New molecular targets in radiotherapy: DNA damage signalling and repair in targeted and non-targeted cells

European Journal of Pharmacology

Volumn 625, Issue 1-3, 2009, Pages 151-155

  Burdak Rothkamm, Susanne ^a,b   Prise, Kevin M ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b STOKE MANDEVILLE HOSPITAL   (United Kingdom)

Author keywords

Bystander effects; DNA damage; DNA repair; Radiotherapy

Indexed keywords

2 MORPHOLINO 6 (1 THIANTHRENYL) 4 PYRANONE; 7 HYDROXYSTAUROSPORINE; 8 FLUORO 3,4 DIHYDRO 2 [4 (METHYLAMINOMETHYL)PHENYL]PYRROLO[3,4,5 E,F][2]BENZAZEPIN 6(5H) ONE; AG 14361; AG 14447; ATM PROTEIN; ATR PROTEIN; AZD 7762; BRCA1 PROTEIN; BRCA2 PROTEIN; CEP 3891; CEP 6800; CHECKPOINT KINASE 1; CP 466722; ISOGRANULATIMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; NU 7441; OLAPARIB; PF 00477736; PROTEIN SERINE THREONINE KINASE INHIBITOR; TANESPIMYCIN; UNCLASSIFIED DRUG; XL 884;

BREAST CANCER; BYSTANDER EFFECT; CANCER CELL DESTRUCTION; CANCER RADIOTHERAPY; CELL CYCLE ARREST; CHROMOSOME DAMAGE; CLINICAL TRIAL; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; GENE MUTATION; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; IONIZING RADIATION; OVARY CANCER; PRIORITY JOURNAL; REVIEW;

ANTINEOPLASTIC AGENTS; BYSTANDER EFFECT; CELL CYCLE; COMBINED MODALITY THERAPY; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; HUMANS; NEOPLASMS; RADIATION, IONIZING; SIGNAL TRANSDUCTION;

EID: 71749091838     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2009.09.068     Document Type: Review

References (66)

