Acquired resistance to temozolomide in glioma cell lines: Molecular mechanisms and potential translational applications

Oncology

Volumn 78, Issue 2, 2010, Pages 103-114

  Zhang, Jihong ^a   Stevens, Malcolm F G ^a   Laughton, Charles A ^a   Madhusudan, Srinivasan ^a   Bradshaw, Tracey D ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Base excision repair; Glioblastoma multiforme; Methylguanine methyl transferase; Mismatch repair; Resistance; Temozolomide

Indexed keywords

5 (3 METHYLTRIAZENE 1 YL) IMIDAZOLE 4 CARBOXAMIDE; 6 O BENZYLGUANINE; 8 HYDROXY 2 METHYL 4(3H) QUINAZOLINONE; ANTINEOPLASTIC AGENT; DNA BINDING PROTEIN; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; MITOZOLOMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NTH ENDONUCLEASE 3 LIKE 1 PROTEIN; TEMOZOLOMIDE; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL CYCLE; CELL LYSATE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CROSS RESISTANCE; DOWN REGULATION; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; EXCISION REPAIR; GLIOMA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; MISMATCH REPAIR; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR GROWTH; UPREGULATION; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS, ALKYLATING; CELL CYCLE; CELL LINE, TUMOR; DACARBAZINE; DNA REPAIR; DNA, NEOPLASM; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG RESISTANCE, NEOPLASM; FLOW CYTOMETRY; GLIOBLASTOMA; GLIOMA; HUMANS; NITROGEN MUSTARD COMPOUNDS; O(6)-METHYLGUANINE-DNA METHYLTRANSFERASE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; QUINAZOLINES; TUMOR STEM CELL ASSAY;

EID: 77950059191     PISSN: 00302414     EISSN: None     Source Type: Journal    
DOI: 10.1159/000306139     Document Type: Article

References (50)

