N-methylpurine DNA glycosylase and DNA polymerase β modulate BER inhibitor potentiation of glioma cells to temozolomide

Neuro-Oncology

Volumn 13, Issue 5, 2011, Pages 471-486

  Tang, Jiang Bo ^b,c   Svilar, David ^a,b   Trivedi, Ram N ^a,b   Wang, Xiao Hong ^b   Goellner, Eva M ^a,b   Moore, Briana ^b   Hamilton, Ronald L ^a   Banze, Lauren A ^b   Brown, Ashley R ^b   Sobol, Robert W ^a,b,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^c UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Base excision repair; Methoxyamine; N methylpurine DNA glycosylase; Poly(ADP ribose) polymerase; Temozolomide

Indexed keywords

DNA DIRECTED DNA POLYMERASE BETA; DNA GLYCOSYLTRANSFERASE; METHOXYAMINE; N (5,6 DIHYDRO 6 OXO 2 PHENANTHRIDINYL) 2 DIMETHYLAMINOACETAMIDE; N METHYLPURINE DNA GLYCOSYLASE; TEMOZOLOMIDE; UNCLASSIFIED DRUG; VELIPARIB;

ARTICLE; CELL STRAIN LN428; CELL STRAIN T98G; CONTROLLED STUDY; DRUG INHIBITION; DRUG POTENTIATION; ENZYME INHIBITION; EXCISION REPAIR; GLIOMA CELL; HUMAN; HUMAN CELL; MODULATION; PROTEIN EXPRESSION;

ANTINEOPLASTIC AGENTS, ALKYLATING; APOPTOSIS; BLOTTING, WESTERN; BRAIN; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; DACARBAZINE; DNA GLYCOSYLASES; DNA MODIFICATION METHYLASES; DNA POLYMERASE BETA; DNA REPAIR; DNA REPAIR ENZYMES; DRUG SYNERGISM; GLIOMA; GUANINE; HUMANS; HYDROXYLAMINES; PROMOTER REGIONS, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR SUPPRESSOR PROTEINS;

EID: 79959992212     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/nor011     Document Type: Article

References (82)

