Induction of glutathione-dependent DNA double-strand breaks by the novel anticancer drug brostallicin

Molecular Cancer Therapeutics

Volumn 8, Issue 7, 2009, Pages 1985-1994

  Guirouilh Barbat, Josée ^a   Zhang, Yong Wei ^a   Pommier, Yves ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APHIDICOLIN; BROSTALLICIN; BUTHIONINE SULFOXIMINE; DOUBLE STRANDED DNA; ENDONUCLEASE; GLUTATHIONE; HISTONE H2AX; PROTEIN; PROTEIN 53BP1; PROTEIN MRE 11; TRABECTEDIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE S PHASE; CELL PROLIFERATION; CELL STRAIN HCT116; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DNA SYNTHESIS; DNA SYNTHESIS INHIBITION; DOUBLE STRANDED DNA BREAK; DRUG RESPONSE; EXCISION REPAIR; GROWTH INHIBITION; HUMAN; HUMAN CELL; LYMPHOCYTE; PHARMACODYNAMICS; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ANTINEOPLASTIC AGENTS; ANTINEOPLASTIC AGENTS, ALKYLATING; APOPTOSIS; BLOTTING, WESTERN; CELL CYCLE; CELL PROLIFERATION; DIOXOLES; DNA BREAKS, DOUBLE-STRANDED; DNA REPLICATION; DNA-BINDING PROTEINS; GLUTATHIONE; GUANIDINES; HCT116 CELLS; HISTONES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PHOSPHOPROTEINS; PYRROLES; TETRAHYDROISOQUINOLINES;

EID: 67651158999     PISSN: 15357163     EISSN: None     Source Type: Journal    
DOI: 10.1158/1535-7163.MCT-09-0320     Document Type: Article

References (49)

