MGMT expression predicts parp-mediated resistance to temozolomide

Molecular Cancer Therapeutics

Volumn 14, Issue 5, 2015, Pages 1236-1246

  Erice, Oihane ^a,d   Smith, Michael P ^a   White, Rachel ^b   Goicoechea, Ibai ^a,d   Barriuso, Jorge ^a   Jones, Chris ^c   Margison, Geoffrey P ^a   Acosta, Juan C ^b   Wellbrock, Claudia ^a   Arozarena, Imanol ^a,e  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^d BIODONOSTIA HEALTH RESEARCH INSTITUTE   (Spain)

^e UNIVERSITY OF HUDDERSFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H2AX; LOMEGUATRIB; MESYLIC ACID METHYL ESTER; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; OLAPARIB; SELUMETINIB; TEMOZOLOMIDE; VELIPARIB; ALKYLATING AGENT; DACARBAZINE; DNA LIGASE; DNA METHYLTRANSFERASE; MGMT PROTEIN, HUMAN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; TUMOR SUPPRESSOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CELL CYCLE ARREST; CELL PROLIFERATION; CHEMOSENSITIZATION; COLONY FORMATION; COLORECTAL CANCER CELL LINE; CONTROLLED STUDY; DNA DAMAGE; DNA METHYLATION; DNA REPAIR; DRUG POTENTIATION; EMBRYO; GLIOBLASTOMA CELL LINE; GROWTH INHIBITION (CONCENTRATION); HISTONE PHOSPHORYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MELANOMA; MELANOMA CELL; MELANOMA CELL LINE; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; ZEBRA FISH; ANALOGS AND DERIVATIVES; ANIMAL; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; METABOLISM; MOUSE; TUMOR CELL LINE;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; CELL LINE, TUMOR; CELL PROLIFERATION; DACARBAZINE; DNA MODIFICATION METHYLASES; DNA REPAIR ENZYMES; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MELANOMA; MICE; POLY(ADP-RIBOSE) POLYMERASE INHIBITORS; POLY(ADP-RIBOSE) POLYMERASES; TUMOR SUPPRESSOR PROTEINS;

EID: 84942096774     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-14-0810     Document Type: Article

References (49)

