International Journal of Radiation Oncology * Biology * Physics
Volume 72, Issue 4 , Pages 1188-1197 , 15 November 2008

Replication-Dependent Radiosensitization of Human Glioma Cells by Inhibition of Poly(ADP-Ribose) Polymerase: Mechanisms and Therapeutic Potential

  • Fiona A. Dungey, B.Sc.

      Affiliations

    • Genome Damage and Stability Centre, University of Sussex, Brighton, United Kingdom
  • ,
  • Dana A. Löser, M.Sc.

      Affiliations

    • Genome Damage and Stability Centre, University of Sussex, Brighton, United Kingdom
  • ,
  • Anthony J. Chalmers, F.R.C.R., Ph.D.

      Affiliations

    • Genome Damage and Stability Centre, University of Sussex, Brighton, United Kingdom
    • Brighton and Sussex Medical School, University of Sussex, Brighton, United Kingdom
    • Corresponding Author InformationReprint requests to: Anthony J. Chalmers, F.R.C.R., Ph.D., Brighton and Sussex Medical School, Genome Damage and Stability Centre, University of Sussex, Brighton BN1 9PX United Kingdom. Tel: (+44) 127-387-6637; Fax: (+44) 127-367-8121

Received 10 June 2008 ,Revised 23 July 2008 ,Accepted 24 July 2008.

