Inhibition of PARP1-dependent end-joining contributes to Olaparib-mediated radiosensitization in tumor cells

Molecular Oncology

Volumn 8, Issue 8, 2014, Pages 1616-1625

  Kötter, Annika ^a   Cornils, Kerstin ^a   Borgmann, Kerstin ^a   Dahm Daphi, Jochen ^a   Petersen, Cordula ^a   Dikomey, Ekkehard ^a   Mansour, Wael Y ^a,b  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b CAIRO UNIVERSITY   (Egypt)

Author keywords

DSB repair; Non homologous end joining; Olaparib; PARP1 dependent end joining; Radiosensitivity

Indexed keywords

APHIDICOLIN; DOUBLE STRANDED DNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; OLAPARIB;

A549 CELL LINE; ARTICLE; CANCER CELL LINE; CELL SURVIVAL; CHROMATIN; COLONY FORMATION; CONTROLLED STUDY; DNA END JOINING REPAIR; DNA REPAIR; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; ENZYME INHIBITION; FLOW CYTOMETRY; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IRRADIATION; PROTEIN STRUCTURE; RADIOSENSITIVITY; RADIOSENSITIZATION; WHOLE CELL;

EID: 84911953126     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2014.06.008     Document Type: Article

References (39)

1. Audebert M., Salles B., Calsou P. Involvement of poly(ADP-ribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J.Biol. Chem. 2004, 279:55117-55126.
2. Baldeyron C., Jacquemin E., Smith J., Jacquemont C., De Oliveira I., Gad S., Feunteun J., Stoppa-Lyonnet D., Papadopoulo D. A single mutated BRCA1 allele leads to impaired fidelity of double strand break end-joining. Oncogene 2002, 21:1401-1410.
3. Bentley J., Diggle C.P., Harnden P., Knowles M.A., Kiltie A.E. DNA double strand break repair in human bladder cancer is error prone and involves microhomology-associated end-joining. Nucleic Acids Res. 2004, 32:5249-5259.
4. Berkovich E., Monnat R.J., Kastan M.B. Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nat. Cell Biol. 2007, 9:683-690.
5. Bryant H.E., Helleday T. Poly(ADP-ribose) polymerase inhibitors as potential chemotherapeutic agents. Biochem. Soc. Trans. 2004, 32:959-961.
6. Catz S.D., Johnson J.L. BCL-2 in prostate cancer: a minireview. Apoptosis 2003, 8:29-37.
7. Dungey F.A., Loser D.A., Chalmers A.J. Replication-dependent radiosensitization of human glioma cells by inhibition of poly(ADP-ribose) polymerase: mechanisms and therapeutic potential. Int. J. Radiat. Oncol. Biol. Phys. 2008, 72:1188-1197.
8. 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., Ashworth A. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 2005, 434:917-921.
9. Garber K. PARP inhibitors bounce back. Nat. Rev. Drug Discov. 2013, 12:725-727.
10. Hartwell L.H., Szankasi P., Roberts C.J., Murray A.W., Friend S.H. Integrating genetic approaches into the discovery of anticancer drugs. Science 1997, 278:1064-1068.
11. Helleday T., Lo J., van Gent D.C., Engelward B.P. DNA double-strand break repair: from mechanistic understanding to cancer treatment. DNA Repair (Amst) 2007, 6:923-935.
12. Huhn D., Bolck H.A., Sartori A.A. Targeting DNA double-strand break signalling and repair: recent advances in cancer therapy. Swiss Med. Wkly. 2013, 143:w13837.
13. Iliakis G. Backup pathways of NHEJ in cells of higher eukaryotes: cell cycle dependence. Radiother. Oncol. 2009, 92:310-315.
14. Jia Q., Dulk-Ras A.D., Shen H., Hooykaas P.J., de Pater S. Poly(ADP-ribose)polymerases are involved in microhomology mediated back-up non-homologous end joining in Arabidopsis thaliana. Plant Mol. Biol. 2013, 82:339-351.
15. Kaelin W.G. The concept of synthetic lethality in the context of anticancer therapy. Nat. Rev. Cancer 2005, 5:689-698.
16. Kasten-Pisula U., Menegakis A., Brammer I., Borgmann K., Mansour W.Y., Degenhardt S., Krause M., Schreiber A., Dahm-Daphi J., Petersen C., Dikomey E., Baumann M. The extreme radiosensitivity of the squamous cell carcinoma SKX is due to a defect in double-strand break repair. Radiother. Oncol. 2009, 90:257-264.
17. Kelland L.R., Burgess L., Steel G.G. Differential radiosensitization by the poly(ADP-ribose) transferase inhibitor 3-aminobenzamide in human tumor cells of varying radiosensitivity. Int. J. Radiat. Oncol. Biol. Phys. 1988, 14:1239-1246.
