Prognostic value of O6-methylguanine-DNA methyltransferase status in glioblastoma patients, assessed by five different methods

Journal of Neuro-Oncology

Volumn 97, Issue 3, 2010, Pages 311-322

  Karayan Tapon, Lucie ^a,b,c   Quillien, Véronique ^d,e   Guilhot, Joëlle ^a,c,f   Wager, Michel ^b,c   Fromont, Gaëlle ^b   Saikali, Stephan ^g   Etcheverry, Amandine ^h   Hamlat, Abderrahmane ^g   Loussouarn, Delphine ⁱ   Campion, Loïc ^j   Campone, Mario ^j,k   Vallette, François Marie ^l   Gratas Rabbia Re, Catherine ^i,l  

^a Centre National de la Recherche Scientifique   (France)

^b UNIVERSITÉ DE POITIERS   (France)

^c POITIERS UNIVERSITY HOSPITAL   (France)

^d CENTRE EUGÈNE MARQUIS   (France)

^e UNIVERSITÉ DE RENNES 1   (France)

^f INSERM   (France)

^g RENNES UNIVERSITY HOSPITAL   (France)

^h Parc Scientifique de Luminy   (France)

ⁱ NANTES UNIVERSITY HOSPITAL   (France)

^j CRLCC René Gauducheau   (France)

^k Team 12   (France)

^l UNIVERSITÉ DE NANTES   (France)

more..

Author keywords

Glioblastoma; MGMT methylation; Overall survival; Temozolomide

Indexed keywords

CARMUSTINE; DNA; FOTEMUSTINE; LOMUSTINE; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; PROCARBAZINE; RNA; TEMOZOLOMIDE; VINCRISTINE; DNA METHYLTRANSFERASE; MGMT PROTEIN, HUMAN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; TUMOR SUPPRESSOR PROTEIN;

ADULT; AGED; ARTICLE; CANCER ADJUVANT THERAPY; CPG ISLAND; DNA METHYLATION; FEMALE; GENE EXPRESSION; GLIOBLASTOMA; HUMAN; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; METHYL SPECIFIC POLYMERASE CHAIN REACTION; OVERALL SURVIVAL; POLYMERASE CHAIN REACTION; PROGNOSIS; PROGRESSION FREE SURVIVAL; PROMOTER REGION; PROTEIN EXPRESSION; PYROSEQUENCING; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SURVIVAL TIME; CLINICAL TRIAL; ENZYMOLOGY; GENETICS; KAPLAN MEIER METHOD; METABOLISM; MIDDLE AGED; MORTALITY; MULTICENTER STUDY; NONPARAMETRIC TEST; PROBABILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIME;

ADULT; AGED; AGED, 80 AND OVER; DNA METHYLATION; DNA MODIFICATION METHYLASES; DNA REPAIR ENZYMES; FEMALE; GLIOBLASTOMA; HUMANS; KAPLAN-MEIERS ESTIMATE; MALE; MIDDLE AGED; PROBABILITY; PROGNOSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STATISTICS, NONPARAMETRIC; TIME FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 77953291279     PISSN: 0167594X     EISSN: 15737373     Source Type: Journal    
DOI: 10.1007/s11060-009-0031-1     Document Type: Article

References (47)

