Discordant in vitro and in vivo chemopotentiating effects of the PARP inhibitor veliparib in temozolomide-sensitive versus -resistant glioblastoma multiforme xenografts

Clinical Cancer Research

Volumn 20, Issue 14, 2014, Pages 3730-3741

  Gupta, Shiv K ^a   Mladek, Ann C ^a   Carlson, Brett L ^a   Boakye Agyeman, Felix ^b   Bakken, Katrina K ^a   Kizilbash, Sani H ^a   Schroeder, Mark A ^a   Reid, Joel ^b   Sarkaria, Jann N ^a  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA H2AX; HISTONE H2AX; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; SHORT HAIRPIN RNA; TEMOZOLOMIDE; UNCLASSIFIED DRUG; VELIPARIB; ALKYLATING AGENT; BENZIMIDAZOLE DERIVATIVE; DACARBAZINE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; PARP1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CANCER RESISTANCE; CELL ASSAY; CHEMOSENSITIZATION; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG EFFICACY; DRUG POTENTIATION; GLIOBLASTOMA; IN VITRO STUDY; IN VIVO STUDY; MAXIMUM PLASMA CONCENTRATION; MOUSE; MULTIPLE CYCLE TREATMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; ANALOGS AND DERIVATIVES; ANIMAL; BRAIN NEOPLASMS; COMPARATIVE STUDY; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENE SILENCING; GENETICS; HUMAN; METABOLISM; NUDE MOUSE; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; BENZIMIDAZOLES; BRAIN NEOPLASMS; CELL LINE, TUMOR; DACARBAZINE; DNA DAMAGE; DRUG RESISTANCE, NEOPLASM; GENE KNOCKDOWN TECHNIQUES; GLIOBLASTOMA; HUMANS; MICE, NUDE; POLY(ADP-RIBOSE) POLYMERASE INHIBITORS; POLY(ADP-RIBOSE) POLYMERASES; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84904383968     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-13-3446     Document Type: Article

References (48)

1. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 2009;10:459-66.
2. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352:987-96. (Pubitemid 40349501)
3. Friedman HS, Kerby T, Calvert H. Temozolomide and treatment of malignant glioma. Clin Cancer Res 2000;6:2585-97. (Pubitemid 30482092)
4. Helleday T, Petermann E, Lundin C, Hodgson B, Sharma RA. DNA repair pathways as targets for cancer therapy. Nat Rev Cancer 2008;8:193-204. (Pubitemid 351301852)
5. Kaina B, Christmann M, Naumann S, Roos WP. MGMT: key node in the battle against genotoxicity, carcinogenicity, and apoptosis induced by alkylating agents. DNA Repair 2007;6:1079-99. (Pubitemid 47058389)
6. Kitange GJ, Carlson BL, Mladek AC, Decker PA, Schroeder MA, Wu W, et al. Evaluation of MGMT promoter methylation status and correlation with temozolomide response in orthotopic glioblastoma xenograft model. J Neurooncol 2009;92:23-31.
7. Sarkaria JN, Kitange GJ, James CD, Plummer R, Calvert H, Weller M, et al. Mechanisms of chemoresistance to alkylating agents in malignant glioma. Clin Cancer Res 2008;14:2900-8.
8. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005;352:997-1003. (Pubitemid 40349502)
9. Kitange GJ, Mladek AC, Carlson BL, Schroeder MA, Pokorny JL, Cen L, et al. Inhibition of histone deacetylation potentiates the evolution of acquired temozolomide resistance linked to MGMT upregulation in glioblastoma xenografts. Clin Cancer Res 2012;18:4070-9.
10. D'Atri S, Tentori L, Lacal PM, Graziani G, Pagani E, Benincasa E, et al. Involvement of the mismatch repair system in temozolomide-induced apoptosis. Mol Pharmacol 1998;54:334-41. (Pubitemid 28368823)
11. Cahill DP, Levine KK, Betensky RA, Codd PJ, Romany CA, Reavie LB, et al. Loss of the mismatch repair protein MSH6 in human glioblastomas is associated with tumor progression during temozolomide treatment. Clin Cancer Res 2007;13:2038-45. (Pubitemid 46649870)
12. Felsberg J, Thon N, Eigenbrod S, Hentschel B, Sabel MC, Westphal M, et al. Promoter methylation and expression of MGMT and the DNA mismatch repair genes MLH1, MSH2, MSH6 and PMS2 in paired primary and recurrent glioblastomas. Int J Cancer 2011;129:659-70.
13. Yip S, Miao J, Cahill DP, Iafrate AJ, Aldape K, Nutt CL, et al. MSH6 mutations arise in glioblastomas during temozolomide therapy and mediate temozolomide resistance. Clin Cancer Res 2009;15:4622-9.
14. Calabrese CR, Almassy R, Barton S, Batey MA, Calvert AH, Canan-Koch 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. (Pubitemid 38180960)
15. Thomas HD, Calabrese CR, Batey MA, Canan S, Hostomsky Z, Kyle S, et al. Preclinical selection of a novel poly(ADP-ribose) polymerase inhibitor for clinical trial. Mol Cancer Ther 2007;6:945-56. (Pubitemid 46554564)
16. Helleday T. The underlying mechanism for the PARP and BRCA synthetic lethality: clearing up the misunderstandings. Mol Oncol 2011;5:387-93.
17. Fortini P, Pascucci B, Parlanti E, D'Errico M, Simonelli V, Dogliotti E. The base excision repair: mechanisms and its relevance for cancer susceptibility. Biochimie 2003;85:1053-71. (Pubitemid 38142361)
18. Liu X, Shi Y, Guan R, Donawho C, Luo Y, Palma J, et al. Potentiation of temozolomide cytotoxicity by poly(ADP)ribose polymerase inhibitor ABT-888 requires a conversion of single-stranded DNA damages to double-stranded DNA breaks. Mol Cancer Res 2008;6:1621-9.
19. Masson M, Niedergang C, Schreiber V, Muller S, Menissier-de Murcia J, de Murcia G. XRCC1is specifically associated with poly(ADP-ribose) polymerase and negatively regulates its activity following DNA damage. Mol Cell Biol 1998;18:3563-71. (Pubitemid 28240528)
20. Svilar D, Goellner EM, Almeida KH, Sobol RW. Base excision repair and lesion-dependent subpathways for repair of oxidative DNA damage. Antioxid Redox Signal 2011;14:2491-507.
21. Agnihotri S, Gajadhar AS, Ternamian C, Gorlia T, Diefes KL, Mischel PS, et al. Alkylpurine-DNA-N-glycosylase confers resistance to temozolomide in xenograft models of glioblastoma multiforme and is associated with poor survival in patients. J Clin Invest 2012;122:253-66.
22. Miknyoczki S, Chang H, Grobelny J, Pritchard S, Worrell C, McGann N, 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;6:2290-302. (Pubitemid 47294757)
23. Chalmers AJ. Overcoming resistance of glioblastoma to conventional cytotoxic therapies by the addition of PARP inhibitors. Anticancer Agents Med Chem 2010;10:520-33.
24. Goellner EM, Grimme B, Brown AR, Lin YC, Wang XH, Sugrue KF, et al. Overcoming temozolomide resistance in glioblastoma via dual inhibition of NAD +biosynthesis and base excision repair. Cancer Res 2011;71:2308-17.
25. Horton TM, Jenkins G, Pati D, Zhang L, Dolan ME, Ribes-Zamora A, et al. Poly(ADP-ribose) polymerase inhibitor ABT-888 potentiates the cytotoxic activity of temozolomide in leukemia cells: influence of mismatch repair status and O6-methylguanine-DNA methyltransferase activity. Mol Cancer Ther 2009;8:2232-42.
