253-2257
83. Yeh C.C., Lee C., and Dahiya R. DNA mismatch repair enzyme activity and gene expression in prostate cancer. Biochem Biophys Res Commun 285 (2001) 409-413
84. Zolzer F., and Streffer C. Increased radiosensitivity with chronic hypoxia in four human tumor cell lines. Int J Radiat Oncol Biol Phys 54 (2002) 910-920
85. Horsburgh S., Matthew A., Bristow R.G., and Trachtenberg J. Male BRCA1 and BRCA2 mutation carriers: a pilot study investigating medical characteristics of patients participating in a prostate cancer prevention clinic. Prostate 65 (2005) 124-129
86. McCabe N., Turner N.C., Lord C.J., Kluzek K., Bialkowska A., Swift S., Giavora S., O'Connor M.J., Tutt A.N., Zdzienicka M.Z., Smith G.C., and Ashworth A. Deficiency in the repair of DNA damage by homologous recombination and sensitivity to poly (ADP-ribose) polymerase inhibition. Cancer Res 66 (2006) 8109-8115