1. Albert J.M., Cao C., Kim K.W., Willey C.D., Geng L., Xiao D., Wang H., Sandler A., Johnson D.H., Colevas A.D., Low J., Rothenberg M.L., and Lu B. Inhibition of poly(ADP-ribose) polymerase enhances cell death and improves tumor growth delay in irradiated lung cancer models. Clin. Cancer Res. 13 (2007) 3033-3042
2. Azzam E.I., De Toledo S.M., Spitz D.R., and Little J.B. Oxidative metabolism modulates signal transduction and micronucleus formation in bystander cells from alpha-particle-irradiated normal human fibroblast cultures. Cancer Res. 62 (2002) 5436-5442
3. Balajee A.S., Ponnaiya B., Baskar R., and Geard C.R. Induction of replication protein a in bystander cells. Radiat. Res. 162 (2004) 677-686
4. Blasina A., Hallin J., Chen E., Arango M.E., Kraynov E., Register J., Grant S., Ninkovic S., Chen P., Nichols T., O'Connor P., and Anderes K. Breaching the DNA damage checkpoint via PF-00477736, a novel small-molecule inhibitor of checkpoint kinase 1. Mol. Cancer Ther. 7 (2008) 2394-2404
5. Bryant H.E., and Helleday T. Inhibition of poly (ADP-ribose) polymerase activates ATM which is required for subsequent homologous recombination repair. Nucleic Acids Res. 34 (2006) 1685-1691
6. Burdak-Rothkamm S., Short S.C., Folkard M., Rothkamm K., and Prise K.M. ATR-dependent radiation-induced gammaH2AX foci in bystander primary human astrocytes and glioma cells. Oncogene 26 (2007) 993-1002
7. Burdak-Rothkamm S., Rothkamm K., and Prise K.M. ATM acts downstream of ATR in the DNA damage response signaling of bystander cells. Cancer Res. 68 (2008) 7059-7065
8. Calabrese C.R., Almassy R., Barton S., Batey M.A., Calvert A.H., Canan-Koch S., Durkacz B.W., Hostomsky Z., Kumpf R.A., Kyle S., Li J., Maegley K., Newell D.R., Notarianni E., Stratford I.J., Skalitzky D., Thomas H.D., Wang L.Z., Webber S.E., Williams K.J., and Curtin N.J. Anticancer chemosensitization and radiosensitization by the novel poly(ADP-ribose) polymerase-1 inhibitor AG14361. J. Natl. Cancer Inst. 96 (2004) 56-67
9. 2+ signaling. Am. J. Physiol., Cell Physiol. 291 (2006) C1082-C1088
10. Chen S., Zhao Y., Han W., Zhao G., Zhu L., Wang J., Bao L., Jiang E., Xu A., Hei T.K., Yu Z., and Wu L. Mitochondria-dependent signalling pathway are involved in the early process of radiation-induced bystander effects. Br. J. Cancer 98 (2008) 1839-1844
11. Cowell I.G., Durkacz B.W., and Tilby M.J. Sensitization of breast carcinoma cells to ionizing radiation by small molecule inhibitors of DNA-dependent protein kinase and ataxia telangiectsia mutated. Biochem. Pharmacol. 71 (2005) 13-20
12. Curtin N.J., Wang L.Z., Yiakouvaki A., Kyle S., Arris C.A., Canan-Koch S., Webber S.E., Durkacz B.W., Calvert H.A., Hostomsky Z., and Newell D.R. Novel poly(ADP-ribose) polymerase-1 inhibitor, AG14361, restores sensitivity to temozolomide in mismatch repair-deficient cells. Clin. Cancer Res. 10 (2004) 881-889
13. Drew Y., and Calvert H. The potential of PARP inhibitors in genetic breast and ovarian cancers. Ann. N.Y. Acad. Sci. 1138 (2008) 136-145
14. Farmer H., McCabe N., Lord C.J., Tutt A.N., Johnson D.A., Richardson T.B., Santarosa M., Dillon K.J., Hickson I., Knights C., Martin N.M., Jackson S.P., Smith G.C., and Ashworth A. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434 (2005) 917-921
15. Fong P.C., Boss D.S., Yap T.A., Tutt A., Wu P., Mergui-Roelvink M., Mortimer P., Swaisland H., Lau A., O'Connor M.J., Ashworth A., Carmichael J., Kaye S.B., Schellens J.H., and de Bono J.S. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N. Engl. J. Med. 361 (2009) 123-134
16. Goodhead D.T. Initial events in the cellular effects of ionizing radiations: clustered damage in DNA. Int. J. Radiat. Biol. 65 (1994) 7-17
17. Helleday T., Bryant H.E., and Schultz N. Poly(ADP-ribose) polymerase (PARP-1) in homologous recombination and as a target for cancer therapy. Cell Cycle 4 (2005) 1176-1178
