Epigenetic modulation of the drug resistance genes MGMT, ABCB1 and ABCG2 in glioblastoma multiforme

BMC Cancer

Volumn 13, Issue , 2013, Pages

  Oberstadt, Moritz C ^a   Bien Möller, Sandra ^a   Weitmann, Kerstin ^a   Herzog, Susann ^a   Hentschel, Katharina ^a   Rimmbach, Christian ^a   Vogelgesang, Silke ^a   Balz, Ellen ^a   Fink, Matthias ^a   Michael, Heike ^a   Zeden, Jan Philip ^a   Bruckmüller, Henrike ^b   Werk, Anneke N ^b   Cascorbi, Ingolf ^b   Hoffmann, Wolfgang ^a   Rosskopf, Dieter ^a   Schroeder, Henry W S ^a   Kroemer, Heyo K ^a  

^a UNIVERSITY OF GREIFSWALD   (Germany)

^b UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

Author keywords

DNA methylation; Drug resistance; Glioblastoma multiforme; MGMT

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; CYTOSINE; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; MULTIDRUG RESISTANCE PROTEIN 1; TEMOZOLOMIDE; THYMINE;

ABCB1 GENE; ABCG2 GENE; ADULT; AGED; ARTICLE; CANCER PROGNOSIS; CANCER RADIOTHERAPY; EPIGENETICS; FEMALE; GENE EXPRESSION; GENE FREQUENCY; GENETIC CORRELATION; GENOTYPE; GLIOBLASTOMA; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MGMT GENE; NUCLEOTIDE SEQUENCE; OVERALL SURVIVAL; PROMOTER REGION; PROTEIN METHYLATION; PYROSEQUENCING; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; SINGLE NUCLEOTIDE POLYMORPHISM; TUMOR GENE;

ADULT; AGED; ATP-BINDING CASSETTE TRANSPORTERS; BRAIN NEOPLASMS; DNA METHYLATION; DNA MODIFICATION METHYLASES; DNA REPAIR ENZYMES; DRUG RESISTANCE, NEOPLASM; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION; GLIOBLASTOMA; HUMANS; MALE; MIDDLE AGED; NEOPLASM PROTEINS; P-GLYCOPROTEIN; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC; RECURRENCE; TUMOR SUPPRESSOR PROTEINS;

EID: 84891352564     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-13-617     Document Type: Article

References (44)

