Malignant melanoma cells acquire resistance to DNA interstrand cross-linking chemotherapeutics by p53-triggered upregulation of DDB2/XPC-mediated DNA repair

Oncogene

Volumn 33, Issue 15, 2014, Pages 1964-1974

  Barckhausen, C ^a   Roos, W P ^a   Naumann, S C ^a   Kaina, B ^a  

^a UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

DDB2; drug resistance; interstrand cross links; metastatic melanoma; p53; XPC

Indexed keywords

ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; DRUG RESISTANCE, NEOPLASM; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROGRAFTS; HUMANS; IMMUNOBLOTTING; MELANOMA; MICE; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR SUPPRESSOR PROTEIN P53; UP-REGULATION;

EID: 84899428083     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.141     Document Type: Article

References (55)

1. Castresana JS, Rubio MP, Vazquez JJ, Idoate M, Sober AJ, Seizinger BR, et al. Lack of allelic deletion and point mutation as mechanisms of p53 activation in human malignant melanoma. Int J Cancer 1993; 55: 562-565
2. Lubbe J, Reichel M, Burg G, Kleihues P. Absence of p53 gene mutations in cutaneous melanoma. J Invest Dermatol 1994; 102: 819-821
3. Roos WP, Jost E, Belohlavek C, Nagel G, Fritz G, Kaina B. Intrinsic anticancer drug resistance of malignant melanoma cells is abrogated by IFN-{beta} and valproic acid. Cancer Res 2011; 71: 4150-4160
4. Soengas MS, Capodieci P, Polsky D, Mora J, Esteller M, Opitz-Araya X, et al. Inactivation of the apoptosis effector Apaf-1 in malignant melanoma. Nature 2001; 409: 207-211
5. Carson C, Omolo B, Chu H, Zhou Y, Sambade MJ, Peters EC, et al. A prognostic signature of defective p53-dependent G1 checkpoint function in melanoma cell lines. Pigment Cell Melanoma Res 2012; 25: 514-526
6. Kleeberg UR, Engel E, Israels P, Brocker EB, Tilgen W, Kennes C, et al. Palliative therapy of melanoma patients with fotemustine. Inverse relationship between tumour load and treatment effectiveness. Melanoma Res 1995; 5: 195-200
7. Kaina B, Christmann M, Naumann S, Roos WP. MGMT: Key node in the battle against genotoxicity, carcinogenicity and apoptosis induced by alkylating agents. DNA Repair (Amst) 2007; 6: 1079-1099
8. Hayes MT, Bartley J, Parsons PG, Eaglesham GK, Prakash AS. Mechanism of action of fotemustine, a new chloroethylnitrosourea anticancer agent: Evidence for the formation of two DNA-reactive intermediates contributing to cytotoxicity. Biochemistry 1997; 36: 10646-10654
9. Dolan ME, Norbeck L, Clyde C, Hora NK, Erickson LC, Pegg AE. Expression of mammalian O6-Alkylguanine-DNA alkyltransferase in a cell line sensitive to alkylating agents. Carcinogenesis 1989; 10: 1613-1619
10. Chen JM, Zhang YP, Wang C, Sun Y, Fujimoto J, Ikenaga M. O6-methylguanine-DNA methyltransferase activity in human tumors. Carcinogenesis 1992; 13: 1503-1507
11. Tellez CS, Shen L, Estecio MR, Jelinek J, Gershenwald JE, Issa JP. CpG island methylation profiling in human melanoma cell lines. Melanoma Res 2009; 19: 146-155
12. Passagne I, Evrard A, Winum JY, Depeille P, Cuq P, Montero JL, et al. Cytotoxicity, DNA damage, and apoptosis induced by new fotemustine analogs on human melanoma cells in relation to O6-methylguanine DNA-methyltransferase expression. J Pharmacol Exp Ther 2003; 307: 816-823
13. Naumann SC, Roos WP, Jost E, Belohlavek C, Lennerz V, Schmidt CW, et al. Temozolomide-And fotemustine-induced apoptosis in human malignant melanoma cells: Response related to MGMT, MMR, DSBs, and p53. Br J Cancer 2009; 100: 322-333
14. Christmann M, Pick M, Lage H, Schadendorf D, Kaina B. Acquired resistance of melanoma cells to the antineoplastic agent fotemustine is caused by reactivation of the DNA repair gene MGMT. Int J Cancer 2001; 92: 123-129
15. Ludlum DB. Formation of cyclic adducts in nucleic acids by the haloethylnitrosoureas. IARC Sci Publ 1986; 70: 137-146