1. 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 et al (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987-996
2. Drablos F, Feyzi E, Aas PA, Vaagbo CB, Kavli B, Bratlie MS, Pena-Diaz J, Otterlei M, Slupphaug G, Krokan HE (2004) Alkylation damage in DNA and RNA-repair mechanisms and medical significance. DNA Repair (Amst) 3:1389-1407. doi: 10.1016/j.dnarep.2004.05.004 (Pubitemid 39221738)
3. Esteller M, Garcia-Foncillas J, Andion E, Goodman SN, Hidalgo OF, Vanaclocha V, Baylin SB, Herman JG (2000) Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N Engl J Med 343:1350-1354
4. Criniere E, Kaloshi G, Laigle-Donadey F, Lejeune J, Auger N, Benouaich-Amiel A, Everhard S, Mokhtari K, Polivka M, Delattre JY, Hoang-Xuan K, Thillet J et al (2007) MGMT prognostic impact on glioblastoma is dependent on therapeutic modalities. J Neurooncol 83:173-179. doi:10.1007/s11060-006-9320-0 (Pubitemid 46784990)
5. Donson AM, Addo-Yobo SO, Handler MH, Gore L, Foreman NK (2007) MGMT promoter methylation correlates with survival benefit and sensitivity to temozolomide in pediatric glioblastoma. Pediatr Blood Cancer 48:403-407. doi:10.1002/pbc.20803 (Pubitemid 46340105)
6. Hegi ME, Diserens AC, Godard S, Dietrich PY, Regli L, Ostermann S, Otten P, Van Melle G, de Tribolet N, Stupp R (2004) Clinical trial substantiates the predictive value of O-6-methylguanine- DNA methyltransferase promoter methylation in glioblastoma patients treated with temozolomide. Clin Cancer Res 10:1871-1874
7. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, Bromberg JE, Hau P et al (2005) MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 352:997-1003
8. Watanabe T, Katayama Y, Komine C, Yoshino A, Ogino A, Ohta T, Fukushima T (2005) O6-Methylguanine-DNA methyltransferase methylation and TP53 mutation in malignant astrocytomas and their relationships with clinical course. Int J Cancer 113:581-587. doi:10.1002/ijc.20625 (Pubitemid 40038734)
9. Eoli M, Menghi F, Bruzzone MG, De Simone T, Valletta L, Pollo B, Bissola L, Silvani A, Bianchessi D, D'Incerti L, Filippini G, Broggi G et al (2007) Methylation of O6-methylguanine DNA methyltransferase and loss of heterozygosity on 19q and/or 17p are overlapping features of secondary glioblastomas with prolonged survival. Clin Cancer Res 13:2606-2613
10. Paz MF, Yaya-Tur R, Rojas-Marcos I, Reynes G, Pollan M, Aguirre-Cruz L, Garcia-Lopez JL, Piquer J, Safont MJ, Balana C, Sanchez-Cespedes M, Garcia-Villanueva M et al (2004) CpG island hypermethylation of the DNA repair enzyme methyltransferase predicts response to temozolomide in primary gliomas. Clin Cancer Res 10:4933-4938
11. 6-methylguanine- DNA methyltransferase methylation in serum and tumor DNA predicts response to 1,3-bis(2-chloroethyl)-1-nitrosourea but not to temozolomide plus cisplatin in glioblastoma multiforme. Clin Cancer Res 9:1461-1468
12. Blanc JL, Wager M, Guilhot J, Kusy S, Bataille B, Chantereau T, Lapierre F, Larsen CJ, Karayan-Tapon L (2004) Correlation of clinical features and methylation status of MGMT gene promoter in glioblastomas. J Neurooncol 68:275-283. doi:10.1023/ B:NEON.0000033385.37098.85
13. 6- methylguanine-deoxyribonucleic acid methyltransferase gene and prognosis in patients with high-grade astrocytic tumors treated with surgery, radiotherapy, and 1-(4-amino-2-methyl-5-pyrimidinyl) methyl-3-(2-chloroethyl)-3-nitrosourea- based chemotherapy. Neurosurgery 54:349-357
14. Gorlia T, van den Bent MJ, Hegi ME, Mirimanoff RO, Weller M, Cairncross JG, Eisenhauer E, Belanger K, Brandes AA, Allgeier A, Lacombe D, Stupp R (2008) Nomograms for predicting survival of patients with newly diagnosed glioblastoma: prognostic factor analysis of EORTC and NCIC trial 26981-22981/CE.3. Lancet Oncol 9:29-38. doi:10.1016/S1470-2045(07)70384-4
15. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, Ludwin SK, Allgeier A, Fisher B, Belanger K, Hau P, Brandes AA et al (2009) 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 10:459-466. doi:10.1016/S1470-2045(09)70025-7