1. Mrugala MM, Chamberlain MC. Mechanisms of disease: Temozolomide and glioblastoma-look to the future. Nat Clin Pract Oncol 2008;5:476-486.
2. Tentori L, Graziani G. Recent approaches to improve the antitumor efficacy of temozolomide. Curr Med Chem 2009;16:245-257.
3. Sobol RW. Temozolomide. In: Schwab, M, ed. Encyclopedia of Cancer. Berlin, Heidelberg, New York: Springer, 2009.
4. Shrivastav N, Li D, Essigmann JM. Chemical biology of mutagenesis and DNA repair: Cellular responses to DNA alkylation. Carcinogenesis 2010;31:59-70.
5. Sarkaria JN, Kitange GJ, James CD, et al. Mechanisms of chemoresistance to alkylating agents in malignant glioma. Clin Cancer Res 2008;14:2900-2908.
6. Wood RD, Mitchell M, Lindahl T. Human DNA repair genes, 2005. Mutat Res 2005;577:275-283. (Pubitemid 41225506)
7. Wood RD, Mitchell M, Sgouros J, et al. Human DNA repair genes. Science 2001;291:1284-1289. (Pubitemid 32173086)
8. Hegi ME, Diserens AC, Gorlia T, et al. Mgmt gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005;352:997-1003. (Pubitemid 40349502)
9. Pollack IF, Hamilton RL, Sobol RW, et al. Mgmt expression strongly correlates with outcome in childhood malignant gliomas: Results from the ccg-945 cohort. J Clin Oncol 2006;24:3431-3437. (Pubitemid 46638900)
10. Cahill DP, Levine KK, Betensky RA, et al. 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. (Pubitemid 46649870)
11. McMurry TB. Mgmt inhibitors-the trinity college-paterson institute experience, a chemist's perception. DNA Repair (Amst) 2007;6:1161-1169. (Pubitemid 47058399)
12. Ranson M, Hersey P, Thompson D, et al. Randomized trial of the combination of lomeguatrib and temozolomide compared with temozolomide alone in chemotherapy naive patients with metastatic cutaneous melanoma. J Clin Oncol 2007;25:2540-2545. (Pubitemid 47041227)
13. Adhikari S, Choudhury S, Mitra PS, et al. Targeting base excision repair for chemosensitization. Anti-cancer agents in medicinal chemistry 2008;8:351-357. (Pubitemid 351761420)
14. Almeida KH, Sobol RW. A unified view of base excision repair: Lesion-dependent protein complexes regulated by post-translational modification. DNA Repair 2007;6:695-711. (Pubitemid 46670095)
15. Sobol RW, Prasad R, Evenski A, et al. The lyase activity of the DNA repair protein ß-polymerase protects from DNA-damage-induced cytotoxicity. Nature 2000;405:807-810. (Pubitemid 30407855)
16. Kinsella TJ. Coordination of DNA mismatch repair and base excision repair processing of chemotherapy and radiation damage for targeting resistant cancers. Clin Cancer Res 2009;15:1853-1859.
17. Liu L, Gerson SL. Therapeutic impact of methoxyamine: Blocking repair of abasic sites in the base excision repair pathway. Current Opinion in Investigative Drugs 2004;5:623-627.
18. Chalmers AJ. The potential role and application of parp inhibitors in cancer treatment. Br Med Bull 2009;89:23-40.
19. Tentori L, Leonetti C, Scarsella M, et al. Poly (adp-ribose) glycohydrolase inhibitor as chemosensitiser of malignant melanoma for temozolomide. Eur J Cancer 2005;41:2948-2957. (Pubitemid 41713135)
20. Jaiswal AS, Banerjee S, Panda H, et al. A novel inhibitor of DNA polymerase {beta} enhances the ability of temozolomide to impair the growth of colon cancer cells. Mol Cancer Res 2009;7:1973-1983.
21. Mizushina Y, Manita D, Takeuchi T, et al. The inhibitory action of kohamaic acid a derivatives on mammalian DNA polymerase beta. Molecules 2009;14:102-121.
22. Tang J, Goellner EM, Wang XW, et al. Bioenergetic metabolites regulate base excision repair-dependent cell death in response to DNA damage. Molecular Cancer Research 2010;8:67-79.
23. Trivedi RN, Almeida KH, Fornsaglio JL, et al. The role of base excision repair in the sensitivity and resistance to temozolomide mediated cell death. Cancer Res 2005;65:6394-6400. (Pubitemid 40994427)
