MGMT DNA repair gene promoter/enhancer haplotypes alter transcription factor binding and gene expression

Cellular Oncology

Volumn 39, Issue 5, 2016, Pages 435-447

  Xu, Meixiang ^a   Cross, Courtney E ^a,b   Speidel, Jordan T ^a   Abdel Rahman, Sherif Z ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b A T STILL UNIVERSITY   (United States)

Author keywords

MGMT P E haplotypes; Promoter activity; siRNA regulation; Transcription factor binding

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; CCAAT ENHANCER BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYTIDINE DIPHOSPHATE; EPIDERMAL GROWTH FACTOR; HEPATOCYTE NUCLEAR FACTOR 4; HYPOXIA INDUCIBLE FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; MYOCYTE ENHANCER FACTOR 2; OCTAMER TRANSCRIPTION FACTOR 4; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PROTEIN P53; SMAD PROTEIN; SMALL INTERFERING RNA; STAT1 PROTEIN; STAT3 PROTEIN; STAT4 PROTEIN; STAT5 PROTEIN; STAT6 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR ETS; TRANSCRIPTION FACTOR GATA; TRANSCRIPTION FACTOR GATA 1; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR PAX5; TRANSCRIPTION FACTOR SP1; TRANSCRIPTION FACTOR YY1; DNA LIGASE; DNA METHYLTRANSFERASE; MGMT PROTEIN, HUMAN; PROTEIN BINDING; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; DNA REPAIR; ENHANCER REGION; GENE EXPRESSION; GLIOBLASTOMA CELL LINE; HAPLOTYPE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; SINGLE NUCLEOTIDE POLYMORPHISM; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHYSIOLOGY; TUMOR CELL LINE;

CELL LINE, TUMOR; DNA MODIFICATION METHYLASES; DNA REPAIR; DNA REPAIR ENZYMES; GENE EXPRESSION REGULATION, NEOPLASTIC; HAPLOTYPES; HUMANS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

EID: 84974801245     PISSN: 22113428     EISSN: 22113436     Source Type: Journal    
DOI: 10.1007/s13402-016-0286-4     Document Type: Article

References (51)