1. Piperi C, Themistocleous MS, Papavassiliou GA, Farmaki E, Levidou G, Korkolopoulou P, Adamopoulos C, Papavassiliou AG. High incidence of MGMT and RARbeta promoter methylation in primary glioblastomas: association with histopathological characteristics, inflammatory mediators and clinical outcome. Mol Med 2010, 16(1-2):1-9. 2757033, 19809523.
2. Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007, 114(2):97-109. 10.1007/s00401-007-0243-4, 1929165, 17618441.
3. Reifenberger G, Collins VP. Pathology and molecular genetics of astrocytic gliomas. J Mol Med 2004, 82(10):656-670. 10.1007/s00109-004-0564-x, 15316624.
4. Rich JN, Hans C, Jones B, Iversen ES, McLendon RE, Rasheed BK, Dobra A, Dressman HK, Bigner DD, Nevins JR, et al. Gene expression profiling and genetic markers in glioblastoma survival. Cancer Res 2005, 65(10):4051-4058. 10.1158/0008-5472.CAN-04-3936, 15899794.
5. Bleau AM, Huse JT, Holland EC. The ABCG2 resistance network of glioblastoma. Cell Cycle 2009, 8(18):2936-2944.
6. Hegi ME, Diserens AC, Gorlia T, Hamou MF, de Tribolet N, Weller M, Kros JM, Hainfellner JA, Mason W, Mariani L, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005, 352(10):997-1003. 10.1056/NEJMoa043331, 15758010.
7. Demeule M, Shedid D, Beaulieu E, del Maestro RF, Moghrabi A, Ghosn PB, Moumdjian R, Berthelet F, Beliveau R. Expression of multidrug-resistance P-glycoprotein (MDR1) in human brain tumors. Int J Cancer 2001, 93(1):62-66. 10.1002/ijc.1306, 11391622.
8. Nakayama M, Wada M, Harada T, Nagayama J, Kusaba H, Ohshima K, Kozuru M, Komatsu H, Ueda R, Kuwano M. Hypomethylation status of CpG sites at the promoter region and overexpression of the human MDR1 gene in acute myeloid leukemias. Blood 1998, 92(11):4296-4307.
9. Nakano H, Nakamura Y, Soda H, Kamikatahira M, Uchida K, Takasu M, Kitazaki T, Yamaguchi H, Nakatomi K, Yanagihara K, et al. Methylation status of breast cancer resistance protein detected by methylation-specific polymerase chain reaction analysis is correlated inversely with its expression in drug-resistant lung cancer cells. Cancer 2008, 112(5):1122-1130. 10.1002/cncr.23285, 18219662.
10. Jiang ZP, Xu P, Liu RR, Li HD, Wang GP, Zhao XL, Chen FP. Correlation between MDR1 methylation status in the promoter region and MDR1 genetic polymorphism in 194 healthy Chinese Han subjects. Pharmacogenomics 2008, 9(12):1801-1808. 10.2217/14622416.9.12.1801, 19072639.
11. Imai Y, Nakane M, Kage K, Tsukahara S, Ishikawa E, Tsuruo T, Miki Y, Sugimoto Y. C421A polymorphism in the human breast cancer resistance protein gene is associated with low expression of Q141K protein and low-level drug resistance. Mol Cancer Ther 2002, 1(8):611-616.
12. Morisaki K, Robey RW, Ozvegy-Laczka C, Honjo Y, Polgar O, Steadman K, Sarkadi B, Bates SE. Single nucleotide polymorphisms modify the transporter activity of ABCG2. Cancer Chemother Pharmacol 2005, 56(2):161-172. 10.1007/s00280-004-0931-x, 15838659.
13. Mikeska T, Bock C, El-Maarri O, Hubner A, Ehrentraut D, Schramm J, Felsberg J, Kahl P, Buttner R, Pietsch T, et al. Optimization of quantitative MGMT promoter methylation analysis using pyrosequencing and combined bisulfite restriction analysis. J Mol Diagn 2007, 9(3):368-381. 10.2353/jmoldx.2007.060167, 1899414, 17591937.
14. Karayan-Tapon L, Quillien V, Guilhot J, Wager M, Fromont G, Saikali S, Etcheverry A, Hamlat A, Loussouarn D, Campion L, et al. Prognostic value of O6-methylguanine-DNA methyltransferase status in glioblastoma patients, assessed by five different methods. J Neurooncol 2010, 97(3):311-322. 10.1007/s11060-009-0031-1, 19841865.
15. Hermes M, Geisler H, Osswald H, Riehle R, Kloor D. Alterations in S-adenosylhomocysteine metabolism decrease O6-methylguanine DNA methyltransferase gene expression without affecting promoter methylation. Biochem Pharmacol 2008, 75(11):2100-2111. 10.1016/j.bcp.2008.02.031, 18395186.
