ABT-888 enhances cytotoxic effects of temozolomide independent of MGMT status in serum free cultured glioma cells

Journal of Translational Medicine

Volumn 13, Issue 1, 2015, Pages

  Balvers, Rutger K ^a   Lamfers, Martine L M ^a   Kloezeman, Jenneke J ^a   Kleijn, Anne ^a   Berghauser Pont, Lotte M E ^a   Dirven, Clemens M F ^a   Leenstra, Sieger ^a,b  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b Microvida Laboratory for Medical Microbiology and Immunology   (Netherlands)

Author keywords

ABT 888; Combination therapy; Drug screening; Glioblastoma; GSC; MGMT; PARP inhibition; Temozolomide

Indexed keywords

ETOPOSIDE; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; TEMOZOLOMIDE; VELIPARIB; BENZIMIDAZOLE DERIVATIVE; DACARBAZINE; DNA LIGASE; DNA METHYLTRANSFERASE; MGMT PROTEIN, HUMAN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; SERUM-FREE MEDIUM; TUMOR SUPPRESSOR PROTEIN;

ADULT; AGED; ANTINEOPLASTIC ACTIVITY; APOPTOSIS ASSAY; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL VIABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; DNA METHYLATION ASSAY; DOUBLE STRANDED DNA BREAK; DRUG CYTOTOXICITY; DRUG POTENTIATION; DRUG SCREENING; DRUG SENSITIVITY; FEASIBILITY STUDY; GLIOBLASTOMA CELL LINE; GLIOMA; GLIOMA CELL LINE; GLIOMA STEM CELL; HUMAN; HUMAN TISSUE; IN VITRO STUDY; MONOTHERAPY; PROTEIN EXPRESSION; PROTEIN INDUCTION; TREATMENT RESPONSE; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; APOPTOSIS; BRAIN NEOPLASMS; CANCER STEM CELL; DRUG EFFECTS; METABOLISM; PATHOLOGY; SERUM-FREE MEDIUM; TUMOR CELL CULTURE;

APOPTOSIS; AUTOPHAGY; BENZIMIDAZOLES; BRAIN NEOPLASMS; CULTURE MEDIA, SERUM-FREE; DACARBAZINE; DNA BREAKS, DOUBLE-STRANDED; DNA MODIFICATION METHYLASES; DNA REPAIR ENZYMES; GLIOMA; HUMANS; NEOPLASTIC STEM CELLS; POLY(ADP-RIBOSE) POLYMERASE INHIBITORS; POLY(ADP-RIBOSE) POLYMERASES; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEINS;

EID: 84928720748     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/s12967-015-0427-y     Document Type: Article

References (49)