18. 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. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res. 64 (2004) 9152-9159
19. Hollick J.J., Rigoreau L.J., Cano-Soumillac C., Cockcroft X., Curtin N.J., Frigerio M., Golding B.T., Guiard S., Hardcastle I.R., Hickson I., Hummersone M.G., Menear K.A., Martin N.M., Matthews I., Newell D.R., Ord R., Richardson C.J., Smith G.C., and Griffin R.J. Pyranone, thiopyranone, and pyridone inhibitors of phosphatidylinositol 3-kinase related kinases. Structure-activity relationships for DNA-dependent protein kinase inhibition, and identification of the first potent and selective inhibitor of the ataxia telangiectasia mutated kinase. J. Med. Chem. 50 (2007) 1958-1972
20. Hotte S.J., Oza A., Winquist E.W., Moore M., Chen E.X., Brown S., Pond G.R., Dancey J.E., and Hirte H.W. Phase I trial of UCN-01 in combination with topotecan in patients with advanced solid cancers: a Princess Margaret Hospital Phase II Consortium Study. Ann. Oncol. 17 (2006) 334-340
21. Hu B., Wu L., Han W., Zhang L., Chen S., Xu A., Hei T.K., and Yu Z. The time and spatial effects of bystander response in mammalian cells induced by low dose radiation. Carcinogenesis 27 (2006) 245-251
22. Jiang X., Zhao B., Britton R., Lim L.Y., Leong D., Sanghera J.S., Zhou B.B., Piers E., Andersen R.J., and Roberge M. Inhibition of Chk1 by the G2 DNA damage checkpoint inhibitor isogranulatimide. Mol. Cancer Ther. 3 (2004) 1221-1227
23. Jones C., and Plummer E.R. PARP inhibitors and cancer therapy - early results and potential applications. Br. J. Radiol. 81 1 (2008) S2-S5
24. Kashino G., Prise K.M., Schettino G., Folkard M., Vojnovic B., Michael B.D., Suzuki K., Kodama S., and Watanabe M. Evidence for induction of DNA double strand breaks in the bystander response to targeted soft X-rays in CHO cells. Mutat. Res. 556 (2004) 209-215
25. Kashino G., Suzuki K., Matsuda N., Kodama S., Ono K., Watanabe M., and Prise K.M. Radiation induced bystander signals are independent of DNA damage and DNA repair capacity of the irradiated cells. Mutat. Res. 619 (2007) 134-138
26. Koturbash I., Rugo R.E., Hendricks C.A., Loree J., Thibault B., Kutanzi K., Pogribny I., Yanch J.C., Engelward B.P., and Kovalchuk O. Irradiation induces DNA damage and modulates epigenetic effectors in distant bystander tissue in vivo. Oncogene 25 (2006) 4267-4275
27. Koturbash I., Boyko A., Rodriguez-Juarez R., McDonald R.J., Tryndyak V.P., Kovalchuk I., Pogribny I.P., and Kovalchuk O. Role of epigenetic effectors in maintenance of the long-term persistent bystander effect in spleen in vivo. Carcinogenesis 28 (2007) 1831-1838
28. Lara Jr. P.N., Mack P.C., Synold T., Frankel P., Longmate J., Gumerlock P.H., Doroshow J.H., and Gandara D.R. The cyclin-dependent kinase inhibitor UCN-01 plus cisplatin in advanced solid tumors: a California cancer consortium phase I pharmacokinetic and molecular correlative trial. Clin. Cancer Res. 11 (2005) 4444-4450
29. Lobrich M., and Jeggo P.A. The impact of a negligent G2/M checkpoint on genomic instability and cancer induction. Nat. Rev. Cancer 7 (2007) 861-869
30. Lord C.J., and Ashworth A. Targeted therapy for cancer using PARP inhibitors. Curr. Opin. Pharmacol. 8 (2008) 363-369
31. Mack P.C., Jones A.A., Gustafsson M.H., Gandara D.R., Gumerlock P.H., and Goldberg Z. Enhancement of radiation cytotoxicity by UCN-01 in non-small cell lung carcinoma cells. Radiat. Res. 162 (2004) 623-634
32. McCabe N., Turner N.C., Lord C.J., Kluzek K., Bialkowska A., Swift S., Giavara 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