1. Newlands ES, O'Reilly SM, Glaser MG, Bower M, Evans H, Brock C, Brampton MH, Colquhoun I, Lewis P, Rice-Edwards JM, Il-lingworth RD, Richards PG: The Charing Cross Hospital experience with temozolomide in patients with gliomas. Eur J Cancer 1996; 32A: 2236-2241.
2. Chakravarti A, Erkkinen MG, Nestler U, Stupp R, Mehta M, Aldape K, Gilbert MR, Black PM, Loeffler JS: Temozolomide-mediated radiation enhancement in glioblastoma: a report on underlying mechanisms. Clin Cancer Res 2007; 12: 4738-4746.
3. Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO: Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005; 352: 987-996.
4. Vaupel P, Kallinowski F, Okunieff P: Blood flow, oxygen and nutrient supply and metabolic microenvironment of human tumors: a review. Can Res 1989; 49: 6449-6465.
5. Denny BJ, Wheelhouse RT, Stevens MF, Tsang LL, Slack JA: NMR and molecular modeling investigation of the mechanism of activation of the antitumor drug temozolomide and its interaction with DNA. Biochemistry 1994; 33: 9045-9051.
6. Kyrtopoulos SA, Anderson LM, Chhabra SK, Souliotis VL, Pletsa V, Valavanis C, Georgiadis P: DNA adducts and the mechanism of carcinogenesis and cytotoxicity of methylating agents of environmental and clinical significance. Cancer Detect and Prev 1997; 21: 391-405.
7. Margison GP, Santibanez-Koref MF: O-6-alkylguanine-DNA alkyltransferase: role in carcinogenesis and chemotherapy. Bioessays 2002; 24: 255-266.
8. D'Atri S, Tentori L, Lacal PM, Graziani G, Pagani E, Benincasa E, Zambruno G, Bonmassar E, Jiricny J: Involvement of the mismatch repair system in temozolomide-induced apoptosis. Mol Pharmacol 1998; 54: 334-341.
9. Pieper RO: Understanding and manipulating O6-methylguanine-DNA methyltransferase expression. Pharmacol Ther 1997; 74: 285-297.
10. Silber JR, Blank A, Bobola MS, Ghatan S, Kolstoe DD, Berger MS: O6-methylguanine-DNA methyltransferase-deficient phenotype in human gliomas: frequency and time to tumor progression after alkylating agentbased chemotherapy. Clin Cancer Res 1999; 5: 807-814.
11. Hegi ME, Diserens A, Gorlia T, Hamou M, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JEC, Hau P, Mirimanoff RO, Cairncross JG, Janzer RC, Stupp R: MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005; 352: 997-1003.
12. Stupp R, van den Bent MJ, Hegi ME: Optimal role of temozolomide in the treatment of malignant gliomas. Curr Neurol Neurosci Rep 2005; 5: 198-206.
13. Bobola MS, Tseng SH, Blank A, Berger MS, Silber JR: Role of O6-methylguanine-DNA methyltransferase in resistance of human brain tumor cell lines to the clinically relevant methylating agents temozolomide and streptozotocin. Clin Cancer Res 1996; 2: 735-741.
14. Hegi ME, Diserens A-C, Godard S, Dietrich P-Y, Regli L, Ostermann S, Otten P, Van Melle G, de Tribolet N, Stupp R: Clinical trial substantiates the predictive value of O-6-methylguanine-DNA methyltransferase promoter methylation in glioblastoma patients treated with temozolomide. Clin Cancer Res 2004; 10: 1871-1874.
15. Dolan ME, Moschel RC, Pegg AE: Depletion of mammalian O6-alkylguanine-DNA alkyltransferase activity by O6-benzylguanine provides a means to evaluate the role of this protein in protection against carcinogenic and therapeutic alkulating agents. Proc Natl Acad SciUSA 1990; 87: 5368-5372.
16. Clemons M, Kelly J, Watson AJ, Howell A, McElhinney RS, McMurry TBH, Margison GP: O6-(4-bromothenyl) guanine reverses temozolomide resistance in human breast tumor MCF-7 cells and xenografts. Brit J Can 2005; 93: 1152-1156.
17. Gerson SL: Clinical relevance of MGMT in the treatment of cancer. J Clin Oncol 2002; 20: 2388-2399.
18. Esteller M, Herman JG: Generating mutations but providing chemosensitivity: the role of O6-methylguanine DNA methyltransferase in human cancer. Oncogene 2004; 23: 1-8.
19. Karran P, Hampson R: Genomic instability and tolerance to alkylating agents. Cancer Surveys 1996; 28: 69-85.
20. Palombo F, Gallinari P, Iaccarino I, Lettieri T, Hughes M, D'Arrigo A, Truong O, Hsuan JJ, Jiricny J: GTBP, a 160-kilodalton protein essential for mismatch-binding activity in human cells. Science 1995; 268: 1912-1914.
21. Li GM, Modrich P: Restoration of mismatch repair to nuclear extracts of H6 colorectal tumor cells by a heterodimer of human MutL homologs. Proc Natl Acad Sci USA 1995; 92: 1950-1954.
22. Bryant HE, Helleday T: Poly (ADP-ribose) polymerase inhibitors as potential chemotherapeutic agents. Biochem Soc Trans 2004; 32: 959-961.
23. Plummer ER, Middleton MR, Jones C, Olsen A, Hickson I, McHugh P, Margison GP, McGown G, Thorncroft M, Watson AJ, Boddy AV, Calvert AH, Harris AL, Newell DR, Curtin NJ: Temozolomide pharmacodynamics in patients with metastatic melanoma: DNA damage and activity of repair enzymes O6-alkylguanine alkyltransferase and poly (ADP-ribose) polymerase-1. Clin Cancer Res 2005; 11: 3402-3409.
24. Silber JR, Bobola MS, Blank A, Schoeler KD, Haroldson PD, Huynh MB, Kolstoe DD: The Apurinic/Apyrimidinic Endonuclease Activity of Ape1/Ref-1 Contributes to Human Glioma Cell Resistance to Alkylating Agents and Is Elevated by Oxidative Stress. Clin Cancer Res 2002; 8: 3008-3018.
25. Bobola MS, Blank A, Berger MS, Stevens BA, Silber JR: Apurinic/apyrimidinic endonuclease activity is elevated in huma n adult gliomas. Clin Can Res 2001; 7: 3510-3518.