24. Trivedi RN, Wang XH, Jelezcova E, et al. Human methyl purine DNA glycosylase and DNA polymerase ß expression collectively predict sensitivity to temozolomide. Molecular Pharmacology 2008;74:505-516.
25. Rosa S, Fortini P, Karran P, et al. Processing in vitro of an abasic site reacted with methoxyamine: A new assay for the detection of abasic sites formed in vivo. Nucleic Acids Res 1991;19:5569-5574. (Pubitemid 21912956)
26. Yan L, Bulgar A, Miao Y, et al. Combined treatment with temozolomide and methoxyamine: Blocking apurininc/pyrimidinic site repair coupled with targeting topoisomerase iialpha. Clin Cancer Res 2007;13:1532-1539. (Pubitemid 46450445)
27. Hottiger MO, Hassa PO, Luscher B, et al. Toward a unified nomenclature for mammalian adp-ribosyltransferases. Trends Biochem Sci 2010;35:208-219.
28. Hassa PO, Haenni SS, Elser M, et al. Nuclear adp-ribosylation reactions in mammalian cells: Where are we today and where are we going? Microbiol Mol Biol Rev 2006;70:789-829. (Pubitemid 44484693)
29. Schreiber V, Dantzer F, Ame JC, et al. Poly (adp-ribose): Novel functions for an old molecule. Nat Rev Mol Cell Biol 2006;7:517-528. (Pubitemid 44036457)
30. Dantzer F, Ame JC, Schreiber V, et al. Poly (adp-ribose) polymerase-1 activation during DNA damage and repair. Methods Enzymol 2006;409:493-510.
31. Fisher AE, Hochegger H, Takeda S, et al. Poly (adp-ribose) polymerase 1 accelerates single-strand break repair in concert with poly (adp-ribose) glycohydrolase. Mol Cell Biol 2007;27:5597-5605. (Pubitemid 47124411)
32. Ratnam K, Low JA. Current development of clinical inhibitors of poly (adp-ribose) polymerase in oncology. Clin Cancer Res 2007;13:1383-1388. (Pubitemid 46450426)
33. Cheng CL, Johnson SP, Keir ST, et al. Poly (adp-ribose) polymerase-1 inhibition reverses temozolomide resistance in a DNA mismatch repairdeficient malignant glioma xenograft. Mol Cancer Ther 2005;4:1364-1368.
34. Tentori L, Leonetti C, Scarsella M, 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. Clinical Cancer Research 2003;9:5370-5379. (Pubitemid 37413592)
35. Tentori L, Portarena I, Torino F, et al. Poly (adp-ribose) polymerase inhibitor increases growth inhibition and reduces g (2)/m cell accumulation induced by temozolomide in malignant glioma cells. Glia 2002;40:44-54. (Pubitemid 35181342)
36. Tentori L, Portarena I, Vernole P, et al. Effects of single or split exposure of leukemic cells to temozolomide, combined with poly (adp-ribose) polymerase inhibitors on cell growth, chromosomal aberrations and base excision repair components. Cancer Chemotherapy & Pharmacology 2001;47:361-369. (Pubitemid 32640776)
37. Miknyoczki SJ, Jones-Bolin S, Pritchard S, et al. Chemopotentiation of temozolomide, irinotecan, and cisplatin activity by cep-6800, a poly (adp-ribose) polymerase inhibitor. Mol Cancer Ther 2003;2:371-382.
38. Calabrese CR, Almassy R, Barton S, et al. Anticancer chemosensitization and radiosensitization by the novel poly (adp-ribose) polymerase-1 inhibitor ag14361. J Natl Cancer Inst 2004;96:56-67. (Pubitemid 38180960)
39. Calabrese CR, Batey MA, Thomas HD, et al. Identification of potent nontoxic poly (adp-ribose) polymerase-1 inhibitors: Chemopotentiation and pharmacological studies. Clin Cancer Res 2003;9:2711-2718. (Pubitemid 36842117)
40. Curtin NJ, Wang LZ, Yiakouvaki A, et al. Novel poly (adp-ribose) polymerase-1 inhibitor, ag14361, restores sensitivity to temozolomide in mismatch repair-deficient cells. Clin Cancer Res 2004;10:881-889. (Pubitemid 38198886)
41. Palma JP, Wang YC, Rodriguez LE, et al. Abt-888 confers broad in vivo activity in combination with temozolomide in diverse tumors. Clin Cancer Res 2009;15:7277-7290.