1. Belden S, Flaherty KT. MEK and RAF inhibitors for BRAF-mutated cancers. Expert Rev Mol Med 2012;14:e17.
2. Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, et al. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. N Engl J Med 2011;364:2507-16.
3. Flaherty KT, Infante JR, Daud A, Gonzalez R, Kefford RF, Sosman J, et al. Combined BRAF and MEK inhibition in melanoma with BRAF V600 mutations. N Engl J Med 2012;367:1694-703.
4. Marchesi F, Turriziani M, Tortorelli G, Avvisati G, Torino F, De Vecchis L. Triazene compounds: mechanism of action and related DNA repair systems. Pharmacol Res 2007;56:275-87.
5. Mouawad R, Sebert M, Michels J, Bloch J, Spano JP, Khayat D. Treatment for metastatic malignant melanoma: old drugs and new strategies. Crit Rev Oncol Hematol 2010;74:27-39.
6. Koekkoek JA, Wiggenraad RG, Zwinkels H, Oosterkamp HM, Taphoorn MJ. Survival over 6 years in a patient with brain metastases from melanoma treated with temozolomide. BMJ Case Rep 2012;24:2012.
7. Siena S, Crino L, Danova M, Del Prete S, Cascinu S, Salvagni S, et al. Dosedense temozolomide regimen for the treatment of brain metastases from melanoma, breast cancer, or lung cancer not amenable to surgery or radiosurgery: a multicenter phase II study. Ann Oncol 2010;21:655-61.
8. Zhu W, Zhou L, Qian JQ, Qiu TZ, Shu YQ, Liu P. Temozolomide for treatment of brain metastases: A review of 21 clinical trials. World J Clin Oncol 2014;5:19-27.
9. Middleton MR, Grob JJ, Aaronson N, Fierlbeck G, Tilgen W, Seiter S, et al. Randomized phase III study of temozolomide versus dacarbazine in the treatment of patients with advanced metastatic malignant melanoma. J Clin Oncol 2000;18:158-66.
10. Patel PM, Suciu S, Mortier L, Kruit WH, Robert C, Schadendorf D, et al. Extended schedule, escalated dose temozolomide versus dacarbazine in stage IV melanoma: final results of a randomised phase III study (EORTC 18032). Eur J Cancer 2011;47:1476-83.
11. 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.
12. Verbeek B, Southgate TD, Gilham DE, Margison GP. O6-Methylguanine-DNA methyltransferase inactivation and chemotherapy. Br Med Bull 2008;85:17-33.
13. Wick W, Platten M, Meisner C, Felsberg J, Tabatabai G, Simon M, et al. Temozolomide chemotherapy alone versus radiotherapy alone for malignant astrocytoma in the elderly: the NOA-08 randomised, phase 3 trial. Lancet Oncol 2012;13:707-15.
14. Khan OA, Ranson M, Michael M, Olver I, Levitt NC, Mortimer P, et al. A phase II trial of lomeguatrib and temozolomide in metastatic colorectal cancer. Br J Cancer 2008;98:1614-8.
15. Ranson M, Hersey P, Thompson D, Beith J, McArthur GA, Haydon A, et al. Randomized trial of the combination of lomeguatrib and temozolomide compared with temozolomide alone in chemotherapy naive patients with metastatic cutaneous melanoma. J Clin Oncol 2007;25:2540-5.
16. Ranson M, Middleton MR, Bridgewater J, Lee SM, Dawson M, Jowle D, et al. Lomeguatrib, a potent inhibitor of O6-alkylguanine-DNA-alkyltransferase: phase I safety, pharmacodynamic, and pharmacokinetic trial and evaluation in combination with temozolomide in patients with advanced solid tumors. Clin Cancer Res 2006;12:1577-84.
17. Basu B, Yap TA, Molife LR, de Bono JS. Targeting the DNA damage response in oncology: past, present and future perspectives. Curr Opin Oncol 2012;24:316-24.
18. Lee JM, Ledermann JA, Kohn EC. PARP inhibitors for BRCA1/2 mutationassociated and BRCA-like malignancies. Ann Oncol 2014;25:32-40.
19. Bedikian AY, Papadopoulos NE, Kim KB, HwuWJ, Homsi J, GlassMR, et al. A phase IB trial of intravenous INO-1001 plus oral temozolomide in subjects with unresectable stage-III or IV melanoma. Cancer Invest 2009;27:756-63.
20. Plummer R, Jones C, MiddletonM, Wilson R, Evans J, Olsen A, et al. Phase I study of the poly (ADP-ribose) polymerase inhibitor, AG014699, in combination with temozolomide in patients with advanced solid tumors. Clin Cancer Res 2008;14:7917-23.
21. Hussain M, Carducci MA, Slovin S, Cetnar J, Qian J, McKeegan EM, et al. Targeting DNA repair with combination veliparib (ABT-888) and temozolomide in patients with metastatic castration-resistant prostate cancer. Invest New Drugs 2014;32:904-12.
22. Khan OA, Gore M, Lorigan P, Stone J, Greystoke A, Burke W, et al. A phase I study of the safety and tolerability of olaparib (AZD2281, KU0059436) and dacarbazine in patients with advanced solid tumours. Br J Cancer 2011;104:750-5.
23. Plummer R, Lorigan P, Steven N, Scott L, Middleton MR, Wilson RH, et al. A phase II study of the potent PARP inhibitor, Rucaparib (PF-01367338, AG014699), with temozolomide in patients with metastatic melanoma demonstrating evidence of chemopotentiation. Cancer Chemother Pharmacol 2013;71:1191-9.
24. Arozarena I, Goicoechea I, Erice O, Ferguson J, Margison GP, Wellbrock C. Differential chemosensitivity to antifolate drugs between RAS and BRAF melanoma cells. Mol Cancer 2014;13:154.
