Cancer Treatment Reviews
Volume 28, Issue 6 , Pages 291-303 , December 2002

DNA-based drug interactions of cisplatin

  • M Crul

      Affiliations

    • The Netherlands Cancer Institute, Amsterdam, The Netherlands
    • Slotervaart Hospital, Amsterdam, The Netherlands
    • Corresponding Author InformationCorrespondence to: M. Crul, Department of Pharmacy and Pharmacology, Slotervaart Hospital, Louwesweg 6, 1066 EC Amsterdam, The Netherlands, Tel.: +31-20-5124481; Fax: +31-20-5124753
  • ,
  • R.C.A.M van Waardenburg

      Affiliations

    • The Netherlands Cancer Institute, Amsterdam, The Netherlands
    • St. Jude Children’s Research Hospital, Memphis, USA
  • ,
  • J.H Beijnen

      Affiliations

    • Slotervaart Hospital, Amsterdam, The Netherlands
    • Division of Drug Toxicology, Faculty of Pharmacy, Utrecht University, Utrecht, The Netherlands
  • ,
  • J.H.M Schellens

      Affiliations

    • The Netherlands Cancer Institute, Amsterdam, The Netherlands
    • Division of Drug Toxicology, Faculty of Pharmacy, Utrecht University, Utrecht, The Netherlands