33. Miknyoczki S.J., Jones-Bolin S., Pritchard S., Hunter K., Zhao H., Wan W., Ator M., Bihovsky R., Hudkins R., Chatterjee S., Klein-Szanto A., Dionne C., and Ruggeri B. Chemopotentiation of temozolomide, irinotecan, and cisplatin activity by CEP-6800, a poly(ADP-ribose) polymerase inhibitor. Mol. Cancer Ther. 2 (2003) 371-382
34. Morgan W.F. Is there a common mechanism underlying genomic instability, bystander effects and other nontargeted effects of exposure to ionizing radiation?. Oncogene 22 (2003) 7094-7099
35. Mothersill C., and Seymour C. Radiation-induced bystander effects, carcinogenesis and models. Oncogene 22 (2003) 7028-7033
36. Nagasawa H., and Little J.B. Bystander effect for chromosomal aberrations induced in wild-type and repair deficient CHO cells by low fluences of alpha particles. Mutat. Res. 508 (2002) 121-129
37. Nagasawa H., Cremesti A., Kolesnick R., Fuks Z., and Little J.B. Involvement of membrane signaling in the bystander effect in irradiated cells. Cancer Res. 62 (2002) 2531-2534
38. Nagasawa H., Huo L., and Little J.B. Increased bystander mutagenic effect in DNA double-strand break repair-deficient mammalian cells. Int. J. Radiat. Biol. 79 (2003) 35-41
39. Nagasawa H., Peng Y., Wilson P.F., Lio Y.C., Chen D.J., Bedford J.S., and Little J.B. Role of homologous recombination in the alpha-particle-induced bystander effect for sister chromatid exchanges and chromosomal aberrations. Radiat. Res. 164 (2005) 141-147
40. Nagasawa H., Wilson P.F., Chen D.J., Thompson L.H., Bedford J.S., and Little J.B. Low doses of alpha particles do not induce sister chromatid exchanges in bystander Chinese hamster cells defective in homologous recombination. DNA Repair (Amst) 7 (2008) 515-522
41. Noel G., Godon C., Fernet M., Giocanti N., Megnin-Chanet F., and Favaudon V. Radiosensitization by the poly(ADP-ribose) polymerase inhibitor 4-amino-1, 8-naphthalimide is specific of the S phase of the cell cycle and involves arrest of DNA synthesis. Mol. Cancer Ther. 5 (2006) 564-574
42. Nutley B.P., Smith N.F., Hayes A., Kelland L.R., Brunton L., Golding B.T., Smith G.C., Martin N.M., Workman P., and Raynaud F.I. Preclinical pharmacokinetics and metabolism of a novel prototype DNA-PK inhibitor NU7026. Br. J. Cancer 93 (2005) 1011-1018
43. Plummer E.R. Inhibition of poly(ADP-ribose) polymerase in cancer. Curr. Opin. Pharmacol. 6 (2006) 364-368
44. Plummer R., Jones C., Middleton M., Wilson R., Evans J., Olsen A., Curtin N., Boddy A., McHugh P., Newell D., Harris A., Johnson P., Steinfeldt H., Dewji R., Wang D., Robson L., and Calvert H. Phase I study of the poly(ADP-ribose) polymerase inhibitor, AG014699, in combination with temozolomide in patients with advanced solid tumors. Clin. Cancer Res. 14 (2008) 7917-7923
45. Prise K.M., and O'Sullivan J.M. Radiation-induced bystander signalling in cancer therapy. Nat. Rev. Cancer 9 (2009) 351-360
46. Prise K.M., Belyakov O.V., Folkard M., and Michael B.D. Studies of bystander effects in human fibroblasts using a charged particle microbeam. Int. J. Radiat. Biol. 74 (1998) 793-798
47. Rainey M.D., Charlton M.E., Stanton R.V., and Kastan M.B. Transient inhibition of ATM kinase is sufficient to enhance cellular sensitivity to ionizing radiation. Cancer Res. 68 (2008) 7466-7474
48. Ree A.H., Bratland A., Nome R.V., Stokke T., Fodstad O., and Andersson Y. Inhibitory targeting of checkpoint kinase signaling overrides radiation-induced cell cycle gene regulation: a therapeutic strategy in tumor cell radiosensitization?. Radiother. Oncol. 72 (2004) 305-310
49. Sarkaria J.N., and Eshleman J.S. ATM as a target for novel radiosensitizers. Semin. Radiat. Oncol. 11 (2001) 316-327
50. Shao C., Folkard M., Michael B.D., and Prise K.M. Bystander signaling between glioma cells and fibroblasts targeted with counted particles. Int. J. Cancer 116 (2005) 45-51