42. Koh DW, Lawler AM, Poitras MF, et al. Failure to degrade poly (adp-ribose) causes increased sensitivity to cytotoxicity and early embryonic lethality. Proc Natl Acad Sci U S A 2004;101:17699-17704. (Pubitemid 40051949)
43. Cortes U, Tong WM, Coyle DL, et al. Depletion of the 110-kilodalton isoform of poly (adp-ribose) glycohydrolase increases sensitivity to genotoxic and endotoxic stress in mice. Mol Cell Biol 2004;24:7163-7178. (Pubitemid 39014442)
44. Wang D, Zhong ZY, Zhang QH, et al. [Effect of adenoviral nmethylpurine DNA glycosylase overexpression on chemosensitivity of human osteosarcoma cells]. Zhonghua Bing Li Xue Za Zhi 2006;35:352-356. (Pubitemid 44213393)
45. Fishel ML, He Y, Smith ML, et al. Manipulation of base excision repair to sensitize ovarian cancer cells to alkylating agent temozolomide. Clin Cancer Res 2007;13:260-267. (Pubitemid 46121878)
46. Rinne ML, He Y, Pachkowski BF, et al. N-methylpurine DNA glycosylase overexpression increases alkylation sensitivity by rapidly removing nontoxic 7-methylguanine adducts. Nucleic Acids Res 2005;33:2859-2867. (Pubitemid 41511225)
47. Park MJ, Kim MS, Park IC, et al. Pten suppresses hyaluronic acidinduced matrix metalloproteinase-9 expression in u87mg glioblastoma cells through focal adhesion kinase dephosphorylation. Cancer Res 2002;62:6318-6322.
48. Ishii N, Maier D, Merlo A, et al. Frequent co-alterations of tp53, p16/cdkn2a, p14arf, pten tumor suppressor genes in human glioma cell lines. Brain Pathol 1999;9:469-479. (Pubitemid 29316287)
49. Zufferey R, Dull T, Mandel RJ, et al. Self-inactivating lentivirus vector for safe and efficient in vivo gene delivery. J Virol 1998;72:9873-9880. (Pubitemid 28520853)
50. Zufferey R, Nagy D, Mandel RJ, et al. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. Nat Biotechnol 1997;15:871-875.
51. Yoshizawa K, Jelezcova E, Brown AR, et al. Gastrointestinal hyperplasia with altered expression of DNA polymerase ß. PLoS ONE 2009;4:e6493.
52. Clegg RM. Fluorescence resonance energy transfer and nucleic acids. Methods Enzymol 1992;211:353-388.
53. Yaron A, Carmel A, Katchalski-Katzir E. Intramolecularly quenched fluorogenic substrates for hydrolytic enzymes. Anal Biochem 1979;95:228-235. (Pubitemid 9194287)
54. Taioli E, Ragin C, Wang XH, et al. Recurrence in oral and pharyngeal cancer is associated with quantitative mgmt promoter methylation. BMC Cancer 2009;9:354.
55. Maksimenko A, Ishchenko AA, Sanz G, et al. A molecular beacon assay for measuring base excision repair activities. Biochem Biophys Res Commun 2004;319:240-246. (Pubitemid 38670186)
56. Zielinska A, Davies OT, Meldrum RA, et al. Direct visualization of repair of oxidative damage by ogg1 in the nuclei of live cells. J Biochem Mol Toxicol 2010 (in press).
57. Lau AY, Wyatt MD, Glassner BJ, et al. Molecular basis for discriminating between normal and damaged bases by the human alkyladenine glycosylase, aag. Proceedings of the National Academy of Science 2000;97:13573-13578.
58. Connor EE, Wilson JJ, Wyatt MD. Effects of substrate specificity on initiating the base excision repair of n-methylpurines by variant human 3-methyladenine DNA glycosylases. Chem Res Toxicol 2005;18:87-94. (Pubitemid 40111096)
59. Sobol RW, Kartalou M, Almeida KH, et al. Base excision repair intermediates induce p53-independent cytotoxic and genotoxic responses. J Biol Chem 2003;278:39951-39959. (Pubitemid 37248559)
60. Sobol RW, Horton JK, Kuhn R, et al. Requirement of mammalian DNA polymerase-beta in base-excision repair. Nature 1996;379:183-186. (Pubitemid 26020204)
61. Stein GH. T98g: An anchorage-independent human tumor cell line that exhibits stationary phase g1 arrest in vitro. Journal of cellular physiology 1979;99:43-54. (Pubitemid 9150429)
