Evidence for different mechanisms of 'unhooking' for melphalan and cisplatin-induced DNA interstrand cross-links in vitro and in clinical acquired resistant tumour samples

BMC Cancer

Volumn 12, Issue , 2012, Pages

  Spanswick, Victoria J ^a   Lowe, Helen L ^a   Newton, Claire ^a   Bingham, John P ^a   Bagnobianchi, Alessia ^a   Kiakos, Konstantinos ^a   Craddock, Charles ^b   Ledermann, Jonathan A ^c   Hochhauser, Daniel ^a   Hartley, John A ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b QUEEN ELIZABETH HOSPITAL   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Acquired drug resistance; Cisplatin; DNA cross linking agent; DNA damage response; DNA interstrand cross linking; DNA repair; Melphalan; Multiple myeloma; Ovarian cancer

Indexed keywords

CISPLATIN; GAMMA HISTONE H2AX; GEMCITABINE; HISTONE H2AX; MELPHALAN; RAD51 PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CANCER RESISTANCE; COMET ASSAY; CONTROLLED STUDY; DNA CROSS LINKING; DNA DAMAGE; DNA MODIFICATION; DNA STRAND; DRUG EFFECT; DRUG MECHANISM; GEL ELECTROPHORESIS; GENE EXPRESSION; GENE IDENTIFICATION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IN VITRO STUDY; MOLECULAR DYNAMICS; ONCOGENE; PLASMA CELL; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SENSITIVITY ANALYSIS; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; CISPLATIN; DEOXYCYTIDINE; DNA; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DRUG RESISTANCE, NEOPLASM; FEMALE; HISTONES; HOMOLOGOUS RECOMBINATION; HUMANS; MELPHALAN; MULTIPLE MYELOMA; OVARIAN NEOPLASMS; RAD51 RECOMBINASE; SIGNAL TRANSDUCTION;

EID: 84866722920     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-12-436     Document Type: Article

References (32)