16. Brescia P, Ortensi B, Fornasari L, Levi D, Broggi G, Pelicci G. CD133 is essential for glioblastoma stem cell maintenance. Stem Cells 2013, 31(5):857-869. 10.1002/stem.1317, 23307586.
17. Weller M, Felsberg J, Hartmann C, Berger H, Steinbach JP, Schramm J, Westphal M, Schackert G, Simon M, Tonn JC, et al. Molecular predictors of progression-free and overall survival in patients with newly diagnosed glioblastoma: a prospective translational study of the German Glioma Network. J Clin Oncol 2009, 27(34):5743-5750. 10.1200/JCO.2009.23.0805, 19805672.
18. Esteller M, Garcia-Foncillas J, Andion E, Goodman SN, Hidalgo OF, Vanaclocha V, Baylin SB, Herman JG. Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. N Engl J Med 2000, 343(19):1350-1354. 10.1056/NEJM200011093431901, 11070098.
19. Dunn J, Baborie A, Alam F, Joyce K, Moxham M, Sibson R, Crooks D, Husband D, Shenoy A, Brodbelt A, et al. Extent of MGMT promoter methylation correlates with outcome in glioblastomas given temozolomide and radiotherapy. Br J Cancer 2009, 101(1):124-131. 10.1038/sj.bjc.6605127, 2713697, 19536096.
20. Qian XC, Brent TP. Methylation hot spots in the 5′ flanking region denote silencing of the O6-methylguanine-DNA methyltransferase gene. Cancer Res 1997, 57(17):3672-3677.
21. Watts GS, Pieper RO, Costello JF, Peng YM, Dalton WS, Futscher BW. Methylation of discrete regions of the O6-methylguanine DNA methyltransferase (MGMT) CpG island is associated with heterochromatinization of the MGMT transcription start site and silencing of the gene. Mol Cell Biol 1997, 17(9):5612-5619. 232409, 9271436.
22. Turner JG, Gump JL, Zhang C, Cook JM, Marchion D, Hazlehurst L, Munster P, Schell MJ, Dalton WS, Sullivan DM. ABCG2 expression, function, and promoter methylation in human multiple myeloma. Blood 2006, 108(12):3881-3889. 10.1182/blood-2005-10-009084, 1895461, 16917002.
23. To KK, Zhan Z, Bates SE. Aberrant promoter methylation of the ABCG2 gene in renal carcinoma. Mol Cell Biol 2006, 26(22):8572-8585. 10.1128/MCB.00650-06, 1636795, 16954373.
24. McDonald KL, Rapkins RW, Olivier J, Zhao L, Nozue K, Lu D, Tiwari S, Kuroiwa-Trzmielina J, Brewer J, Wheeler HR, et al. The T genotype of the MGMT C>T (rs16906252) enhancer single-nucleotide polymorphism (SNP) is associated with promoter methylation and longer survival in glioblastoma patients. Eur J Cancer 2013, 49(2):360-368. 10.1016/j.ejca.2012.08.012, 22975219.
25. Ogino S, Hazra A, Tranah GJ, Kirkner GJ, Kawasaki T, Nosho K, Ohnishi M, Suemoto Y, Meyerhardt JA, Hunter DJ, et al. MGMT germline polymorphism is associated with somatic MGMT promoter methylation and gene silencing in colorectal cancer. Carcinogenesis 2007, 28(9):1985-1990. 10.1093/carcin/bgm160, 17621591.
26. Hawkins NJ, Lee JH, Wong JJ, Kwok CT, Ward RL, Hitchins MP. MGMT methylation is associated primarily with the germline C > T SNP (rs16906252) in colorectal cancer and normal colonic mucosa. Mod Pathol 2009, 22(12):1588-1599. 10.1038/modpathol.2009.130, 19734844.
27. Kristensen LS, Nielsen HM, Hager H, Hansen LL. Methylation of MGMT in malignant pleural mesothelioma occurs in a subset of patients and is associated with the T allele of the rs16906252 MGMT promoter SNP. Lung Cancer 2011, 71(2):130-136. 10.1016/j.lungcan.2010.05.008, 20627446.
28. Leng S, Bernauer AM, Hong C, Do KC, Yingling CM, Flores KG, Tessema M, Tellez CS, Willink RP, Burki EA, et al. The A/G allele of rs16906252 predicts for MGMT methylation and is selectively silenced in premalignant lesions from smokers and in lung adenocarcinomas. Clin Cancer Res 2011, 17(7):2014-2023. 10.1158/1078-0432.CCR-10-3026, 3070839, 21355081.
29. Hoffmeyer S, Burk O, von Richter O, Arnold HP, Brockmoller J, Johne A, Cascorbi I, Gerloff T, Roots I, Eichelbaum M, et al. Functional polymorphisms of the human multidrug-resistance gene: multiple sequence variations and correlation of one allele with P-glycoprotein expression and activity in vivo. Proc Natl Acad Sci U S A 2000, 97(7):3473-3478. 10.1073/pnas.97.7.3473, 16264, 10716719.