62. Donawho CK, Luo Y, Penning TD, 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;13:2728-2737. (Pubitemid 46795129)
63. Gygi SP, Rochon Y, Franza BR, et al. Correlation between protein and mrna abundance in yeast. Mol Cell Biol 1999;19:1720-1730. (Pubitemid 29098230)
64. Svilar D, Goellner EM, Almeida KH, et al. Base excision repair and lesion-dependent sub-pathways for repair of oxidative DNA damage. Antioxid Redox Signal 2011 (in press).
65. Cerda SR, Turk PW, Thor AD, et al. Altered expression of the DNA repair protein, n-methylpurine-DNA glycosylase (mpg) in breast cancer. FEBS Lett 1998;431:12-18. (Pubitemid 28330843)
66. Kim NK, Ahn JY, Song J, et al. Expression of the DNA repair enzyme, n-methylpurine-DNA glycosylase (mpg) in astrocytic tumors. Anticancer Res 2003;23:1417-1423. (Pubitemid 36754109)
67. Prasad R, Shock DD, Beard WA, et al. Passing the baton: Substrate channeling in mammalian base excision repair pathways. J Biol Chem 2010;285:40479-40488.
68. Khodyreva SN, Prasad R, Ilina ES, et al. Apurinic/apyrimidinic (ap) site recognition by the 5'-drp/ap lyase in poly (adp-ribose) polymerase-1 (parp-1). Proc Natl Acad Sci U S A 2010;107:22090-22095.
69. Liu X, Shi Y, Guan R, et al. Potentiation of temozolomide cytotoxicity by poly (adp) ribose polymerase inhibitor abt-888 requires a conversion of single-stranded DNA damages to double-stranded DNA breaks. Mol Cancer Res 2008;6:1621-1629.
70. Bryant HE, Schultz N, Thomas HD, et al. Specific killing of brca2-deficient tumours with inhibitors of poly (adp-ribose) polymerase. Nature 2005;434:913-917. (Pubitemid 40559005)
71. Farmer H, McCabe N, Lord CJ, et al. Targeting the DNA repair defect in brca mutant cells as a therapeutic strategy. Nature 2005;434:917-921. (Pubitemid 40559006)
72. Kim NK, An HJ, Kim HJ, et al. Altered expression of the DNA repair protein, n-methylpurine-DNA glycosylase (mpg) in human gonads. Anticancer Res 2002;22:793-798. (Pubitemid 34475230)
73. Albertella MR, Lau A, O'Connor MJ. The overexpression of specialized DNA polymerases in cancer. DNA Repair (Amst) 2005;4:583-593. (Pubitemid 40462046)
74. Barton VN, Donson AM, Kleinschmidt-DeMasters BK, et al. Parp1 expression in pediatric central nervous system tumors. Pediatr Blood Cancer 2009;53:1227-1230.
75. Goncalves A, Finetti P, Sabatier R, et al. Poly (adp-ribose) polymerase-1 mrna expression in human breast cancer: A meta-analysis. Breast Cancer Res Treat 2011 (in press).
76. Pizem J, Popovic M, Cor A. Expression of gli1 and parp1 in medulloblastoma: An immunohistochemical study of 65 cases. J Neurooncol 2010.
77. Giard DJ, Aaronson SA, Todaro GJ, et al. In vitro cultivation of human tumors: Establishment of cell lines derived from a series of solid tumors. J Natl Cancer Inst 1973;51:1417-1423.
78. Kruse CA, Mitchell DH, Kleinschmidt-DeMasters BK, et al. Characterization of a continuous human glioma cell line dbtrg-05mg: Growth kinetics, karyotype, receptor expression, and tumor suppressor gene analyses. In Vitro Cell Dev Biol 1992;28 A: 609-614. (Pubitemid 23297274)
79. Allalunis-Turner MJ, Barron GM, Day RS, 3rd, et al. Isolation of two cell lines from a human malignant glioma specimen differing in sensitivity to radiation and chemotherapeutic drugs. Radiat Res 1993;134:349-354. (Pubitemid 23209259)
80. Clark MJ, Homer N, O'Connor BD, et al. U87mg decoded: The genomic sequence of a cytogenetically aberrant human cancer cell line. PLoS Genet 2010;6:e1000832.
81. Van Meir E, Sawamura Y, Diserens AC, et al. Human glioblastoma cells release interleukin 6 in vivo and in vitro. Cancer Res 1990;50:6683-6688. (Pubitemid 20348800)
82. Van Meir EG, Kikuchi T, Tada M, et al. Analysis of the p53 gene and its expression in human glioblastoma cells. Cancer Res 1994;54:649-652. (Pubitemid 24068319)