18. Kumar T.S., Kari V., Choudhary B., Nambiar M., Akila T.S., Raghavan S.C. Anti-apoptotic protein BCL2 down-regulates DNA end joining in cancer cells. J.Biol. Chem. 2010, 285:32657-32670.
19. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
20. Li Z., Kustikova O.S., Kamino K., Neumann T., Rhein M., Grassman E., Fehse B., Baum C. Insertional mutagenesis by replication-deficient retroviral vectors encoding the large T oncogene. Ann. N. Y. Acad. Sci. 2007.
21. Lord C.J., Ashworth A. Mechanisms of resistance to therapies targeting BRCA-mutant cancers. Nat. Med. 2013, 19:1381-1388.
22. Loser D.A., Shibata A., Shibata A.K., Woodbine L.J., Jeggo P.A., Chalmers A.J. Sensitization to radiation and alkylating agents by inhibitors of poly(ADP-ribose) polymerase is enhanced in cells deficient in DNA double-strand break repair. Mol. Cancer Ther. 2010, 9:1775-1787.
23. Mansour W.Y., Schumacher S., Rosskopf R., Rhein T., Schmidt-Petersen F., Gatzemeier F., Haag F., Borgmann K., Willers H., Dahm-Daphi J. Hierarchy of nonhomologous end-joining, single-strand annealing and gene conversion at site-directed DNA double-strand breaks. Nucleic Acids Res. 2008, 36:4088-4098.
24. Mansour W.Y., Rhein T., Dahm-Daphi J. The alternative end-joining pathway for repair of DNA double-strand breaks requires PARP1 but is not dependent upon microhomologies. Nucleic Acids Res. 2010, 38:6065-6077.
25. Mansour W.Y., Borgmann K., Petersen C., Dikomey E., Dahm-Daphi J. The absence of Ku but not defects in classical non-homologous end-joining is required to trigger PARP1-dependent end-joining. DNA Repair (Amst) 2013, 12:1134-1142.
26. Muller C., Monferran S., Gamp A.C., Calsou P., Salles B. Inhibition of Ku heterodimer DNA end binding activity during granulocytic differentiation of human promyelocytic cell lines. Oncogene 2001, 20:4373-4382.
27. Nussenzweig A., Nussenzweig M.C. A backup DNA repair pathway moves to the forefront. Cell 2007, 131:223-225.
28. O'Shaughnessy J., Osborne C., Pippen J.E., Yoffe M., Patt D., Rocha C., Koo I.C., Sherman B.M., Bradley C. Iniparib plus chemotherapy in metastatic triple-negative breast cancer. N.Engl. J. Med. 2011, 364:205-214.
29. Ossovskaya V., Koo I.C., Kaldjian E.P., Alvares C., Sherman B.M. Upregulation of poly (ADP-ribose) polymerase-1 (PARP1) in triple-negative breast Cancer and other primary human tumor types. Genes & Cancer 2010, I:10.
30. Powell C., Mikropoulos C., Kaye S.B., Nutting C.M., Bhide S.A., Newbold K., Harrington K.J. Pre-clinical and clinical evaluation of PARP inhibitors as tumour-specific radiosensitisers. Cancer Treat Rev. 2010, 36:566-575.
31. Pucci S., Mazzarelli P., Rabitti C., Giai M., Gallucci M., Flammia G., Alcini A., Altomare V., Fazio V.M. Tumor specific modulation of KU70/80 DNA binding activity in breast and bladder human tumor biopsies. Oncogene 2001, 20:739-747.
32. Rehman F.L., Lord C.J., Ashworth A. Synthetic lethal approaches to breast cancer therapy. Nat. Rev. Clin. Oncol. 2010, 7:718-724.
33. Senra J.M., Telfer B.A., Cherry K.E., McCrudden C.M., Hirst D.G., O'Connor M.J., Wedge S.R., Stratford I.J. Inhibition of PARP-1 by olaparib (AZD2281) increases the radiosensitivity of a lung tumor xenograft. Mol. Cancer Ther. 2011, 10:1949-1958.
34. Shin K.H., Kang M.K., Kim R.H., Kameta A., Baluda M.A., Park N.H. Abnormal DNA end-joining activity in human head and neck cancer. Int. J. Mol. Med. 2006, 17:917-924.
35. Tutt A.N., Lord C.J., McCabe N., Farmer H., Turner N., Martin N.M., Jackson S.P., Smith G.C., Ashworth A. Exploiting the DNA repair defect in BRCA mutant cells in the design of new therapeutic strategies for cancer. Cold Spring Harb. Symp. Quant. Biol. 2005, 70:139-148.
36. Walker J.R., Corpina R.A., Goldberg J. Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair. Nature 2001, 412:607-614.
37. Wang H., Perrault A.R., Takeda Y., Qin W., Iliakis G. Biochemical evidence for Ku-independent backup pathways of NHEJ. Nucleic Acids Res. 2003, 31:5377-5388.
38. Wang M., Wu W., Rosidi B., Zhang L., Wang H., Iliakis G. PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res. 2006, 34:6170-6182.
39. Wang Q., Gao F., May W.S., Zhang Y., Flagg T., Deng X. Bcl2 negatively regulates DNA double-strand-break repair through a nonhomologous end-joining pathway. Mol. Cell 2008, 29:488-498.