1. R. A. Becker, R. Montesano, Repair of O 4-methyldeoxythymidine residues in DNA by mammalian liver extracts. Carcinogenesis 6, 313–317 (1985)
2. M. Christmann, B. Verbeek, W. P. Roos, B. Kaina, O(6)-methylguanine-DNA methyltransferase (MGMT) in normal tissues and tumors: enzyme activity, promoter methylation and immunohistochemistry. Biochim. Biophys. Acta 1816, 179–190 (2011)
3. D. S. Daniels, T. T. Woo, K. X. Luu, D. M. Noll, N. D. Clarke, A. E. Pegg, J. A. Tainer, DNA binding and nucleotide flipping by the human DNA repair protein AGT. Nat. Struct. Mol. Biol. 11, 714–720 (2004)
4. A. E. Pegg, Mammalian O 6-alkylguanine-DNA alkyltransferase: regulation and importance in response to alkylating carcinogenic and therapeutic agents. Cancer Res. 50, 6119–6129 (1990)
5. P. E. Jackson, C. N. Hall, A. F. Badawi, P. J. O’Connor, D. P. Cooper, A. C. Povey, Frequency of Ki-ras mutations and DNA alkylation in colourectal tissue from individuals living in Manchester. Mol. Carcinog. 16, 12–19 (1996)
6. A. E. Pegg, Repair of O(6)-alkylguanine by alkyltransferases. Mutat. Res. 462, 83–100 (2000)
7. S. L. Gerson, Clinical relevance of MGMT in the treatment of cancer. J. Clin. Oncol. 20, 2388–2399 (2002)
8. S. L. Gerson, MGMT: its role in cancer aetiology and cancer therapeutics. Nat. Rev. Cancer 4, 296–307 (2004)
9. G. P. Margison, M. F. Santibáñez Koref, A. C. Povey, Mechanisms of carcinogenicity/chemotherapy by O6-methylguanine. Mutagenesis 17, 483–487 (2002)
10. G. P. Margison, A. C. Povey, B. Kaina, M. F. Santibáñez Koref, Variability and regulation of O 6-alkylguanine-DNA alkyltransferase. Carcinogenesis 24, 625–635 (2003)
11. J. R. Silber, M. S. Bobola, A. Blank, M. C. Chamberlain, O(6)-methylguanine-DNA methyltransferase in glioma therapy: promise and problems. Biochim. Biophys. Acta 1826, 71–82 (2012)
12. W. Wick, M. Weller, M. van den Bent, M. Sanson, M. Weiler, A. von Deimling, C. Plass, M. Hegi, M. Platten, G. Reifenberger, MGMT testing–the challenges for biomarker-based glioma treatment. Nat. Rev. Neurol. 10(7), 372–385 (2014)
13. B. Kaina, M. Christmann, S. Naumann, W. P. Roos, MGMT: key node in the battle against genotoxicity, carcinogenicity and apoptosis induced by alkylating agents. DNA Repair 6, 1079–1099 (2007)
14. A. E. Pegg, Q. Fang, N. A. Loktionova, Human variants of O6-alkylguanine-DNA alkyltransferase. DNA Repair 6, 1071–1078 (2007)
15. K. K. Bhakat, S. Mitra, CpG methylation-dependent repression of the human O6-methylguanine-DNA methyltransferase gene linked to chromatin structure alteration. Carcinogenesis 24, 1337–1345 (2003)
16. R. P. Danam, S. R. Howell, T. P. Brent, L. C. Harris, Epigenetic regulation of O 6-methylguanine-DNA methyltransferase gene expression by histone acetylation and methyl-CpG binding proteins. Mol. Cancer Ther. 4, 61–69 (2005)
17. M. Krześniak, D. Butkiewicz, A. Samojedny, M. Chorazy, M. Rusin, Polymorphisms in TDG and MGMT genes - epidemiological and functional study in lung cancer patients from Poland. Ann. Hum. Genet. 68, 300–312 (2004)
18. S. Ogino, A. Hazra, G. J. Tranah, G. J. Kirkner, T. Kawasaki, K. Nosho, M. Ohnishi, Y. Suemoto, J. A. Meyerhardt, D. J. Hunter, et al., MGMT germline polymorphism is associated with somatic MGMT promoter methylation and gene silencing in colourectal cancer. Carcinogenesis 28, 1985–1990 (2007)
19. S. Leng, A. M. Bernauer, C. Hong, K. C. Do, C. M. Yingling, K. G. Flores, M. Tessema, C. S. Tellez, R. P. Willink, E. A. Burki, 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. 17, 2014–2023 (2011)