16. Mineura K, Yanagisawa T, Watanabe K, Kowada M, Yasui N (1996) Human brain tumor O(6)-methylguanine-DNA methyltransferase mRNA and its significance as an indicator of selective chloroethylnitrosourea chemotherapy. Int J Cancer 69:420-425
17. Rolhion C, Penault-Llorca F, Kemeny JL, Kwiatkowski F, Lemaire JJ, Chollet P, Finat-Duclos F, Verrelle P (1999) O(6)- Methylguanine-DNA methyltransferase gene (MGMT) expression in human glioblastomas in relation to patient characteristics and p53 accumulation. Int J Cancer 84:416-420
18. 6-Methylguanine-DNA methyltranspherase gene expression in gliomas by means of real-time quantitative RT-PCR and clinical response to nitrosoureas. Int J Cancer 103:67-72. doi:10.1002/ijc.10757 (Pubitemid 35424207)
19. 6-methylguanine-DNA methyltransferase gene expression in gliomas by platinum compounds. Oncol Rep 14:1275-1280
20. 6-methylguanine-DNA methyltransferase gene messenger RNA in gliomas by means of real-time RTPCR and clinical response to nitrosoureas. Cell Mol Neurobiol 25:1067-1071. doi:10.1007/s10571-005-8475-0 (Pubitemid 43154828)
21. Anda T, Shabani HK, Tsunoda K, Tokunaga Y, Kaminogo M, Shibata S, Hayashi T, Iseki M (2003) Relationship between expression of O6-methylguanine-DNA methyltransferase, glutathione- S-transferase pi in glioblastoma and the survival of the patients treated with nimustine hydrochloride: an immunohistochemical analysis. Neurol Res 25:241-248. doi:10.1179/ 016164103101201445 (Pubitemid 36520478)
22. Capper D, Mittelbronn M, Meyermann R, Schittenhelm J (2008) Pitfalls in the assessment of MGMT expression and in its correlation with survival in diffuse astrocytomas: proposal of a feasible immunohistochemical approach. Acta Neuropathol 115:249-259. doi:10.1007/s00401-007-0310-x
23. 6-methylguanine- DNA methyltransferase and survival in inope diagnosed glioblastoma patients treated with neoadjuvant temozolomide. J Clin Oncol 25:1470-1475. doi:10.1200/JCO. 2006.07.4807
24. 6-methylguanine-DNA methyltransferase in the non-neoplastic and neoplastic components of gliomas. J Neurooncol 70:333-340. doi:10.1007/s11060- 004-9170-6 (Pubitemid 40057961)
25. 6-Methylguanine-DNA methyltransferase expression strongly correlates with outcome in childhood malignant gliomas: results from the CCG-945 Cohort. J Clin Oncol 24:3431-3437. doi:10.1200/JCO.2006.05.7265 (Pubitemid 46638900)
26. Rodriguez FJ, Thibodeau SN, Jenkins RB, Schowalter KV, Caron BL, O'Neill BP, David James C, Passe S, Slezak J, Giannini C (2008) MGMT immunohistochemical expression and promoter methylation in human glioblastoma. Appl Immunohistochem Mol Morphol 16:59-65
27. Grasbon-Frodl EM, Kreth FW, Ruiter M, Schnell O, Bise K, Felsberg J, Reifenberger G, Tonn JC, Kretzschmar HA (2007) Intratumoral homogeneity of MGMT promoter hypermethylation as demonstrated in serial stereotactic specimens from anaplastic astrocytomas and glioblastomas. Int J Cancer 121:2458-2464. doi:10.1002/ijc.23020 (Pubitemid 350022415)
28. 6-methylguanine-methyltransferase (MGMT) immunohistochemistry in glioblastoma multiforme: observer variability and lack of association with patient survival impede its use as clinical biomarker. Brain Pathol 18:520-532. doi:10.1111/j.1750-3639.2008.00153.x
29. Stupp R, Hegi ME (2007) Methylguanine methyltransferase testing in glioblastoma: when and how? J Clin Oncol 25:1459- 1460. doi:10.1200/JCO.2006.09. 7139 (Pubitemid 46733069)
30. Kagan J, Srivastava S, Barker PE, Belinsky SA, Cairns P (2007) Towards clinical application of methylated DNA sequences as cancer biomarkers: a joint NCI's EDRN and NIST workshop on standards, methods, assays, reagents and tools. Cancer Res 67:4545-4549
31. Preusser M (2009) MGMT analysis at DNA, RNA and protein levels in glioblastoma tissue. Histol Histopathol 24:511-518