26. Longley DB, Johnston PG: Molecular mechanisms of drug resistance. J Pathol 2005; 205: 275-292.
27. Nicoletti I, Migliorati G, Pagliacci MC, Grignani F, Riccardi C: A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J Immunol Methods 1991; 139: 271-279.
28. Brown JM, Wouters BG: Apoptosis, p53, and tumor cell sensitivity to anticancer agents. Cancer Res 1999; 59: 1391-1399.
29. Bradford MM: A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248-254.s
30. Passagne I, Evrard A, Winum JY, Depeille P, Cuq P, Montero JL, Cupissol D, Vian L: Cytotoxicity, DNA damage, and apoptosis induced by new fotemustine analogs on human melanoma cells in relation to O6-methylguanine DNA-methyltransferase expression. J Pharmacol Exp Ther 2003; 307: 816-823.
31. Zhang Q-M, Yonekura S-I, Takao M, Yasui A, Sugiyama H, Yonei S: DNA glycosylase activities for thymine residues oxidized in the methyl group are functions of the hNEIL1 and hNTH1 enzymes in human cells. DNA Repair 2005; 4: 71-79.
32. Hiramoto T, Nakanishi T, Sumiyoshi T, Fukuda T, Matsuura S, Tauchi H, Komatsu K, Shibasaki Y, Inui H, Watatani M, Yasutomi M, Sumii K, Kajiyama G, Kamada N, Miyagawa K, Kamiya K: Mutations of a novel human RAD54 homologue, RAD54B, inpr imary cancer. Oncogene 1999; 18: 3422-3425.
33. Fritz G, Tano K, Mitra S, Kaina B. Inducibility of the DNA repair gene encoding O6-methylguanine-DNA methyltransferase in mammalian cells by DNA-damaging treatments. Mol Cell Biol 1991; 11: 4660-4668.
34. Alvino E, Castiglia D, Capora li S, Pepponi R, Caporaso P, Lacal PM, Marra G, Fischer F, Zambruno G, Bonmassar E, Jiricny J D'Atri S: A single cycle of treatment with temozolomide, alone or combined with O-6-benzylguanine, induces strong chemoresistance in melanoma cell clones in vitro: role of O-6-methylguanine-DNA methyltransferase and the mismatch repair system. Int J Oncol 2006; 29: 785-797.
35. Margison GP, Povey AC, Kaina B, Santibanez Koref MF: Variability and regulation of O6-alkylguanine-DNA alkyltransferase. Carcinogenesis 2003; 24: 625-635.
36. Pegg AE, Dolan ME, Moschel RC: Structure, function, and inhibition of O6-alkylguanine-DNA alkyltransferase. Prog Nucleic Acid Res Mol Biol 1995; 51: 167-223.
37. Bearzatto A, Szadkowski M, Macpherson P, Jiricny J, Karran P: Epigenetic regulation of the MGMT and hMSH6 DNA repair genes in cells resistant to methylating agents. Cancer Res 200 0; 60: 3262-3270.
38. Cahill DP, Levine KK, Betensky RA, Codd PJ, Romany CA, Reavie LB, Batchelor TT, Futreal PA, Stratton MR, Curry WT, Iafrate AJ, Louis DN: Loss of the mismatch repair protein MSH6 in human glioblastomas is associated with tumor progression during temozolomide treatment. Clin Cancer Res 2007; 13: 2038-2045.
39. Wiew rodt D, Nagel G, Dreimuller N, Hundsberger T, Perneczky A, Kaina B: MGMT in primary and recurrent human glioblastomas after radiation and chemotherapy and comparison with p53 status and clinical outcome. Int J Can 2008; 122: 1391-1399.
40. Liu L, Gerson SL: Targeted modulation of MGMT: clinical implications. Clin Can Res 2006; 12: 328-331.
41. Liu L, Markowitz S, Gerson SL: Mismatch repair mutations override alkyltransferase in conferring resistance to temozolomide but not to 1, 3-bis (2-chloroethyl) nitrosourea. Cancer Res 1996; 56: 5375-5379.
42. Humbert O, Fiumicino S, Aquilina G, Branch P, Oda S, Zijno A, Karran P, Bignami M: Mismatch repair and differential sensitivity of mouse and human cells to methylating agents. Carcinogenesis 1999; 20: 205-214.
43. Fishel R, Wilson T: MutS homologs in mammalian cells. Curr Opin Gen Dev 1997; 7: 105-113.
44. Umar A, Koi M, Risinger JI, Glaab WE, Tindall KR, Kolodner RD, Boland CR, Barrett JC, Kunkel TA: Correction of hypermutability, N-methyl-N'-nitro-N- nitrosoguanidine resistance, and defective DNA mismatch repair by introducing chromosome 2 into human tumor cells with mutations in MSH2 and MSH6. Cancer Res 1997; 57: 3949-3955.
45. Auger N, Thillet J, Wanherdrick K, Idbaih A, Legrier M-E, Dutrillaux B, Sanson M, Poupon M-F: Genetic alterations associated with acquired temozolomide resistance in SNB-19, a human glioma cell line. Mol Can Ther 2006; 5: 12182-2192.
46. Bisgaard ML, Jäger AC, Dalgaard P, øndergaard JO, Rehfeld JF, Nielson FC: Allelic loss of chromosome 2p21-16.3 is associated with reduced survival in sporadic colorectal cancer. Scan J Gastroenterol 2001; 36: 405-409.
47. Hunter C, Smith R, Cahill DP et al: A hypermutation phenotype and somatic MSH6 mutations in recurrent human malignant gliomas after alkylator chemotherapy. Can Res 2006; 66: 3987-3991.
48. Sobol RW, Horton JK, Kuhn R, Gu H, Singhal RK, Prasad R, Rajewsky K, Wilson SH: Requirement of mammalian DNA polymerase-beta in base-excision repair. Nature 1996; 379: 183-186.
49. Curtin NJ, Wang L-Z, Yiakouvaki A, Kyle S, Arris CA, Canan-Koch S, Webber SE, Durkacz B, Calvert HA, Hoscomsky Z, Newell DR: Novel poly (ADP-ribose) polymerase-1 inhibitor, AG14361, restores sensitivity to temozolomide in mismatch repair-deficient cel ls. Clin Can Res 2004; 10 : 881-889.
50. Tentori L, Grazianin G: Recent approaches to improve the antitumor efficacy of temozolomide. Curr Med Chem 2009; 16: 245-257.