Inhibition of nuclear factor-κB activity by temozolomide involves O6-methylguanine-induced inhibition of p65 DNA binding

Cancer Research

Volumn 67, Issue 14, 2007, Pages 6889-6898

  Yamini, Bakhtiar ^a,d   Yu, Xiaohong ^a   Dolan, M Eileen ^a   Wu, Michael H ^a   Kufe, Donald W ^c   Weichselbaum, Ralph R ^b  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d UNIVERSITY OF CHICAGO MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 O METHYLGUANINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; SYNAPTOTAGMIN I; TEMOZOLOMIDE; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL DEATH; CELL STRAIN HCT116; COLONY FORMING UNIT; CONTROLLED STUDY; CYTOTOXICITY; DNA BINDING; DNA DAMAGE; DRUG ACTIVITY; DRUG EFFECT; DRUG MECHANISM; GEL MOBILITY SHIFT ASSAY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; METHYLATION; MISMATCH REPAIR; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DNA BINDING; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION INITIATION;

ACTIVE TRANSPORT, CELL NUCLEUS; ANTINEOPLASTIC AGENTS, ALKYLATING; CELL LINE, TUMOR; DACARBAZINE; DNA DAMAGE; GUANINE; HUMANS; LUCIFERASES; MICROSCOPY, FLUORESCENCE; NF-KAPPA B; PROTEIN BINDING; SUBCELLULAR FRACTIONS; TETRADECANOYLPHORBOL ACETATE; TIME FACTORS; TRANSCRIPTION FACTOR RELA;

EID: 34547119552     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-06-4496     Document Type: Article

References (50)