20. K. L. McDonald, R. W. Rapkins, J. Olivier, L. Zhao, K. Nozue, D. Lu, S. Tiwari, J. Kuroiwa-Trzmielina, J. Brewer, H. R. Wheeler, 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 49, 360–368 (2013)
21. M. Xu, I. Nekhayeva, C. E. Cross, C. M. Rondelli, J. K. Wickliffe, S. Z. Abdel-Rahman, Influence of promoter/enhancer region haplotypes on MGMT transcriptional regulation: a potential biomarker for human sensitivity to alkylating agents. Carcinogenesis 35(3), 564–571 (2014)
22. S. E. Johnatty, M. Abdellatif, L. Shimmin, R. B. Clark, E. Boerwinkle, Beta 2 adrenergic receptor 5′ haplotypes influence promoter activity. Br. J. Pharmacol. 137, 1213–1216 (2002)
23. H. Takane, D. Kobayashi, T. Hirota, J. Kigawa, N. Terakawa, K. Otsubo, I. Ieiri, Haplotype-oriented genetic analysis and functional assessment of promoter variants in the MDR1 (ABCB1) gene. J. Pharmacol. Exp. Ther. 311, 1179–1187 (2004)
24. N. J. Hawkins, J. H. Lee, J. J. Wong, C. T. Kwok, R. L. Ward, M. P. Hitchins, MGMT methylation is associated primarily with the germline C > T SNP (rs16906252) in colourectal cancer and normal colonic mucosa. Mod. Pathol. 22, 1588–1599 (2009)
25. I. L. Candiloro, A. Dobrovic, Detection of MGMT promoter methylation in normal individuals is strongly associated with the T allele of the rs16906252 MGMT promoter single nucleotide polymorphism. Cancer Prev. Res. 2, 862–867 (2009)
26. L. S. Kristensen, H. M. Nielsen, H. Hager, L. L. Hansen, 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 71, 130–136 (2011)
27. M. H. Chae, J. S. Jang, H. G. Kang, J. H. Park, J. M. Park, W. K. Lee, S. Kam, E. B. Lee, J. W. Son, J. Y. Park, O6-alkylguanine-DNA alkyltransferase gene polymorphisms and the risk of primary lung cancer. Mol. Carcinog. 45, 239–249 (2006)
28. Z. Hu, H. Wang, M. Shao, G. Jin, W. Sun, Y. Wang, H. Liu, Y. Wang, H. Ma, J. Qian, et al., Genetic variants in MGMT and risk of lung cancer in southeastern Chinese: a haplotype-based analysis. Hum. Mutat. 28, 431–440 (2007)
29. L. Wang, H. Liu, Z. Zhang, M. R. Spitz, Q. Wei, Association of genetic variants of O 6-methylguanine-DNA methyltransferase with risk of lung cancer in non-Hispanic whites. Cancer Epidemiol. Biomark. Prev. 15, 2364–2369 (2006)
30. J. H. Park, N. S. Kim, J. Y. Park, Y. S. Chae, J. G. Kim, S. K. Sohn, J. H. Moon, B. W. Kang, H. M. Ryoo, S. H. Bae, et al., MGMT -535G > T polymorphism is associated with prognosis for patients with metastatic colourectal cancer treated with oxaliplatin-based chemotherapy. J. Cancer Res. Clin. Oncol. 136, 1135–1142 (2010)
31. I. Zawlik, S. Vaccarella, D. Kita, M. Mittelbronn, S. Franceschi, H. Ohgaki, Promoter methylation and polymorphisms of the MGMT gene in glioblastomas: a population-based study. Neuroepidemiology 32, 21–29 (2009)
32. J. Felsberg, M. Rapp, S. Loeser, R. Fimmers, W. Stummer, M. Goeppert, H. J. Steiger, B. Friedensdorf, G. Reifenberger, M. C. Sabel, Prognostic significance of molecular markers and extent of resection in primary glioblastoma patients. Clin. Cancer Res. 15, 6683–6693 (2009)
33. Z. Zhang, L. Wang, S. Wei, Z. Liu, L. E. Wang, E. M. Sturgis, Q. Wei, Polymorphisms of the DNA repair gene MGMT and risk and progression of head and neck cancer. DNA Repair 9, 558–566 (2010)
34. S. B. Gabriel, S. F. Schaffner, H. Nguyen, J. M. Moore, J. Roy, B. Blumenstiel, J. Higgins, M. DeFelice, A. Lochner, M. Faggart, et al., The structure of haplotype blocks in the human genome. Science 296, 2225–2229 (2002)
35. L. C. Harris, P. M. Potter, K. Tano, S. Shiota, S. Mitra, T. P. Brent, Characterization of the promoter region of the human O6-methylguanine-DNA methyltransferase gene. Nucleic Acids Res. 19, 6163–6167 (1991)