1. D'Incalci M, Sessa C. DNA minor groove binding ligands: a new class of anticancer agents. Expert Opin Investig Drugs 1997;6:875-84.
2. Marchini S, Broggini M, Sessa C, D'Incalci M. Development of distamycin-related DNA binding anticancer drugs. Expert Opin Investig Drugs 2001;10:1703-14.
3. Schoffski P, Dumez H, Wolter P, et al. Clinical impact of trabectedin (ecteinascidin-743) in advanced/metastatic soft tissue sarcoma. Expert Opin Pharmacother 2008;9:1609-18.
4. Fayette J, Coquard IR, Alberti L, et al. ET-743: a novel agent with activity in soft-tissue sarcomas. Curr Opin Oncol 2006;18:347-53.
5. Aune GJ, Furuta T, Pommier Y. Ecteinascidin 743: a novel anticancer drug with a unique mechanism of action. Anticancer Drugs 2002;13:545-55.
6. Ghielmini M, Bosshard G, Capolongo L, et al. Estimation of the haematological toxicity of minor groove alkylators using tests on human cord blood cells. Br J Cancer 1997;75:878-83.
7. Cozzi P. The discovery of a new potential anticancer drug: a case history. Farmaco 2003;58:213-20.
8. Cristofanilli M, Bryan WJ, Miller LL, et al. Phase II study of adozelesin in untreated metastatic breast cancer. Anticancer Drugs 1998;9:779-82.
9. Leonce S, Kraus-Berthier L, Golsteyn RM, et al. Generation of replication-dependent double-strand breaks by the novel N2-G-alkylator S23906-1. Cancer Res 2006;66:7203-10.
10. Kiakos K, Sato A, Asao T, McHugh PJ, Lee M, Hartley JA. DNA sequence selective adenine alkylation, mechanism of adduct repair, and in vivo antitumor activity of the novel achiral seco-amino-cyclopropylbenz[ e]indolone analogue of duocarmycin AS-I-145. Mol Cancer Ther 2007;6:2708-18.
11. Geroni C, Pennella G, Capoongo L, et al. Antitumor activity of PNU-166196, a novel minor groove binder selected for clinical development. Proc Am Assoc Cancer Res 2000;2000:265.
12. Cozzi P. Distamycin derivatives as potential anticancer agents. IDrugs 2001;4:573-81.
13. Fedier A, Fowst C, Tursi J, et al. Brostallicin (PNU-166196) - a new DNA minor groove binder that retains sensitivity in DNA mismatch repair-deficient tumour cells. Br J Cancer 2003;89:1559-65.
14. Branch P, Hampson R, Karran P. DNA mismatch binding defects, DNA damage tolerance, and mutator phenotypes in human colorectal carcinoma cell lines. Cancer Res 1995;55:2304-9.
15. Drummond JT, Anthoney A, Brown R, Modrich P. Cisplatin and adriamycin resistance are associated with MutLα and mismatch repair deficiency in an ovarian tumor cell line. J Biol Chem 1996;271:19645-8.
16. Leahy M, Ray-Coquard I, Verweij J, et al. Brostallicin, an agent with potential activity in metastatic soft tissue sarcoma: a phase II study from the European Organisation for Research and Treatment of Cancer Soft Tissue and Bone Sarcoma Group. Eur J Cancer 2007;43:308-15.
17. Hartmann JT. Systemic treatment options for patients with refractory adult-type sarcoma beyond anthracyclines. Anticancer Drugs 2007;18:245-54.
18. Geroni C, Marchini S, Cozzi P, et al. Brostallicin, a novel anticancer agent whose activity is enhanced upon binding to glutathione. Cancer Res 2002;62:2332-6.
19. Pompella A, Corti A, Paolicchi A, Giommarelli C, Zunino F. γ-Glutamyl-transferase, redox regulation and cancer drug resistance. Curr Opin Pharmacol 2007;7:360-6.
20. McIlwain CC, Townsend DM, Tew KD. Glutathione S-transferase polymorphisms: cancer incidence and therapy. Oncogene 2006;25:1639-48.
21. Tsuchida S, Sato K. Glutathione transferases and cancer. Crit Rev Biochem Mol Biol 1992;27:337-84.
22. Clapper ML, Szarka CE. Glutathione S-transferases - biomarkers of cancer risk and chemopreventive response. Chem Biol Interact 1998;111-112:377-88.
23. Hayes JD, Pulford DJ. The glutathione S-transferase supergene family: regulation of GST and the contribution of the isoenzymes to cancer chemoprotection and drug resistance. Crit Rev Biochem Mol Biol 1995;30:445-600.
24. Moscow JA, Fairchild CR, Madden MJ, et al. Expression of anionic glutathione-S-transferase and P-glycoprotein genes in human tissues and tumors. Cancer Res 1989;49:1422-8.
25. Sato K, Satoh K, Tsuchida S, et al. Specific expression of glutathione S-transferase π forms in (pre)neoplastic tissues: their properties and functions. Tohoku J Exp Med 1992;168:97-103.
26. Guirouilh-Barbat J, Pommier Y. Et-743 induced DNA double strand breaks: a link between histone γ-H2AX, transcription coupled nucleotide excision repair and Mre11 endonuclease [abstract 4642]. 97th Annual Meeting of the American Association for Cancer Research, Washington, District of Columbia, 2006. p. 1090.