30. Costa BM, Caeiro C, Guimaraes I, Martinho O, Jaraquemada T, Augusto I, Castro L, Osorio L, Linhares P, Honavar M, et al. Prognostic value of MGMT promoter methylation in glioblastoma patients treated with temozolomide-based chemoradiation: a Portuguese multicentre study. Oncol Rep 2010, 23(6):1655-1662.
31. Martinez R, Martin-Subero JI, Rohde V, Kirsch M, Alaminos M, Fernandez AF, Ropero S, Schackert G, Esteller M. A microarray-based DNA methylation study of glioblastoma multiforme. Epigenetics 2009, 4(4):255-264.
32. Lu C, Shervington A. Chemoresistance in gliomas. Mol Cell Biochem 2008, 312(1-2):71-80.
33. Andersson U, Malmer B, Bergenheim AT, Brannstrom T, Henriksson R. Heterogeneity in the expression of markers for drug resistance in brain tumors. Clin Neuropathol 2004, 23(1):21-27.
34. Schaich M, Kestel L, Pfirrmann M, Robel K, Illmer T, Kramer M, Dill C, Ehninger G, Schackert G, Krex D. A MDR1 (ABCB1) gene single nucleotide polymorphism predicts outcome of temozolomide treatment in glioblastoma patients. Ann Oncol 2009, 20(1):175-181.
35. Derks S, Lentjes MH, Hellebrekers DM, de Bruine AP, Herman JG, van Engeland M. Methylation-specific PCR unraveled. Cell Oncol 2004, 26(5-6):291-299.
36. Christians A, Hartmann C, Benner A, Meyer J, von Deimling A, Weller M, Wick W, Weiler M. Prognostic value of three different methods of MGMT promoter methylation analysis in a prospective trial on newly diagnosed glioblastoma. PLoS One 2012, 7(3):e33449. 10.1371/journal.pone.0033449, 3302822, 22428052.
37. Kristensen LS, Treppendahl MB, Asmar F, Girkov MS, Nielsen HM, Kjeldsen TE, Ralfkiaer E, Hansen LL, Gronbaek K. Investigation of MGMT and DAPK1 methylation patterns in diffuse large B-cell lymphoma using allelic MSP-pyrosequencing. Sci Rep 2013, 3:2789. 3784959, 24071855.
38. Garcia-Manero G, Bueso-Ramos C, Daniel J, Williamson J, Kantarjian HM, Issa JP. DNA methylation patterns at relapse in adult acute lymphocytic leukemia. Clin Cancer Res 2002, 8(6):1897-1903.
39. Gao P, Yang X, Xue YW, Zhang XF, Wang Y, Liu WJ, Wu XJ. Promoter methylation of glutathione S-transferase pi1 and multidrug resistance gene 1 in bronchioloalveolar carcinoma and its correlation with DNA methyltransferase 1 expression. Cancer 2009, 115(14):3222-3232. 10.1002/cncr.24369, 19484794.
40. David GL, Yegnasubramanian S, Kumar A, Marchi VL, de Marzo AM, Lin X, Nelson WG. MDR1 promoter hypermethylation in MCF-7 human breast cancer cells: changes in chromatin structure induced by treatment with 5-Aza-cytidine. Cancer Biol Ther 2004, 3(6):540-548.
41. Enokida H, Shiina H, Igawa M, Ogishima T, Kawakami T, Bassett WW, Anast JW, Li LC, Urakami S, Terashima M, et al. CpG hypermethylation of MDR1 gene contributes to the pathogenesis and progression of human prostate cancer. Cancer Res 2004, 64(17):5956-5962. 10.1158/0008-5472.CAN-04-0081, 15342374.
42. Tahara T, Arisawa T, Shibata T, Yamashita H, Yoshioka D, Hirata I. Effect of promoter methylation of multidrug resistance 1 (MDR1) gene in gastric carcinogenesis. Anticancer Res 2009, 29(1):337-341.
43. Bleau AM, Hambardzumyan D, Ozawa T, Fomchenko EI, Huse JT, Brennan CW, Holland EC. PTEN/PI3K/Akt pathway regulates the side population phenotype and ABCG2 activity in glioma tumor stem-like cells. Cell Stem Cell 2009, 4(3):226-235. 10.1016/j.stem.2009.01.007, 3688060, 19265662.
44. Bady P, Sciuscio D, Diserens AC, Bloch J, van den Bent MJ, Marosi C, Dietrich PY, Weller M, Mariani L, Heppner FL, et al. MGMT methylation analysis of glioblastoma on the Infinium methylation BeadChip identifies two distinct CpG regions associated with gene silencing and outcome, yielding a prediction model for comparisons across datasets, tumor grades, and CIMP-status. Acta Neuropathol 2012, 124(4):547-560. 10.1007/s00401-012-1016-2, 3444709, 22810491.