26. Tentori L, Muzi A, Dorio AS, Scarsella M, Leonetti C, Shah GM, et al. Pharmacological inhibition of poly(ADP-ribose) polymerase (PARP) activity in PARP-1 silenced tumour cells increases chemosensitivity to temozolomide and to a N3-adenine selective methylating agent. Curr Cancer Drug Targets 2010;10:368-83.
27. Clarke MJ, Mulligan EA, Grogan PT, Mladek AC, Carlson BL, Schroeder MA, et al. Effective sensitization of temozolomide by ABT-888 is lost with development of temozolomide resistance in glioblastoma xenograft lines. Mol Cancer Ther 2009;8:407-14.
28. Nadkarni A, Shrivastav M, Mladek AC, Schwingler PM, Grogan PT, Chen J, et al. ATM inhibitor KU-55933 increases the TMZ responsiveness of only inherently TMZ-sensitive GBM cells. J Neurooncol 2012;110:349-57.
29. Capes-Davis A, Reid YA, Kline MC, Storts DR, Strauss E, Dirks WG, et al. Match criteria for human cell line authentication: where do we draw the line? Int J Cancer 2013;132:2510-9.
30. Middlemas DS, Stewart CF, Kirstein MN, Poquette C, Friedman HS, Houghton PJ, et al. Biochemical correlates of temozolomide sensitivity in pediatric solid tumor xenograft models. Clin Cancer Res 2000;6:998-1007. (Pubitemid 30159360)
31. Giannini C, Sarkaria JN, Saito A, Uhm JH, Galanis E, Carlson BL, et al. Patient tumor EGFR and PDGFRA gene amplifications retained in an invasive intracranial xenograft model of glioblastoma multiforme. Neuro Oncol 2005;7:164-76. (Pubitemid 40590516)
32. Curtin NJ, Wang LZ, Yiakouvaki A, Kyle S, Arris CA, Canan-Koch S, et al. Novel poly(ADP-ribose) polymerase-1 inhibitor, AG14361, restores sensitivity to temozolomide in mismatch repair-deficient cells. Clin Cancer Res 2004;10:881-9. (Pubitemid 38198886)
33. Donawho CK, Luo Y, Penning TD, Bauch JL, Bouska JJ, Bontcheva-Diaz VD, 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;13:2728-37. (Pubitemid 46795129)
34. Tentori L, Leonetti C, Scarsella M, Muzi A, Mazzon E, Vergati M, et al. Inhibition of poly(ADP-ribose) polymerase prevents irinotecan-induced intestinal damage and enhances irinotecan/temozolomide efficacy against colon carcinoma. Faseb J 2006;20:1709-11.
35. Tentori L, Leonetti C, Scarsella M, D'Amati G, Vergati M, Portarena I, et al. Systemic administration of GPI 15427, a novel poly(ADP-ribose) polymerase-1 inhibitor, increases the antitumor activity of temozolomide against intracranial melanoma, glioma, lymphoma. Clin Cancer Res 2003;9:5370-9. (Pubitemid 37413592)
36. Daniel RA, Rozanska AL, Thomas HD, Mulligan EA, Drew Y, Castelbuono DJ, et al. Inhibition of poly(ADP-ribose) polymerase-1 enhances temozolomide and topotecan activity against childhood neuroblastoma. Clin Cancer Res 2009;15:1241-9.
37. Liu X, Han EK, Anderson M, Shi Y, Semizarov D, Wang G, et al. Acquired resistance to combination treatment with temozolomide and ABT-888 is mediated by both base excision repair and homologous recombination DNA repair pathways. Mol Cancer Res 2009;7:1686-92.
38. Liu X, Palma J, Kinders R, Shi Y, Donawho C, Ellis PA, et al. An enzyme-linked immunosorbent poly(ADP-ribose) polymerase biomarker assay for clinical trials of PARP inhibitors. Anal Biochem 2008;381:240-7.
39. Penning TD, Zhu GD, Gandhi VB, Gong J, Liu X, Shi Y, et al. Discovery of the Poly(ADP-ribose) polymerase (PARP) inhibitor 2-[(R)-2-methylpyrrolidin-2-yl] -1H-benzimidazole-4-carboxamide (ABT-888) for the treatment of cancer. J Med Chem 2009;52:514-23.
40. Kummar S, Kinders R, Gutierrez ME, Rubinstein L, Parchment RE, Phillips LR, et al. Phase 0 clinical trial of the poly (ADP-ribose) polymerase inhibitor ABT-888 in patients with advanced malignancies. J Clin Oncol 2009;27:2705-11.
41. Tentori L, Turriziani M, Franco D, Serafino A, Levati L, Roy R, et al. Treatment with temozolomide and poly(ADP-ribose) polymerase inhibitors induces early apoptosis and increases base excision repair gene transcripts in leukemic cells resistant to triazene compounds. Leukemia 1999;13:901-9. (Pubitemid 29292141)
42. Murai J, Huang SY, Das BB, Renaud A, Zhang Y, Doroshow JH, et al. Trapping of PARP1 and PARP2 by Clinical PARP Inhibitors. Cancer Res 2012;72:5588-99.
43. Jagtap P, Szabo C. Poly(ADP-ribose) polymerase and the therapeutic effects of its inhibitors. Nat Rev Drug Discov 2005;4:421-40. (Pubitemid 40704125)
44. Bryant HE, Petermann E, Schultz N, Jemth AS, Loseva O, Issaeva N, et al. PARP is activated at stalled forks to mediate Mre11-dependent replication restart and recombination. Embo J 2009;28:2601-15.
45. Calvert H, Azzariti A. The clinical development of inhibitors of poly (ADP-ribose) polymerase. Ann Oncol 2011;22 Suppl 1:i53-9.
46. Ekblad T, Camaioni E, Schuler H, Macchiarulo A. PARP inhibitors: polypharmacology versus selective inhibition. Febs J 2013;280:3563-75.
47. Shen Y, Rehman FL, Feng Y, Boshuizen J, Bajrami I, Elliott R, et al. BMN673, a novel and highly potent PARP1/2 inhibitor for the treatment of human cancers with DNA repair deficiency. Clin Cancer Res 2013;19:5003-15.
48. Quinn JA, Jiang SX, Reardon DA, Desjardins A, Vredenburgh JJ, Friedman AH, et al. Phase II trial of temozolomide (TMZ) plus irinotecan (CPT-11) in adults with newly diagnosed glioblastoma multiforme before radiotherapy. J Neuro-Oncol 2009;95:393-400.