References 

  1. Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352:987–996
  2. Keime-Guibert F, Chinot O, Taillandier L, et al. Radiotherapy for glioblastoma in the elderly. N Engl J Med. 2007;356:1527–1535
  3. Corn BW, Yousem DM, Scott CB, et al. White matter changes are correlated significantly with radiation dose: Observations from a randomized dose-escalation trial for malignant glioma (Radiation Therapy Oncology Group 83-02). Cancer. 1994;74:2828–2835
  4. Groves MD, Maor MH, Meyers C, et al. A phase II trial of high-dose bromodeoxyuridine with accelerated fractionation radiotherapy followed by procarbazine, lomustine, and vincristine for glioblastoma multiforme. Int J Radiat Oncol Biol Phys. 1999;45:127–135
  5. Goodhead DT. Initial events in the cellular effects of ionizing radiations: Clustered damage in DNA. Int J Radiat Biol. 1994;65:7–17
  6. Saleh-Gohari N, Bryant HE, Schultz N, et al. Spontaneous homologous recombination is induced by collapsed replication forks that are caused by endogenous DNA single-strand breaks. Mol Cell Biol. 2005;25:7158–7169
  7. Caldecott KW. Protein–protein interactions during mammalian DNA single-strand break repair. Biochem Soc Trans. 2003;31:247–251
  8. Dantzer F, de La Rubia G, Menissier-De Murcia J, et al. Base excision repair is impaired in mammalian cells lacking poly(ADP-ribose) polymerase-1. Biochemistry. 2000;39:7559–7569
  9. Chalmers AJ. Poly(ADP-ribose) polymerase-1 and ionizing radiation: Sensor, signaller and therapeutic target. Clin Oncol (R Coll Radiol). 2004;16:29–39
  10. Shall S, de Murcia G. Poly(ADP-ribose) polymerase-1: What have we learned from the deficient mouse model?. Mutat Res. 2000;460:1–15
  11. Susse S, Scholz CJ, Burkle A, et al. Poly(ADP-ribose) polymerase (PARP-1) and p53 independently function in regulating double-strand break repair in primate cells. Nucleic Acids Res. 2004;32:669–680
  12. Woon EC, Threadgill MD. Poly(ADP-ribose)polymerase inhibition—Where now?. Curr Med Chem. 2005;12:2373–2392
  13. Bryant HE, Schultz N, Thomas HD, et al. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature. 2005;434:913–917
  14. Farmer H, McCabe N, Lord CJ, et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature. 2005;434:917–921
  15. Weinfeld M, Chaudhry MA, D'Amours D, et al. Interaction of DNA-dependent protein kinase and poly(ADP-ribose) polymerase with radiation-induced DNA strand breaks. Radiat Res. 1997;148:22–28
  16. Li B, Navarro S, Kasahara N, et al. Identification and biochemical characterization of a Werner syndrome protein complex with Ku70/80 and PARP-1. J Biol Chem. 2004;279:13659–13667
  17. Ruscetti T, Lehnert BE, Halbrook J, et al. Stimulation of the DNA-dependent protein kinase by poly(ADP-ribose) polymerase. J Biol Chem. 1998;273:14461–14467
  18. Veuger SJ, Curtin NJ, Richardson CJ, et al. 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. 2003;63:6008–6015
  19. Veuger SJ, Curtin NJ, Smith GC, et al. Effects of novel inhibitors of poly(ADP-ribose) polymerase-1 and the DNA-dependent protein kinase on enzyme activities and DNA repair. Oncogene. 2004;23:7322–7329
  20. Yang YG, Cortes U, Patnaik S, et al. Ablation of PARP-1 does not interfere with the repair of DNA double-strand breaks, but compromises the reactivation of stalled replication forks. Oncogene. 2004;23:3872–3882
  21. Noel G, Giocanti N, Fernet M, et al. Poly(ADP-ribose) polymerase (PARP-1) is not involved in DNA double-strand break recovery. BMC Cell Biol. 2003;4:7
  22. Chalmers A, Johnston P, Woodcock M, et al. PARP-1, PARP-2, and the cellular response to low doses of ionizing radiation. Int J Radiat Oncol Biol Phys. 2004;58:410–419
  23. McCulloch EA, Till JE. The sensitivity of cells from normal mouse bone marrow to gamma radiation in vitro and in vivo. Radiat Res. 1962;16:822–832
  24. Breslin C, Clements PM, El-Khamisy SF, et al. Measurement of chromosomal DNA single-strand breaks and replication fork progression rates. Methods Enzymol. 2006;409:410–425
  25. Rogakou EP, Pilch DR, Orr AH, et al. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem. 1998;273:5858–5868
  26. Kao GD, McKenna WG, Yen TJ. Detection of repair activity during the DNA damage-induced G2 delay in human cancer cells. Oncogene. 2001;20:3486–3496
  27. Helleday T. Pathways for mitotic homologous recombination in mammalian cells. Mutat Res. 2003;532:103–115
  28. Hochegger H, Dejsuphong D, Fukushima T, et al. Parp-1 protects homologous recombination from interference by Ku and Ligase IV in vertebrate cells. EMBO J. 2006;25:1305–1314
  29. Yap TA, Boss DS, Fong PC, et al. First in human phase I pharmacokinetic (PK) and pharmacodynamic (PD) study of KU-0059436 (Ku), a small molecule inhibitor of poly ADP-ribose polymerase (PARP) in cancer patients (p), including BRCA1/2 mutation carriers. Presented at ASCO Annual Meeting, Chicago. J Clin Oncol. 2007;25(Suppl.):3529
  30. Cao Y, Tsien CI, Shen Z, et al. Use of magnetic resonance imaging to assess blood-brain/blood-glioma barrier opening during conformal radiotherapy. J Clin Oncol. 2005;23:4127–4136
  31. Cheng CL, Johnson SP, Keir ST, et al. Poly(ADP-ribose) polymerase-1 inhibition reverses temozolomide resistance in a DNA mismatch repair-deficient malignant glioma xenograft. Mol Cancer Ther. 2005;4:1364–1368
  32. Miknyoczki S, Chang H, Grobelny J, et al. The selective poly(ADP-ribose) polymerase-1(2) inhibitor, CEP-8983, increases the sensitivity of chemoresistant tumor cells to temozolomide and irinotecan but does not potentiate myelotoxicity. Mol Cancer Ther. 2007;6:2290–2302
  33. Noel G, Godon C, Fernet M, et al. 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. 2006;5:564–574
  34. Schlicker A, Peschke P, Burkle A, et al. 4-Amino-1,8-naphthalimide: A novel inhibitor of poly(ADP-ribose) polymerase and radiation sensitizer. Int J Radiat Biol. 1999;75:91–100
  35. Brock WA, Milas L, Bergh S, et al. Radiosensitization of human and rodent cell lines by INO-1001, a novel inhibitor of poly(ADP-ribose) polymerase. Cancer Lett. 2004;205:155–160
  36. Calabrese CR, Almassy R, Barton S, et al. Anticancer chemosensitization and radiosensitization by the novel poly(ADP-ribose) polymerase-1 inhibitor AG14361. J Natl Cancer Inst. 2004;96:56–67
  37. Donawho CK, Luo Y, Penning TD, et al. ABT-888, an orally active poly(ADP-ribose) polymerase inhibitor that potentiates DNA-damaging agents in preclinical tumor models. Clin Cancer Res. 2007;13:2728–2737
  38. Wang M, Wu W, Rosidi B, et al. PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res. 2006;34:6170–6182
  39. Schultz N, Lopez E, Saleh-Gohari N, et al. Poly(ADP-ribose) polymerase (PARP-1) has a controlling role in homologous recombination. Nucleic Acids Res. 2003;31:4959–4964
  40. Satoh MS, Lindahl T. Role of poly(ADP-ribose) formation in DNA repair. Nature. 1992;356:356–358

 Funded by the Medical Research Council.

 Conflict of interest: none.

PII: S0360-3016(08)03170-2

doi: 10.1016/j.ijrobp.2008.07.031

International Journal of Radiation Oncology * Biology * Physics
Volume 72, Issue 4 , Pages 1188-1197 , 15 November 2008