25. Gaspar N, Marshall L, Perryman L, Bax DA, Little SE, Viana-PereiraM, et al. MGMT-independent temozolomide resistance in pediatric glioblastoma cells associated with a PI3-kinase-mediated HOX/stem cell gene signature. Cancer Res 2010;70:9243-52.
26. Smith MP, Ferguson J, Arozarena I, Hayward R, Marais R, Chapman A, et al. Effect of SMURF2 targeting on susceptibility to MEK inhibitors in melanoma. J Natl Cancer Inst 2013;105:33-46.
27. Arozarena I, Bischof H, Gilby D, Belloni B, Dummer R, Wellbrock C. In melanoma, beta-catenin is a suppressor of invasion. Oncogene 2011;30:4531-43.
28. Watson AJ, Sabharwal A, Thorncroft M, McGown G, Kerr R, Bojanic S, et al. Tumor O (6)-methylguanine-DNA methyltransferase inactivation by oral lomeguatrib. Clin Cancer Res 2010;16:743-9.
29. Acosta JC, Banito A, Wuestefeld T, Georgilis A, Janich P, Morton JP, et al. A complex secretory program orchestrated by the inflammasome controls paracrine senescence. Nat Cell Biol 2013;15:978-90.
30. Murai J, Huang SY, Renaud A, Zhang Y, Ji J, Takeda S, et al. Stereospecific PARP trapping by BMN 673 and comparison with olaparib and rucaparib. Mol Cancer Ther 2014;13:433-43.
31. Murai J, Zhang Y, Morris J, Ji J, Takeda S, Doroshow JH, et al. Rationale for poly (ADP-ribose) polymerase (PARP) inhibitors in combination therapy with camptothecins or temozolomide based on PARP trapping versus catalytic inhibition. J Pharmacol Exp Ther 2014;349:408-16.
32. Chapman A, Fernandez Del Ama L, Ferguson J, Kamarashev J, Wellbrock C, Hurlstone A. Heterogeneous tumor subpopulations cooperate to drive invasion. Cell Rep 2014;8:688-95.
33. Fine RL, Gulati AP, Krantz BA, Moss RA, Schreibman S, Tsushima DA, et al. Capecitabine and temozolomide (CAPTEM) for metastatic, welldifferentiated neuroendocrine cancers: The Pancreas Center at Columbia University experience. Cancer Chemother Pharmacol 2013;71:663-70.
34. Hochhauser D, Glynne-Jones R, Potter V, Gravalos C, Doyle TJ, Pathiraja K, et al. A phase II study of temozolomide in patients with advanced aerodigestive tract and colorectal cancers and methylation of the O6-methylguanine-DNA methyltransferase promoter. Mol Cancer Ther 2013;12:809-18.
35. Lengauer C, Kinzler KW, Vogelstein B. DNA methylation and genetic instability in colorectal cancer cells. Proc Natl Acad Sci U S A 1997;94:2545-50.
36. Pachkowski BF, Tano K, Afonin V, Elder RH, Takeda S, Watanabe M, et al. Cells deficient in PARP-1 show an accelerated accumulation of DNA single strand breaks, but not AP sites, over the PARP-1-proficient cells exposed to MMS. Mutat Res 2009;671:93-9.
37. Naumann SC, Roos WP, Jost E, Belohlavek C, Lennerz V, Schmidt CW, et al. Temozolomide- and fotemustine-induced apoptosis in human malignant melanoma cells: response related to MGMT, MMR, DSBs, and p53. Br J Cancer 2009;100:322-33.
38. Kuilman T, Michaloglou C, Mooi WJ, Peeper DS. The essence of senescence. Genes Dev 2010;24:2463-79.
39. Mhaidat NM, Zhang XD, Allen J, Avery-Kiejda KA, Scott RJ, Hersey P. Temozolomide induces senescence but not apoptosis in human melanoma cells. Br J Cancer 2007;97:1225-33.
40. 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.
41. Su JM, Thompson P, Adesina A, Li XN, Kilburn L, Onar-Thomas A, et al. A phase I trial of veliparib (ABT-888) and temozolomide in children with recurrent CNS tumors: a Pediatric Brain Tumor Consortium reportdagger. Neuro Oncol 2014;16:1661-8.
42. Palma JP, Wang YC, Rodriguez LE, Montgomery D, Ellis PA, Bukofzer G, et al. ABT-888 confers broad in vivo activity in combination with temozolomide in diverse tumors. Clin Cancer Res 2009;15:7277-90.
43. 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.
44. Gupta SK, Mladek AC, Carlson BL, Boakye-Agyeman F, Bakken KK, Kizilbash SH, et al. Discordant in vitro and in vivo chemopotentiating effects of the PARP inhibitor veliparib in temozolomide-sensitive versus-resistant glioblastoma multiforme xenografts. Clin Cancer Res 2014;20:3730-41.
45. Cen L, Carlson BL, Pokorny JL, Mladek AC, Grogan PT, Schroeder MA, et al. Efficacy of protracted temozolomide dosing is limited in MGMT unmethylated GBM xenograft models. Neuro Oncol 2013;15:735-46.
46. Weller M, van den Bent M, Hopkins K, Tonn JC, Stupp R, Falini A, et al. EANO guideline for the diagnosis and treatment of anaplastic gliomas and glioblastoma. Lancet Oncol 2014;15:e395-403.
47. Kulke MH, Hornick JL, Frauenhoffer C, Hooshmand S, Ryan DP, Enzinger PC, et al. O6-methylguanine DNA methyltransferase deficiency and response to temozolomide-based therapy in patientswith neuroendocrine tumors. Clin Cancer Res 2009;15:338-45.
48. Lalezari S, Chou AP, Tran A, Solis OE, Khanlou N, Chen W, et al. Combined analysis of O6-methylguanine-DNA methyltransferase protein expression and promoter methylation provides optimized prognostication of glioblastoma outcome. Neuro Oncol 2013;15:370-81.
49. Mirzayans R, Andrais B, Scott A, MurrayD. New insights into p53 signaling and cancer cell response to DNA damage: implications for cancer therapy. J Biomed Biotechnol 2012;2012:170325.