1. Huse JT, Holland EC. Targeting brain cancer: advances in the molecular pathology of malignant glioma and medulloblastoma. Nat Rev Cancer. 2010;10(5):319-31.
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(10):987-96.
3. Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP, et al. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell. 2010;17(5):510-22.
4. Weller M, Stupp R, Reifenberger G, Brandes AA, van den Bent MJ, Wick W, et al. MGMT promoter methylation in malignant gliomas: ready for personalized medicine? Nat Rev Neurol. 2010;6(1):39-51.
5. 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(10):997-1003.
6. 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(1):253-66.
7. McEllin B, Camacho CV, Mukherjee B, Hahm B, Tomimatsu N, Bachoo RM, et al. PTEN loss compromises homologous recombination repair in astrocytes: implications for glioblastoma therapy with temozolomide or poly(ADP-ribose) polymerase inhibitors. Cancer Res. 2010;70(13):5457-64.
8. Wahlberg E, Karlberg T, Kouznetsova E, Markova N, Macchiarulo A, Thorsell AG, et al. Family-wide chemical profiling and structural analysis of PARP and tankyrase inhibitors. Nat Biotechnol. 2012;30(3):283-8.
9. Pollard SM, Yoshikawa K, Clarke ID, Danovi D, Stricker S, Russell R, et al. Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell. 2009;4(6):568-80.
10. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell. 2006;9(5):391-403.
11. Balvers RK, Kleijn A, Kloezeman JJ, French PJ, Kremer A, van den Bent MJ, et al. Serum-free culture success of glial tumors is related to specific molecular profiles and expression of extracellular matrix-associated gene modules. Neuro Oncol. 2013;15(12):1684-95.
12. Muscal JA, Thompson PA, Giranda VL, Dayton BD, Bauch J, Horton T, et al. Plasma and cerebrospinal fluid pharmacokinetics of ABT-888 after oral administration in non-human primates. Cancer Chemother Pharmacol. 2010;65(3):419-25.
13. Rosso L, Brock CS, Gallo JM, Saleem A, Price PM, Turkheimer FE, et al. A new model for prediction of drug distribution in tumor and normal tissues: pharmacokinetics of temozolomide in glioma patients. Cancer Res. 2009;69(1):120-7.
14. Chou TC. Drug combination studies and their synergy quantification using the Chou-Talalay method. Cancer Res. 2010;70(2):440-6.
15. Biederbick A, Kern HF, Elsasser HP. Monodansylcadaverine (MDC) is a specific in vivo marker for autophagic vacuoles. Eur J Cell Biol. 1995;66(1):3-14.
16. Berghauser Pont LM, Spoor JK, Venkatesan S, Swagemakers S, Kloezeman JJ, Dirven CM, et al. The Bcl-2 inhibitor Obatoclax overcomes resistance to histone deacetylase inhibitors SAHA and LBH589 as radiosensitizers in patient-derived glioblastoma stem-like cells. Genes Cancer. 2014;5(11-12):445-59.
17. Costello JF, Futscher BW, Tano K, Graunke DM, Pieper RO. Graded methylation in the promoter and body of the O6-methylguanine DNA methyltransferase (MGMT) gene correlates with MGMT expression in human glioma cells. J Biol Chem. 1994;269(25):17228-37.
18. van Nifterik KA, van den Berg J, van der Meide WF, Ameziane N, Wedekind LE, Steenbergen RD, et al. Absence of the MGMT protein as well as methylation of the MGMT promoter predict the sensitivity for temozolomide. Br J Cancer. 2010;103(1):29-35.
19. Li A, Walling J, Kotliarov Y, Center A, Steed ME, Ahn SJ, et al. Genomic changes and gene expression profiles reveal that established glioma cell lines are poorly representative of primary human gliomas. Mol Cancer Res. 2008;6(1):21-30.
20. Ostermann S, Csajka C, Buclin T, Leyvraz S, Lejeune F, Decosterd LA, et al. Plasma and cerebrospinal fluid population pharmacokinetics of temozolomide in malignant glioma patients. Clin Cancer Res. 2004;10(11):3728-36.
21. 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(3):370-81.
22. Barazzuol L, Jena R, Burnet NG, Meira LB, Jeynes JC, Kirkby KJ, et al. Evaluation of poly (ADP-ribose) polymerase inhibitor ABT-888 combined with radiotherapy and temozolomide in glioblastoma. Radiat Oncol. 2013;8:65.
23. Albert JM, Cao C, Kim KW, Willey CD, Geng L, Xiao D, et al. Inhibition of poly(ADP-ribose) polymerase enhances cell death and improves tumor growth delay in irradiated lung cancer models. Clin Cancer Res. 2007;13(10):3033-42.