51. Shao C., Lyng F.M., Folkard M., and Prise K.M. Calcium fluxes modulate the radiation-induced bystander responses in targeted glioma and fibroblast cells. Radiat. Res. 166 (2006) 479-487
52. Shao C., Folkard M., and Prise K.M. Role of TGF-beta1 and nitric oxide in the bystander response of irradiated glioma cells. Oncogene 27 (2008) 434-440
53. Shareef M.M., Cui N., Burikhanov R., Gupta S., Satishkumar S., Shajahan S., Mohiuddin M., Rangnekar V.M., and Ahmed M.M. Role of tumor necrosis factor-alpha and TRAIL in high-dose radiation-induced bystander signaling in lung adenocarcinoma. Cancer Res. 67 (2007) 11811-11820
54. Smilenov L.B., Hall E.J., Bonner W.M., and Sedelnikova O.A. A microbeam study of DNA double-strand breaks in bystander primary human fibroblasts. Radiat. Prot. Dosim. 122 (2006) 256-259
55. Sokolov M.V., Smilenov L.B., Hall E.J., Panyutin I.G., Bonner W.M., and Sedelnikova O.A. Ionizing radiation induces DNA double-strand breaks in bystander primary human fibroblasts. Oncogene 24 (2005) 7257-7265
56. Syljuasen R.G., Sorensen C.S., Nylandsted J., Lukas C., Lukas J., and Bartek J. Inhibition of Chk1 by CEP-3891 accelerates mitotic nuclear fragmentation in response to ionizing radiation. Cancer Res. 64 (2004) 9035-9040
57. Tartier L., Gilchrist S., Burdak-Rothkamm S., Folkard M., and Prise K.M. Cytoplasmic irradiation induces mitochondrial-dependent 53BP1 protein relocalization in irradiated and bystander cells. Cancer Res. 67 (2007) 5872-5879
58. Thomas H.D., Calabrese C.R., Batey M.A., Canan S., Hostomsky Z., Kyle S., Maegley K.A., Newell D.R., Skalitzky D., Wang L.Z., Webber S.E., and Curtin N.J. Preclinical selection of a novel poly(ADP-ribose) polymerase inhibitor for clinical trial. Mol. Cancer Ther. 6 (2007) 945-956
59. Tse A.N., Carvajal R., and Schwartz G.K. Targeting checkpoint kinase 1 in cancer therapeutics. Clin. Cancer Res. 13 (2007) 1955-1960
60. Veuger S.J., Curtin N.J., Richardson C.J., Smith G.C., and Durkacz B.W. Radiosensitization and DNA repair inhibition by the combined use of novel inhibitors of DNA-dependent protein kinase and poly(ADP-ribose) polymerase-1. Cancer Res. 63 (2003) 6008-6015
61. Veuger S.J., Curtin N.J., Smith G.C., and Durkacz B.W. Effects of novel inhibitors of poly(ADP-ribose) polymerase-1 and the DNA-dependent protein kinase on enzyme activities and DNA repair. Oncogene 23 (2004) 7322-7329
62. Welch S., Hirte H.W., Carey M.S., Hotte S.J., Tsao M.S., Brown S., Pond G.R., Dancey J.E., and Oza A.M. UCN-01 in combination with topotecan in patients with advanced recurrent ovarian cancer: a study of the Princess Margaret Hospital Phase II Consortium. Gynecol. Oncol. 106 (2007) 305-310
63. Willmore E., de Caux S., Sunter N.J., Tilby M.J., Jackson G.H., Austin C.A., and Durkacz B.W. A novel DNA-dependent protein kinase inhibitor, NU7026, potentiates the cytotoxicity of topoisomerase II poisons used in the treatment of leukemia. Blood 103 (2004) 4659-4665
64. Zabludoff S.D., Deng C., Grondine M.R., Sheehy A.M., Ashwell S., Caleb B.L., Green S., Haye H.R., Horn C.L., Janetka J.W., Liu D., Mouchet E., Ready S., Rosenthal J.L., Queva C., Schwartz G.K., Taylor K.J., Tse A.N., Walker G.E., and White A.M. AZD7762, a novel checkpoint kinase inhibitor, drives checkpoint abrogation and potentiates DNA-targeted therapies. Mol. Cancer Ther. 7 (2008) 2955-2966
65. Zhang Y., Zhou J., Held K.D., Redmond R.W., Prise K.M., and Liber H.L. Deficiencies of double-strand break repair factors and effects on mutagenesis in directly gamma-irradiated and medium-mediated bystander human lymphoblastoid cells. Radiat. Res. 169 (2008) 197-206
66. Zhao Y., Thomas H.D., Batey M.A., Cowell I.G., Richardson C.J., Griffin R.J., Calvert A.H., Newell D.R., Smith G.C., and Curtin N.J. Preclinical evaluation of a potent novel DNA-dependent protein kinase inhibitor NU7441. Cancer Res. 66 (2006) 5354-5362