1. Stupp R, Mason WP, van den Bent MJ, et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352:987-96.
2. Newlands ES, Stevens MF, Wedge SR, Wheelhouse RT, Brock C. Temozolomide: a review of its discovery, chemical properties, pre-clinical development and clinical trials. Cancer Treat Rev 1997;23:35-61.
3. Tisdale MJ. Antitumor imidazotetrazines-XV. Role of guanine O6 alkylation in the mechanism of cytotoxicity of imidazotetrazinones. Biochem Pharmacol 1987;36:457-62.
4. 6-alkylguanine-DNA alkyltransferase correlates with potentiation of temozolomide and CCNU toxicity in human tumour cells. Br J Cancer 1993;67:1299-302.
5. 6-benzylguanine provides a means to evaluate the role of this protein in protection against carcinogenic and therapeutic alkylating agents. Proc Natl Acad Sci U S A 1990;87:5368-72.
6. Gerson SL. Clinical relevance of MGMT in the treatment of cancer. J Clin Oncol 2002;20:2388-99.
7. Stojic L, Brun R, Jiricny J. Mismatch repair and DNA damage signalling. DNA Repair (Amst) 2004;3:1091-101.
8. 6-Methylguanine residues elicit DNA repair synthesis by human cell extracts. J Biol Chem 1993;268:15878-86.
9. Fishel R. The selection for mismatch repair defects in hereditary nonpolyposis colorectal cancer: revising the mutator hypothesis. Cancer Res 2001;61:7369-74.
10. 6-methylguanine is Bcl-2 and caspase-9/3 regulated and Fas/caspase-8 independent. Cancer Res 2000;60:5815-24.
11. Hickman MJ, Samson LD. Role of DNA mismatch repair and p53 in signaling induction of apoptosis by alkylating agents. Proc Natl Acad Sci U S A 1999;96:10764-9.
12. Hickman MJ, Samson LD. Apoptotic signaling in response to a single type of DNA lesion, O(6)-methylguanine. Mol Cell 2004;14:105-16.
13. 2/M arrest and the fate of temozolomide-treated human glioblastoma cells. Cancer Res 2001;61:1957-63.
14. Karin M, Lin A. NF-κB at the crossroads of life and death. Nat Immunol 2002;3:221-7.
15. Baldwin AS. Control of oncogenesis and cancer therapy resistance by the transcription factor NF-κB. J Clin Invest 2001;107:241-6.
16. Ghosh S, May MJ, Kopp EB. NF-κB and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol 1998;16:225-60.
17. Chen FE, Huang DB, Chen YQ, Ghosh G. Crystal structure of p50/p65 heterodimer of transcription factor NF-κB bound to DNA. Nature 1998;391:410-3.
18. Kucharczak J, Simmons MJ, Fan Y, Gelinas C. To be, or not to be: NF-κB is the answer - role of Rel/NF-κB in the regulation of apoptosis. Oncogene 2003;22:8961-82.
19. Vermeulen L, De Wilde G, Notebaert S, Vanden Berghe W, Haegeman G. Regulation of the transcriptional activity of the nuclear factor-κB p65 subunit. Biochem Pharmacol 2002;64:963-70.
20. Anrather J, Racchumi G, Iadecola C. cis-acting, element-specific transcriptional activity of differentially phosphorylated nuclear factor-κB. J Biol Chem 2005;280:244-52.
21. Nakanishi C, Toi M. Nuclear factor-κB inhibitors as sensitizers to anticancer drugs. Nat Rev Cancer 2005;5:297-309.
22. Campbell KJ, Witty JM, Rocha S, Perkins ND. Cisplatin mimics ARF tumor suppressor regulation of RelA (p65) nuclear factor-κB transactivation. Cancer Res 2006;66:929-35.
23. 6-alkylguanine-DNA alkyltransferase in protecting against cyclophosphamide-induced toxicity and mutagenicity. Cancer Res 1999;59:3059-63.
24. Wu MH, Yan B, Humerickhouse R, Dolan ME. Irinotecan activation by human carboxylesterases in colorectal adenocarcinoma cells. Clin Cancer Res 2002;8:2696-700.
25. Kanno T, Brown K, Siebenlist U. Evidence in support of a role for human T-cell leukemia virus type I Tax in activating NF-κB via stimulation of signaling pathways. J Biol Chem 1995;270:11745-8.
26. Park JO, Lopez CA, Gupta VK, et al. Transcriptional control of viral gene therapy by cisplatin. J Clin Invest 2002;110:403-10.
27. Han Y, Englert JA, Delude RL, Fink MP. Ethacrynic acid inhibits multiple steps in the NF-κB signaling pathway. Shock 2005;23:45-53.
28. Yamini B, Yu X, Gillespie GY, Kufe DW, Weichselbaum RR. Transcriptional targeting of adenovirally delivered tumor necrosis factor a by temozolomide in experimental glioblastoma. Cancer Res 2004;64:6381-4.
29. Salloum RM, Jaskowiak NT, Mauceri HJ, et al. NM-3, an isocoumarin, increases the antitumor effects of radiotherapy without toxicity. Cancer Res 2000;60:6958-63.
30. Kimchi ET, Posner MC, Park JO, et al. Progression of Barrett's metaplasia to adenocarcinoma is associated with the suppression of the transcriptional programs of epidermal differentiation. Cancer Res 2005;65:3146-54.
31. Marinari B, Costanzo A, Marzano V, Piccolella E, Tuosto L. CD28 delivers a unique signal leading to the selective recruitment of RelA and p52 NF-κB subunits on IL-8 and Bcl-xL gene promoters. Proc Natl Acad Sci U S A 2004;101:6098-103.
32. Miao F, Gonzalo IG, Lanting L, Natarajan R. In vivo chromatin remodeling events leading to inflammatory gene transcription under diabetic conditions. J Biol Chem 2004;279:18091-7.
33. Yang J, Amiri KI, Burke JR, Schmid JA, Richmond A. BMS-345541 targets inhibitor of κB kinase and induces apoptosis in melanoma: involvement of nuclear factor κB and mitochondria pathways. Clin Cancer Res 2006;12:950-60.
34. Brada M, Judson I, Beale P, et al. Phase I dose-escalation and pharmacokinetic study of temozolomide (SCH 52365) for refractory or relapsing malignancies. Br J Cancer 1999;81:1022-30.
35. 6-benzylguanine analogues on sensitivity of human tumor cells to the cytotoxic effects of alkylating agents. Cancer Res 1991;51:3367-72.
36. 6-Methylguanine DNA methyltransferase and p53 status predict temozolomide sensitivity in human malignant glioma cells. J Neurochem 2006;96:766-76.
37. Jansen M, Bardenheuer W, Sorg UR, Seeber S, Flasshove M, Moritz T. Protection of hematopoietic cells from O(6)-alkylation damage by O(6)-methylguanine DNA methyltransferase gene transfer: studies with different O(6)-alkylating agents and retroviral backbones. Eur J Haematol 2001;67:2-13.
38. 6-alkylguanine-DNA alkyltransferases. Cancer Res 2000;60:5464-9.
39. 3-Methyladenine induces early poly(ADP-ribosylation), reduction of nuclear factor-κB DNA binding ability, and nuclear up-regulation of telomerase activity. Mol Pharmacol 2005;67:572-81.
40. Tisdale MJ. Antitumour imidazotetrazines: XI. Effect of 8-carbamoyl-3-methylimidazo[5,1-d]-1,2,3,5-tetrazin-4(3H)-one [CCRG 81045; M and B 39831 NSC 362856] on poly(ADP-ribose) metabolism. Br J Cancer 1985;52:789-92.
41. Koi M, Umar A, Chauhan DP, et al. Human chromosome 3 corrects mismatch repair deficiency and microsatellite instability and reduces N-methyl-N′-nitro-N-nitrosoguanidine tolerance in colon tumor cells with homozygous hMLH1 mutation. Cancer Res 1994;54:4308-12.
42. Kat A, Thilly WG, Fang WH, Longley MJ, Li GM, Modrich P. An alkylation-tolerant, mutator human cell line is deficient in strand-specific mismatch repair. Proc Natl Acad Sci U S A 1993;90:6424-8.
43. Amiri KI, Horton LW, LaFleur BJ, Sosman JA, Richmond A. Augmenting chemosensitivity of malignant melanoma tumors via proteasome inhibition: implication for bortezomib (VELCADE, PS-341) as a therapeutic agent for malignant melanoma. Cancer Res 2004;64:4912-8.
44. 6-Methylguanine inhibits the binding of transcription factors to DNA. Nucleic Acids Res 1991;19:5739-42.
45. Bull VL, Tisdale MJ. Antitumour imidazotetrazines: XVI. Macromolecular alkylation by 3-substituted imidazotetrazinones. Biochem Pharmacol 1987;36:3215-20.
46. Okazaki T, Sakon S, Sasazuki T, et al. Phosphorylation of serine 276 is essential for p65 NF-κB subunit-dependent cellular responses. Biochem Biophys Res Commun 2003;300:807-12.
47. Garcia-Pineres AJ, Castro V, Mora G, et al. Cysteine 38 in p65/NF-κB plays a crucial role in DNA binding inhibition by sesquiterpene lactones. J Biol Chem 2001;276:39713-20.
48. Tamatani M, Che YH, Matsuzaki H, et al. Tumor necrosis factor induces Bcl-2 and Bcl-x expression through NFκB activation in primary hippocampal neurons. J Biol Chem 1999;274:8531-8.
49. Wang JY, Edelmann W. Mismatch repair proteins as sensors of alkylation DNA damage. Cancer Cell 2006;9:417-8.
50. Karin M, Yamamoto Y, Wang QM. The IKK NF-κB system: a treasure trove for drug development. Nat Rev Drug Discov 2004;3:17-26.