24. Ethier C, Tardif M, Arul L, Poirier GG. PARP-1 modulation of mTOR signaling in response to a DNA alkylating agent. PLoS One. 2012;7(10):e47978.
25. Jiang H, White EJ, Conrad C, Gomez-Manzano C, Fueyo J. Autophagy pathways in glioblastoma. Methods Enzymol. 2009;453:273-86.
26. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2012;8(4):445-544.
27. Kummar S, Chen A, Parchment RE, Kinders RJ, Ji J, Tomaszewski JE, et al. Advances in using PARP inhibitors to treat cancer. BMC Med. 2012;10:25.
28. Krishnakumar R, Kraus WL. The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol Cell. 2010;39(1):8-24.
29. Tentori L, Portarena I, Torino F, Scerrati M, Navarra P, Graziani G. Poly(ADP-ribose) polymerase inhibitor increases growth inhibition and reduces G(2)/M cell accumulation induced by temozolomide in malignant glioma cells. Glia. 2002;40(1):44-54.
30. 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(9):2728-37.
31. 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(23):7277-90.
32. 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(14):5370-9.
33. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444(7120):756-60.
34. Beier D, Schriefer B, Brawanski K, Hau P, Weis J, Schulz JB, et al. Efficacy of clinically relevant temozolomide dosing schemes in glioblastoma cancer stem cell lines. J Neurooncol. 2012;109(1):45-52.
35. Beier D, Schulz JB, Beier CP. Chemoresistance of glioblastoma cancer stem cells-much more complex than expected. Mol Cancer. 2011;10:128.
36. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, Abdulkadir IR, et al. Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer. 2006;5:67.
37. Glas M, Rath BH, Simon M, Reinartz R, Schramme A, Trageser D, et al. Residual tumor cells are unique cellular targets in glioblastoma. Ann Neurol. 2010;68(2):264-9.
38. Clement V, Sanchez P, de Tribolet N, Radovanovic I, Ruiz I, Altaba A. HEDGEHOG-GLI1 signaling regulates human glioma growth, cancer stem cell self-renewal, and tumorigenicity. Curr Biol. 2007;17(2):165-72.
39. Beier D, Rohrl S, Pillai DR, Schwarz S, Kunz-Schughart LA, Leukel P, et al. Temozolomide preferentially depletes cancer stem cells in glioblastoma. Cancer Res. 2008;68(14):5706-15.
40. Blough MD, Westgate MR, Beauchamp D, Kelly JJ, Stechishin O, Ramirez AL, et al. Sensitivity to temozolomide in brain tumor initiating cells. Neuro Oncol. 2010;12(7):756-60.
41. Villalva C, Cortes U, Wager M, Tourani JM, Rivet P, Marquant C, et al. O6-Methylguanine-Methyltransferase (MGMT) promoter methylation status in glioma stem-like cells is correlated to temozolomide sensitivity under differentiation-promoting conditions. Int J Mol Sci. 2012;13(6):6983-94.
42. Ishii N, Maier D, Merlo A, Tada M, Sawamura Y, Diserens AC, et al. Frequent co-alterations of TP53, p16/CDKN2A, p14ARF, PTEN tumor suppressor genes in human glioma cell lines. Brain Pathol. 1999;9(3):469-79.
43. Ohgaki H, Kleihues P. Genetic alterations and signaling pathways in the evolution of gliomas. Cancer Sci. 2009;100(12):2235-41.
44. Cancer Genome Atlas Research, N. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature. 2008;455(7216):1061-8.
45. Turner NC, Lord CJ, Iorns E, Brough R, Swift S, Elliott R, et al. A synthetic lethal siRNA screen identifying genes mediating sensitivity to a PARP inhibitor. EMBO J. 2008;27(9):1368-77.
46. Dedes KJ, Wilkerson PM, Wetterskog D, Weigelt B, Ashworth A, Reis-Filho JS. Synthetic lethality of PARP inhibition in cancers lacking BRCA1 and BRCA2 mutations. Cell Cycle. 2011;10(8):1192-9.
47. Tentori L, Ricci-Vitiani L, Muzi A, Ciccarone F, Pelacchi F, Calabrese R, et al. Pharmacological inhibition of poly(ADP-ribose) polymerase-1 modulates resistance of human glioblastoma stem cells to temozolomide. BMC Cancer. 2014;14(1):151.
48. van den Bent MJ, Carpentier AF, Brandes AA, Sanson M, Taphoorn MJ, Bernsen HJ, et al. Adjuvant procarbazine, lomustine, and vincristine improves progression-free survival but not overall survival in newly diagnosed anaplastic oligodendrogliomas and oligoastrocytomas: a randomized European Organisation for Research and Treatment of Cancer phase III trial. J Clin Oncol. 2006;24(18):2715-22.
49. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV, et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ. 2012;19(1):107-20.