16. Akkari YM, Bateman RL, Reifsteck CA, Olson SB, Grompe M. DNA replication is required To elicit cellular responses to psoralen-induced DNA interstrand cross-links. Mol Cell Biol 2000; 20: 8283-8289
17. Muniandy PA, Thapa D, Thazhathveetil AK, Liu ST, Seidman MM. Repair of laserlocalized DNA interstrand cross-links in G1 phase mammalian cells. J Biol Chem 2009; 284: 27908-27917
18. McHugh PJ, Sarkar S. DNA interstrand cross-link repair in the cell cycle: A critical role for polymerase zeta in G1 phase. Cell Cycle 2006; 5: 1044-1047
19. Sasaki MS, Takata M, Sonoda E, Tachibana A, Takeda S. Recombination repair pathway in the maintenance of chromosomal integrity against DNA interstrand crosslinks. Cytogenet Genome Res 2004; 104: 28-34
20. De Silva IU, McHugh PJ, Clingen PH, Hartley JA. Defining the roles of nucleotide excision repair and recombination in the repair of DNA interstrand cross-links in mammalian cells. Mol Cell Biol 2000; 20: 7980-7990
21. Raschle M, Knipscheer P, Enoiu M, Angelov T, Sun J, Griffith JD, et al. Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 2008; 134: 969-980
22. Tsaryk R, Fabian K, Thacker J, Kaina B. Xrcc2 deficiency sensitizes cells to apoptosis by MNNG and the alkylating anticancer drugs temozolomide, fotemustine and mafosfamide. Cancer Lett 2006; 239: 305-313
23. Roos WP, Tsaalbi-Shtylik A, Tsaryk R, Guvercin F, De Wind N, Kaina B. The translesion polymerase Rev3L in the tolerance of alkylating anticancer drugs. Mol Pharmacol 2009; 76: 927-934
24. Tian M, Shinkura R, Shinkura N, Alt FW. Growth retardation, early death, and DNA repair defects in mice deficient for the nucleotide excision repair enzyme XPF. Mol Cell Biol 2004; 24: 1200-1205
25. Jaspers NG, Raams A, Silengo MC, Wijgers N, Niedernhofer LJ, Robinson AR, et al. First reported patient with human ERCC1 deficiency has cerebro-oculo-facioskeletal syndrome with a mild defect in nucleotide excision repair and severe developmental failure. Am J Hum Genet 2007; 80: 457-466
26. Fety R, Lucas C, Solere P, Cour V, Vignoud J. Hepatic intra-Arterial infusion of fotemustine: Pharmacokinetics. Cancer Chemother Pharmacol 1992; 31: 118-122
27. Pegg AE, Boosalis M, Samson L, Moschel RC, Byers TL, Swenn K, et al. Mechanism of inactivation of human O6-Alkylguanine-DNA alkyltransferase by O6-benzylguanine. Biochemistry 1993; 32: 11998-12006
28. Usanova S, Piee-Staffa A, Sied U, Thomale J, Schneider A, Kaina B, et al. Cisplatin sensitivity of testis tumour cells is due to deficiency in interstrand-crosslink repair and low ERCC1-XPF expression. Mol Cancer 2010; 9: 248
29. Haapajarvi T, Pitkanen K, Laiho M. Human melanoma cell line UV responses show independency of p53 function. Cell Growth Differ 1999; 10: 163-171
30. Wang QE, Zhu Q, Wani G, Chen J, Wani AA. UV radiation-induced XPC translocation within chromatin is mediated by damaged-DNA binding protein, DDB2. Carcinogenesis 2004; 25: 1033-1043
31. Chen Z, Xu XS, Yang J, Wang G. Defining the function of XPC protein in psoralen and cisplatin-mediated DNA repair and mutagenesis. Carcinogenesis 2003; 24: 1111-1121
32. Tarhini AA, Agarwala SS. Management of brain metastases in patients with melanoma. Curr Opin Oncol 2004; 16: 161-166
33. Brent TP, Lestrud SO, Smith DG, Remack JS. Formation of DNA interstrand cross-links by the novel chloroethylating agent 2-chloroethyl(methylsulfonyl) methanesulfonate: Suppression by O6-Alkylguanine-DNA alkyltransferase purified from human leukemic lymphoblasts. Cancer Res 1987; 47: 3384-3387
34. Muller M, Wilder S, Bannasch D, Israeli D, Lehlbach K, Li-Weber M, et al. p53 activates the CD95 (APO-1/Fas) gene in response to DNA damage by anticancer drugs. J Exp Med 1998; 188: 2033-2045
35. Adimoolam S, Ford JM. p53 and DNA damage-inducible expression of the xeroderma pigmentosum group C gene. Proc Natl Acad Sci USA 2002; 99: 12985-12990
36. Hwang BJ, Ford JM, Hanawalt PC, Chu G. Expression of the p48 xeroderma pigmentosum gene is p53-dependent and is involved in global genomic repair. Proc Natl Acad Sci USA 1999; 96: 424-428