1. Hartley JA. Alkylating agents. Oxford Textbook of Oncology 2001, 639-654. Oxford: Oxford University Press, Souhami RL, Tannock I, Hohenberger P, Horiot JC, 2.
2. Kelland L. The resurgence of platinum based cancer therapy. Nat Rev Cancer 2007, 7:573-584. 10.1038/nrc2167, 17625587.
3. Hartley JA. The development of pyrrolobenzodiazepines as antitumor agents. Expert Opin Investig Drugs 2011, 20:733-744. 10.1517/13543784.2011.573477, 21457108.
4. Puzanov I, Lee W, Chen AP, Calcutt MW, Hachey DL, Vermeulen WL, Spanswick VJ, Liao C-Y, Hartley JA, Berlin JD, Rothenberg ML. Phase I, pharmacokinetic and pharmacodynamic study of SJG-136, a novel DNA sequence selective minor groove cross-linking agent, in advanced solid tumors. Clinical. Cancer Res 2011, 17:3794-3802.
5. 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. 10.1128/MCB.20.21.7980-7990.2000, 86408, 11027268.
6. Clingen PH, De Silva IU, McHugh PJ, Ghadessy FJ, Tilby MJ, Thurston DE, Hartley JA. The XPF-ERCC1 endonuclease and homologous recombination contribute to the repair of minor groove DNA interstrand crosslinks in mammalian cells produced by the pyrrolo[2,1-c][1,4]benzodiazepine dimer SJG-136. Nucleic Acids Res 2005, 33:3283-3291. 10.1093/nar/gki639, 1145189, 15944449.
7. Dronkert ML, Kanaar R. Repair of DNA interstrand cross-links. Mutation Res 2001, 486:217-247. 10.1016/S0921-8777(01)00092-1, 11516927.
8. O'Connor PM, Kohn KW. Comparative pharmacokinetics of DNA lesion formation and removal following treatment of L1210 cells with nitrogen mustards. Cancer Commun 1990, 2:387-394.
9. Sunters A, Springer CJ, Bagshawe KD, et al. The cytotoxicity, DNA crosslinking ability and DNA sequence selectivity of the aniline mustards melphalan, chlorambucil and 4-[bis(2-chloroethyl)amino]benzoic acid. Biochem Pharmacol 1992, 44:59-64. 10.1016/0006-2952(92)90038-K, 1632839.
10. Spanswick VJ, Craddock C, Sekhar M, et al. Repair of DNA interstrand crosslinks as a mechanism of clinical resistance to melphalan in multiple myeloma. Blood 2002, 100:224-229. 10.1182/blood.V100.1.224, 12070031.
11. Torres-Garcia SJ, Cousineau L, Caplan S, et al. Correlation of resistance to nitrogen mustards in chronic lymphocytic leukaemia with enhanced removal of melphalan-induced DNA crosslinks. Biochem Pharmacol 1989, 38:3122-3123. 10.1016/0006-2952(89)90025-7, 2783167.
12. Wynne P, Newton C, Ledermann JA, et al. Enhanced repair of DNA interstrand crosslinking in ovarian cancer cells from patients following treatment with platinum-based chemotherapy. Br J Cancer 2007, 97:927-933. 2360410, 17848946.
13. McHugh PJ, Spanswick VJ, Hartley JA. Repair of DNA interstrand crosslinks: molecular mechanisms and clinical relevance. Lancet Oncol 2001, 2:483-490. 10.1016/S1470-2045(01)00454-5, 11905724.
14. McCabe KM, Olson SB, Moses RE. DNA interstrand crosslink repair in mammalian cells. J Cell Physiol 2009, 220:569-573. 10.1002/jcp.21811, 2760924, 19452447.
15. Niedernhofer LJ, Odijk H, Budzowska M, et al. The structure-specific endonuclease Ercc1-XPF is required to resolve DNA interstrand cross-link-induced double-strand breaks. Mol Cell Biol 2004, 24:5776-5787. 10.1128/MCB.24.13.5776-5787.2004, 480908, 15199134.
16. Wang AT, Sengerova B, Cattell E, Inagawa T, Hartley JM, Kiakos K, Burgess-Brown NA, Swift LP, Enzlin JH, Schofield CJ, Gileadi O, Hartley JA, McHugh PJ. Human SNM1A collaborates with XPF-ERCC1 to initiate DNA interstrand cross-link repair. Genes Dev 2011, 25:1859-1870. 10.1101/gad.15699211, 3175721, 21896658.
17. Crossan GP, Patel KJ. The Fanconi anaemia pathway orchestrates incisions at sites of crosslinked DNA. J Pathol 2012, 226:326-337. 10.1002/path.3002, 21956823.
18. Beherns BC, Hamilton TC, Masuda H, et al. Characterisation of a cis-Diamminedichloroplatinum(II)-resistant human ovarian cancer cell line and its use in evaluation of platinum analogues. Cancer Res 1987, 47:414-418.
19. Spanswick VJ, Hartley JM, Hartley JA. Measurement of DNA interstrand crosslinking in individual cells using the single cell gel electrophoresis (comet) assay. Methods in Molecular Biology, Vol 613 Drug-DNA Interaction Protocols 2010, 267-282. Totowa NJ: Humana Press, Fox K.
20. Olive PL, Banath JP, Durand RE. Heterogeneity in radiation-induced DNA damage and repair in tumour and normal cells measured using the " comet" assay. Radiat Res 1990, 122:86-94. 10.2307/3577587, 2320728.
21. Clingen PH, Wu JY-H, Miller J, et al. Histone H2AX phosphorylation as a molecular pharmacological marker for DNA interstrand crosslink cancer chemotherapy. Biochem Pharmacol 2008, 76:19-27. 10.1016/j.bcp.2008.03.025, 18508035.
22. Jansen BA, Brouwer J, Reedijk J. Glutathione induces cellular resistance against cationic dinuclear platinum anticancer drugs. J Inorg Biochem 2002, 89:197-202. 10.1016/S0162-0134(02)00381-1, 12062123.
23. Lu X, Errington J, Curtin NJ, Lunec J, Newell DR. The impact of p53 status on cellular sensitivity to antifolate drugs. Clin Cancer Res 2001, 7:2114-2123.
24. Teoh G, Tai Y-T, Urashima M, Shirahama S, et al. CD40 activation mediates p53-dependent cell cycle regulation in human multiple myeloma cell lines. Blood 2000, 95:1039-1046.
25. Bergman AM, Ruiz van Haperen VW, Veerman G, Kuiper CM, Peters GJ. Synergistic interaction between cisplatin and gemcitabine in vitro. Clin Cancer Res 1996, 2:521-530.
26. Nagourney RA, Brewer CA, Radecki S, et al. Phase II trial of gemcitabine plus cisplatin repeating doublet therapy in previously treated, relapsed ovarian cancer patients. Gynecol Oncol 2003, 88:35-39. 10.1006/gyno.2002.6855, 12504624.
27. Rose PG, Mossbruger K, Fusco N, Smrekar M, Eaton S, Rodriguez M. Gemcitabine reverses cisplatin resistance: Demonstration of activity in platinum- and multidrug-resistant ovarian and peritoneal carcinoma. Gynecol Oncol 2003, 88:17-21. 10.1006/gyno.2002.6850, 12504621.
28. Ledermann JA, Gabra H, Jayson GC, et al. Carboplatin and gemcitabine in patients with 'platinum-resistant' ovarian cancer: demonstration of inhibition of carboplatin-induced DNA interstrand crosslink repair by gemcitabine. Clinical Cancer Res 2010, 16:4899-4905.
29. Moufarij MA, Sampath D, Keating MJ, Plunkett W. Fludarabine increases oxaliplatin cytotoxicity in normal and chronic lymphocytic leukemia lymphocytes by suppressing interstrand DNA crosslink removal. Blood 2006, 108:4187-4193. 10.1182/blood-2006-05-023259, 1895455, 16954499.
30. Shammas MA, Shmookler Reis RJ, Koley H, Batchu RB, Li C, Munshi NC. Dysfunctional homologous recombination mediates genomic instability and progression in myeloma. Blood 2009, 113:2290-2297. 10.1182/blood-2007-05-089193, 2652372, 19050310.
31. Deans AJ, West SC. DNA interstrand crosslink repair and cancer. Nat Rev Cancer 2011, 11:467-480. 10.1038/nrc3088, 21701511.
32. De Silva IU, McHugh PJ, Clingen PH, Hartley JA. Defects in interstrand cross-link uncoupling do not account for the extreme sensitivity of ERCC1 and XPF cells to cisplatin. Nucleic Acids Res 2002, 30:3848-3856. 10.1093/nar/gkf479, 137407, 12202770.