36. M. Christmann, B. Kaina, Transcriptional regulation of human DNA repair genes following genotoxic stress: trigger mechanisms, inducible responses and genotoxic adaptation. Nucleic Acids Res. 41, 8403–8420 (2013)
37. X. Messeguer, R. Escudero, D. Farré, O. Nuñez, J. Martínez, M. M. Albà, PROMO: detection of known transcription regulatory elements using species-tailored searches. Bioinformatics 18, 333–334 (2002)
38. D. Farré, R. Roset, M. Huerta, J. E. Adsuara, L. Roselló, M. M. Albà, X. Messeguer, Identification of patterns in biological sequences at the ALGGEN server: PROMO and MALGEN. Nucleic Acids Res. 31, 3651–3653 (2003)
39. A. Yousuf, M. Y. Bhat Arshad, A. Pandith, D. Afroze, N. P. Khan, K. Alam, P. Shah, M. A. Shah, S. Mudassar, MGMT gene silencing by promoter hypermethylation in gastric cancer in a high incidence area. Cell. Oncol. 37, 245–252 (2014)
40. I. Boldogh, C. V. Ramana, Z. Chen, T. Biswas, T. K. Hazra, S. Grösch, T. Grombacher, S. Mitra, B. Kaina, Regulation of expression of the DNA repair gene O6-methylguanine-DNA methyltransferase via protein kinase C-mediated signaling. Cancer Res. 58, 3950–3956 (1998)
41. J. F. Costello, B. W. Futscher, R. A. Kroes, R. O. Pieper, Methylation-related chromatin structure is associated with exclusion of transcription factors from and suppressed expression of the O-6-methylguanine DNA methyltransferase gene in human glioma cell lines. Mol. Cell. Biol. 14, 6515–6521 (1994)
42. I. Lavon, D. Fuchs, D. Zrihan, G. Efroni, B. Zelikovitch, Y. Fellig, T. Siegal, Novel mechanism whereby nuclear factor κB mediates DNA damage repair through regulation of O6-methylguanine-DNA-methyltransferase. Cancer Res. 67, 8952–8959 (2007)
43. L. Persano, F. Pistollato, E. Rampazzo, A. Della Puppa, S. Abbadi, C. Frasson, F. Volpin, S. Indraccolo, R. Scienza, G. Basso, BMP2 sensitizes glioblastoma stem-like cells to temozolomide by affecting HIF-1α stability and MGMT expression. Cell Death Dis. 3, e412 (2012)
44. S. Ueda, T. Mineta, Y. Nakahara, H. Okamoto, T. Shiraishi, K. Tabuchi, Induction of the DNA repair gene O6-methylguanine-DNA methyltransferase by dexamethasone in glioblastomas. J. Neurosurg. 101, 659–663 (2004)
45. K. K. Bhakat, S. Mitra, Regulation of the human O6-methylguanine-DNA methyltransferase gene by transcriptional coactivators cAMP response element-binding protein-binding protein and p300. J. Biol. Chem. 275, 34197–34204 (2000)
46. K. S. Srivenugopal, J. Shou, S. R. Mullapudi, F. F. Lang Jr., J. S. Rao, F. Ali-Osman, Enforced expression of wild-type p53 curtails the transcription of the O(6)-methylguanine-DNA methyltransferase gene in human tumor cells and enhances their sensitivity to alkylating agents. Clin. Cancer Res. 7, 1398–1409 (2001)
47. A. Natsume, D. Ishii, T. Wakabayashi, T. Tsuno, H. Hatano, M. Mizuno, J. Yoshida, IFN-beta down-regulates the expression of DNA repair gene MGMT and sensitizes resistant glioma cells to temozolomide. Cancer Res. 65, 7573–7579 (2005)
48. A. Reményi, H. R. Schöler, M. Wilmanns, Combinatorial control of gene expression. Nat. Struct. Mol. Biol. 11, 812–815 (2004)
49. R. Pique-Regi, J. F. Degner, A. A. Pai, D. J. Gaffney, Y. Gila, J. K. Pritchard, Accurate inference of transcription factor binding from DNA sequence and chromatin accessibility data. Genome Res. 21(3), 447–455 (2011)
50. C. J. Fry, P. J. Farnham, Context-dependent transcriptional regulation. J. Biol. Chem. 274, 29583–29586 (1999)
51. K. Vazquez-Santillan, J. Melendez-Zajgla, L. Jimenez-Hernandez, G. Martínez-Ruiz, V. Maldonado, NF-κB signaling in cancer stem cells: a promising therapeutic target? Cell. Oncol. 38, 327–339 (2015)