27. Soares DG, Escargueil AE, Poindessous V, et al. From the Cover: Replication and homologous recombination repair regulate DNA double-strand break formation by the antitumor alkylator ecteinascidin 743. Proc Natl Acad Sci U S A 2007;104:13062-7.
28. Guirouilh-Barbat J, Redon C, Pommier Y. Transcription-coupled DNA double-strand breaks are mediated via the nucleotide excision repair and the Mre11-Rad50-Nbs1 complex. Mol Biol Cell 2008;19:3969-81.
29. Bonner WM, Redon CE, Dickey JS, et al. γH2AX and cancer. Nat Rev Cancer 2008;8:957-67.
30. Erba E, Bergamaschi D, Bassano L, et al. Ecteinascidin-743 (ET-743), a natural marine compound, with a unique mechanism of action. Eur J Cancer 2001;37:97-105.
31. Takebayashi Y, Pourquier P, Zimonjic DB, et al. Antiproliferative activity of ecteinascidin 743 is dependent upon transcription-coupled nucleotide-excision repair. Nat Med 2001;7:961-6.
32. Zewail-Foote M, Li VS, Kohn H, Bearss D, Guzman M, Hurley LH. The inefficiency of incisions of ecteinascidin 743-DNA adducts by the UvrABC nuclease and the unique structural feature of the DNA adducts can be used to explain the repair-dependent toxicities of this antitumor agent. Chem Biol 2001;8:1033-49.
33. Tu LC, Matsui SI, Beerman TA. Hedamycin, a DNA alkylator, induces (γ)H2AX and chromosome aberrations: involvement of phosphatidylinositol 3-kinase-related kinases and DNA replication fork movement. Mol Cancer Ther 2005;4:1175-85.
34. Varnes ME, Biaglow JE, Roizin-Towle L, Hall EJ. Depletion of intracellular GSH and NPSH by buthionine sulfoximine and diethyl maleate: factors that influence enhancement of aerobic radiation response. Int J Radiat Oncol Biol Phys 1984;10:1229-33.
35. Schultz LB, Chehab NH, Malikzay A, Halazonetis TD. p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J Cell Biol 2000;151:1381-90.
36. Williams RS, Moncalian G, Williams JS, et al. Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strand-break repair. Cell 2008;135:97-109.
37. Giannini G, Rinaldi C, Ristori E, et al. Mutations of an intronic repeat induce impaired MRE11 expression in primary human cancer with microsatellite instability. Oncogene 2004;23:2640-7.
38. Takemura H, Rao VA, Sordet O, et al. Defective Mre11-dependent activation of Chk2 by ataxia telangiectasia mutated in colorectal carcinoma cells in response to replication-dependent DNA double strand breaks. J Biol Chem 2006;281:30814-23.
39. Furuta T, Takemura H, Liao ZY, et al. Phosphorylation of histone H2AX and activation of Mre11, Rad50, and Nbs1 in response to replication-dependent DNA double-strand breaks induced by mammalian DNA topoisomerase I cleavage complexes. J Biol Chem 2003;278: 20303-12.
40. Meng L, Kohlhagen G, Sausville EA, Pommier Y. DNA-protein crosslinks and replication-dependent histone H2AX phosphorylation induced by aminoflavone (NSC6 86288), a novel anticancer agent active against breast cancer cells. Cancer Res 2005;65:5337-43.
41. Dimitrova DS, Gilbert DM. Temporally coordinated assembly and disassembly of replication factories in the absence of DNA synthesis. Nat Cell Biol 2000;2:686-94.
42. Seiler JA, Conti C, Syed A, Aladjem MI, Pommier Y. The intra-S-phase checkpoint affects both DNA replication initiation and elongation: single-cell and -DNA fiber analyses. Mol Cell Biol 2007;27:5806-18.
43. Conti C, Seiler J, Pommier Y. The mammalian DNA replication elongation checkpoint: implication of Chk1 and relationship with origin firing as determined by single DNA molecule and single cell analyses. Cell Cycle 2007;6:2760-7.
44. Broggini M, Marchini S, Fontana E, Moneta D, Fowst C, Geroni C. Brostallicin: a new concept in minor groove DNA binder development. Anticancer Drugs 2004;15:1-6.
45. Levenson V, Hamlin JL. A general protocol for evaluating the specific effects of DNA replication inhibitors. Nucleic Acids Res 1993;21: 3997-4004.
46. Strumberg D, Pilon AA, Smith M, Hickey R, Malkas L, Pommier Y. Conversion of topoisomerase I cleavage complexes on the leading strand of ribosomal DNA into 5′-phosphorylated DNA double-strand breaks by replication runoff. Mol Cell Biol 2000;20:3977-87.
47. Paulsen RD, Cimprich KA. The ATR pathway: fine-tuning the fork. DNA Repair (Amst) 2007;6:953-66.
48. Rao VA, Conti C, Guirouilh-Barbat J, et al. Endogenous ã-H2AX-ATM-Chk2 checkpoint activation in Bloom's syndrome helicase deficient cells is related to DNA replication arrested forks. Mol Cancer Res 2007;5:713-24.
49. Antony S, Agama KK, Miao ZH, et al. Novel indenoisoquinolines NSC 725776 and NSC724 998 produce persistent topoisomerase I cleavage complexes and overcome multidrug resistance. Cancer Res 2007;67:10397-405.