37. Batista LF, Roos WP, Christmann M, Menck CF, Kaina B. Differential sensitivity of malignant glioma cells to methylating and chloroethylating anticancer drugs: P53 determines the switch by regulating xpc, ddb2, and DNA double-strand breaks. Cancer Res 2007; 67: 11886-11895
38. Batista LF, Roos WP, Kaina B, Menck CF. p53 mutant human glioma cells are sensitive to UV-C-induced apoptosis due to impaired cyclobutane pyrimidine dimer removal. Mol Cancer Res 2009; 7: 237-246
39. Thoma BS, Wakasugi M, Christensen J, Reddy MC, Vasquez KM. Human XPChHR23B interacts with XPA-RPA in the recognition of triplex-directed psoralen DNA interstrand crosslinks. Nucleic Acids Res 2005; 33: 2993-3001
40. Dumaz N, Meek DW. Serine15 phosphorylation stimulates p53 transactivation but does not directly influence interaction with HDM2. Embo J. 1999; 18: 7002-7010
41. Chehab NH, Malikzay A, Stavridi ES, Halazonetis TD. Phosphorylation of Ser-20 mediates stabilization of human p53 in response to DNA damage. Proc Natl Acad Sci USA 1999; 96: 13777-13782
42. Devary Y, Gottlieb RA, Lau LF, Karin M. Rapid and preferential activation of the c-jun gene during the mammalian UV response. Mol Cell Biol 1991; 11: 2804-2811
43. Rafferty JA, Clarke AR, Sellappan D, Koref MS, Frayling IM, Margison GP. Induction of murine O6-Alkylguanine-DNA-Alkyltransferase in response to ionising radiation is p53 gene dose dependent. Oncogene 1996; 12: 693-697
44. Grombacher T, Eichhorn U, Kaina B. p53 is involved in regulation of the DNA repair gene O6-methylguanine-DNA methyltransferase (MGMT) by DNA damaging agents. Oncogene 1998; 17: 845-851
45. Garbe C, Peris K, Hauschild A, Saiag P, Middleton M, Spatz A, et al. Diagnosis and treatment of melanoma: European consensus-based interdisciplinary guideline. Eur J Cancer 2010; 46: 270-283
46. Pavey S, Johansson P, Packer L, Taylor J, Stark M, Pollock PM, et al. Microarray expression profiling in melanoma reveals a BRAF mutation signature. Oncogene 2004; 23: 4060-4067
47. Stark M, Hayward N. Genome-wide loss of heterozygosity and copy number analysis in melanoma using high-density single-nucleotide polymorphism arrays. Cancer Res 2007; 67: 2632-2642
48. Wu YH, Tsai Chang JH, Cheng YW, Wu TC, Chen CY, Lee H. Xeroderma pigmentosum group C gene expression is predominantly regulated by promoter hypermethylation and contributes to p53 mutation in lung cancers. Oncogene 2007; 26: 4761-4773
49. Berdelle N, Nikolova T, Quiros S, Efferth T, Kaina B. Artesunate induces oxidative DNA damage, sustained dna double-strand breaks, and the ATM/ATR damage response in cancer cells. Mol Cancer Ther 2011; 10: 2224-2233
50. Roos W, Baumgartner M, Kaina B. Apoptosis triggered by DNA damage O6-methylguanine in human lymphocytes requires DNA replication and is mediated by p53 and Fas/CD95/Apo-1. Oncogene 2004; 23: 359-367
51. Roos WP, Batista LF, Naumann SC, Wick W, Weller M, Menck CF, et al. Apoptosis in malignant glioma cells triggered by the temozolomide-induced DNA lesion O6-methylguanine. Oncogene 2007; 26: 186-197
52. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, et al. Prevention of apoptosis by Bcl-2: Release of cytochrome c from mitochondria blocked. Science 1997; 275: 1129-1132
53. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248-254
54. Roos WP, Nikolova T, Quiros S, Naumann SC, Kiedron O, Zdzienicka MZ, et al. Brca2/Xrcc2 dependent HR, but not NHEJ, is required for protection against O(6)-methylguanine triggered apoptosis, DSBs and chromosomal aberrations by a process leading to SCEs. DNA Repair (Amst) 2009; 8: 72-86
55. Padget K, Carr R, Pearson AD, Tilby MJ, Austin CA. Camptothecin- stabilised topoisomerase I-DNA complexes in leukaemia cells visualised and quantified in situ by the TARDIS assay (trapped in agarose DNA immunostaining). Biochem Pharmacol 2000; 59(6): 629-638