32. Palmisano WA, Divine KK, Saccomanno G, Gilliland FD, Baylin SB, Herman JG, Belinsky SA (2000) Predicting lung cancer by detecting aberrant promoter methylation in sputum. Cancer Res 60:5954-5958
33. Fackler MJ, McVeigh M, Mehrotra J, Blum MA, Lange J, Lapides A, Garrett E, Argani P, Sukumar S (2004) Quantitative multiplex methylation-specific PCR assay for the detection of promoter hypermethylation in multiple genes in breast cancer. Cancer Res 64:4442-4452 (Pubitemid 38856915)
34. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408. doi:10.1006/meth. 2001.1262
35. Concin N, Becker K, Slade N, Erster S, Mueller-Holzner E, Ulmer H, Daxenbichler G, Zeimet A, Zeillinger R, Marth C, Moll UM (2004) Transdominant DeltaTAp73 isoforms are frequently up-regulated in ovarian cancer. Evidence for their role as epigenetic p53 inhibitors in vivo. Cancer Res 64:2449-2460
36. Wager M, Guilhot J, Blanc JL, Ferrand S, Milin S, Bataille B, Lapierre F, Denis S, Chantereau T, Larsen CJ, Karayan-Tapon L (2006) Prognostic value of increase in transcript levels of Tp73 DeltaEx2-3 isoforms in low-grade glioma patients. Br J Cancer 95:1062-1069. doi:10.1038/sj.bjc.6603410 (Pubitemid 44608169)
37. 6-methylguanine-DNA methyltransferase gene promoter methylation in glioma. J Mol Diagn 10:332-337. doi:10.2353/jmoldx.2008.070169 (Pubitemid 352019119)
38. 6-methylguanine- DNA methyltransferase (MGMT) gene expression in human cancer. Oncogene 22:8835-8844. doi:10.1038/sj.onc.1207183
39. 6-methylguanine-DNA methyltransferase determined by promoter hypermethylation and immunohistochemical expression in anaplastic gliomas. Clin Cancer Res 11:5167-5174
40. Cahill DP, Levine KK, Betensky RA, Codd PJ, Romany CA, Reavie LB, Batchelor TT, Futreal PA, Stratton MR, Curry WT, Iafrate AJ, Louis DN (2007) Loss of the mismatch repair protein MSH6 in human glioblastomas is associated with tumor progression during temozolomide treatment. Clin Cancer Res 13: 2038-2045
41. Grombacher T, Mitra S, Kaina B (1996) Induction of the alkyltransferase (MGMT) gene by DNA damaging agents and the glucocorticoid dexamethasone and comparison with the response of base excision repair genes. Carcinogenesis 17:2329-2336
42. Shen L, Kondo Y, Rosner GL, Xiao L, Hernandez NS, Vilaythong J, Houlihan PS, Krouse RS, Prasad AR, Einspahr JG, Buckmeier J, Alberts DS et al (2005) MGMT promoter methylation and field defect in sporadic colorectal cancer. J Natl Cancer Inst 97:1330-1338. doi:10.1093/jnci/dji275 (Pubitemid 41487800)
43. Maxwell JA, Johnson SP, Quinn JA, McLendon RE, Ali-Osman F, Friedman AH, Herndon JE II, Bierau K, Bigley J, Bigner DD, Friedman HS (2006) Quantitative analysis of O6-alkylguanine- DNA alkyltransferase in malignant glioma. Mol Cancer Ther 5:2531-2539. doi:10.1158/1535-7163.MCT-06-0106 (Pubitemid 44650917)
44. Hattermann K, Mehdorn HM, Mentlein R, Schultka S, Held-Feindt J (2008) A methylation-specific and SYBR-green-based quantitative polymerase chain reaction technique for O(6)- methylguanine DNA methyltransferase promoter methylation analysis. Anal Biochem 377:62-71. doi:10.1016/j.ab.2008.03.014
45. Tayrac MD, Etcheverry A, Aubry M, Saikali S, Hamlat A, Quillien V, Treut AL, Galibert MD, Mosser J (2008) Integrative genomewide analysis reveals a robust genomic glioblastoma signature associated with copy number driving changes in gene expression. Genes Chromosomes Cancer 48:55-68. doi:10.1002/gcc.20618
46. Mikeska T, Bock C, El-Maarri O, Hubner A, Ehrentraut D, Schramm J, Felsberg J, Kahl P, Buttner R, Pietsch T, Waha A (2007) Optimization of quantitative MGMT promoter methylation analysis using pyrosequencing and combined bisulfite restriction analysis. J Mol Diagn 9:368-381. doi:10.2353/jmoldx. 2007.060167
47. Dunn J, Baborie A, Alam F, Joyce K, Moxham M, Sibson R, Crooks D, Husband D, Shenoy A, Brodbelt A, Wong H, Liloglou T, Haylock B, Walker C (2009) Extent of MGMT promoter methylation correlates with outcome in glioblastomas given temozolomide and radiotherapy. Br J Cancer 16:1-8. doi: 10.1038/sj.bjc.6605127