References 

  1. Loehrer S, Einhorn ADJ. Diagnosis and treatment: drugs five years later: Cisplatin. Ann. Int. Med. 1984;100:704–713
  2. Chu G. Cellular responses to cisplatin. The roles of DNA-binding proteins and DNA repair. J. Biol. Chem. 1994;269:787–790
  3. Roberts JM, Knox RJ, Friedlos F, Lydall DA. DNA as the target for the cytotoxic and anti-tumour action of platinum coordination complexes: comparative in vitro and in vivo studies of cisplatin and carboplatin. In:  McBrien DCH,  Slater TF editor. Biochemical Mechanisms of Platinum Antitumour Drugs. Oxford: IRL Press; 1986;p. 29
  4. Eastman A. The formation, isolation and characterization of DNA adducts produced by anticancer platinum complexes. Pharmacol. Ther. 1987;34:155–166
  5. Eastman A. Activation of programmed cell death by anticancer agents: cisplatin as a model system. Cancer Cells. 1990;2:275–280
  6. Gately DP, Howell SB. Cellular accumulation of the anticancer agent cisplatin: a review. Br. J. Cancer. 1993;67:1171–1176
  7. Kondo Y, Kuo SM, Watkins SC, Lazo JS. Metallothionein localization and cisplatin resistance in human hormone-independent prostatic tumor cell lines. Cancer Res. 1995;55:474–477
  8. Mistry P, Kelland LR, Abel G, Sidhar S, Harrap KR. The relationships between glutathione, glutathione-S-transferase and cytotoxicity of platinum drugs and melphalan in eight human ovarian carcinoma cell lines. Br. J. Cancer. 1991;64:215–220
  9. Perego P, Giarola M, Righetti SC, et al.  Association between cisplatin resistance and mutation of p53 gene and reduced bax expression in ovarian carcinoma cell systems. Cancer Res. 1996;56:556–562
  10. Zamble DB, Lippard SJ. Cisplatin and DNA repair in cancer chemotherapy. Trends Biochem. Sci. 1995;20:435–439
  11. Johnson SW, Perez RP, Godwin AK, et al.  Role of platinum-DNA adduct formation and removal in cisplatin resistance in human ovarian cancer cell lines. Biochem. Pharmacol. 1994;47:689–697
  12. Mu D, Hsu DS, Sancar A. Reaction mechanism of human DNA repair excision nuclease. J. Biol. Chem. 1996;271:8285–8294
  13. Sancar A. DNA excision repair. Ann. Rev. Biochem. 1996;65:43–81
  14. Friedberg EC. Relationships between DNA repair and transcription. Ann. Rev. Biochem. 1996;65:15–42
  15. Paques F, Haber JE. Multiple pathways of recombination induced by double-strand breaks in saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 1999;63:349–404
  16. Crul M, Schellens JHM, Beijnen JH, Maliepaard M. Cisplatin resistance and DNA repair. Cancer Treat. Rev. 1997;23:341–366
  17. Pinedo HM, Peters GFJ. Fluorouracil: biochemistry and pharmacology. J. Clin. Oncol. 1998;6:1653–1664
  18. Plunkett W, Huang P, Gandhi V. Metabolism and action of fludarabine phosphate. Sem. Oncol. 1990;17(5 suppl. 8):3–17
  19. Scanlon KJ, Newman EM, Lu Y, Priest DG. Biochemical basis for cisplatin and fluorouracil synergism in human ovarian carcinoma cells. Proc. Natl. Acad. Sci. USA. 1986;83:8923–8925
  20. Etienne MC, Bernard S, Fischel JL, et al.  Dose reduction without loss of efficacy for 5-fluorouracil and cisplatin combined with folinic acid. In vitro study on human head and neck carcinoma cell lines. Br. J. Cancer. 1991;63:372–377
  21. Pratesi G, Gianni L, Manzotti C, Zunino F. Sequence dependence of the antitumor and toxic effects of 5-fluorouracil and cis-diamminedichloroplatinum combination on primary colon tumors in mice. Cancer Chemother. Pharmacol. 1988;21:237–240
  22. Esaki T, Nakano S, Tatsumoto T, et al.  Inhibition by 5-fluorouracil of cis-diamminedichloroplatinum(II)-induced DNA interstrand cross-link removal in a HST-1 human squamous carcinoma cell line. Cancer Res. 1992;52:6501–6506
  23. Johnston PG, Geoffrey F, Drake J, Voeller D, Grem JL, Allegra CJ. The cellular interaction of 5-fluorouracil and cisplatin in a human colon carcinoma cell line. Eur. J. Cancer. 1996;32A:2148–2154
  24. Tanaka T, Masuda H, Naito M, Tamai H. Pretreatment with 5-fluorouracil enhances cytotoxicity and retention of DNA-bound platinum in a cisplatin resistant human ovarian cancer cell line. Anticancer Res. 2001;21:2463–2469
  25. Fujishima H, Nakano S, Masumoto N, et al.  Inhibition by 5-fluorouracil of ERCC1 and γ-glutamylcysteine synthetase messenger RNA expression in a cisplatin-resistant HST-1 human squamous carcinoma cell line. Oncol. Res. 1997;9:167–172
  26. Zaffaroni N, Orlandi L, Gornati D, De Marco C, Vaglini M, Silvestrini R. Fludarabine as a modulator of cisplatin activity in human tumour primary cultures and established cell lines. Eur. J. Cancer. 1996;32A:1766–1773
  27. Yang LY, Li L, Keating MJ, Plunkett W. Arabinosyl-2-fluoroadenine augments cisplatin cytotoxicity and inhibits cisplatin–DNA cross-link repair. Mol. Pharmacol. 1995;47:1072–1079
  28. Li L, Keating MJ, Plunkett W, Yang LY. Fludarabine-mediated repair inhibition of cisplatin-induced DNA lesions in human chronic myelogenous leukemia-blast crisis K562 cells: induction of synergistic cytotoxicity independent of reversal of apoptosis resistance. Mol. Pharmacol. 1997;52:798–806
  29. Li L, Liu X, Glassman AB, et al.  Fludarabine triphosphate inhibits nucleotide excision repair of cisplatin-induced DNA adducts in vitro. Cancer Res. 1997;57:1487–1494
  30. Bergerat JP, Drewinko B, Corry P, Barlogie B, Ho DH. Synergistic lethal effect of cis-dichlorodiammineplatinum and 1-β-d-arabinofuranosylcytosine. Cancer Res. 1981;41:25–30
  31. Berek JS, Schink JC, Knox RM. Synergistic effect of combined intraperitoneal cisplatin and cytosinearabinoside in a murine ovarian cancer model. Obstet. Gynecol. 1989;74:663–666
  32. Spriggs DR, Robbins G, Kufe DW. Effects of cis-diamminedichloroplatinum on DNA incorporation and cytotoxicity of 1-β-d-arabinofuranosylcytosine. Biochem. Pharmacol. 1986;35:4297–4302
  33. Fram RJ, Robichaud N, Bishov SD, Wilson JM. Interactions of cis-diamminedichloroplatinum (II) with 1-β-d-arabinofuranosylcytosine in LoVo colon carcinoma cells. Cancer Res. 1987;47:3360–3365
  34. Rauko P, Novotny L, Reichelova V, Balazova E. Evaluation of synergism of drugs cis-diamminedichloroplatinum (II) and arabinosylcytosine on the level of chemical interaction with DNA and on the growth of mouse leukemia. Gen. Pharmacol. 1991;22:805–810
  35. Swinnen LJ, Barnes DM, Fisher SG, Albain KS, Fisher RI, Erickson LC. 1-β-d-arabinofuranosylcytosine and hydroxyurea production of cytotoxic synergy with cis-diamminedichloroplatinum (II) and modification of platinum-induced DNA interstrand cross-linking. Cancer Res. 1989;49:1383–1389
  36. Ellerhorst JA, Frost P, Abbruzzese JL, Newman RA, Chernajovsky Y. 2-Deoxy-5-azacytidine increases binding of cisplatin to DNA by a mechanism independent of DNA hypomethylation. Br. J. Cancer. 1993;67:209–215
  37. Bergman AM, Ruiz van Haperen VWT, Veerman G, Kuiper CM, Peters GJ. Synergistic interaction between cisplatin and gemcitabine in vitro. Clin. Cancer Res. 1996;2:521–530
  38. van Moorsel CJA, Pinedo HM, Veerman G, et al.  Mechanism of synergism between cisplatin and gemcitabine in ovarian and non-small-cell lung cancer cell lines. Br. J. Cancer. 1999;80:981–990
  39. Theodossiou C, Cook JA, Fisher J, et al.  Interaction of gemcitabine with paclitaxel and cisplatin in human tumor cell lines. Int. J. Oncol. 1998;12:825–832
  40. Voigt W, Bulankin A, Muller T, et al.  Schedule-dependent antagonism of gemcitabine and cisplatin in human anaplastic thyroid cancer cells. Clin. Cancer Res. 2000;6:2087–2093
  41. van Moorsel CJA, Pinedo HM, Smid K, et al.  Schedule-dependent pharmacodynamic effects of gemcitabine and cisplatin in mice bearing Lewis lung murine non-small cell lung tumours. Eur. J. Cancer. 2000;36:2420–2429
  42. v Moorsel CJA, Kroep JR, Pinedo HM, et al.  Pharmacokinetic schedule finding study of the combination of gemcitabine and cisplatin in patients with solid tumors. Ann. Oncol. 1999;10:441–448
  43. Crul M, Schoemaker NE, Pluim D, et al. Phase I/II clinical and pharmacokinetic study of dose-intensive cisplatin and gemcitabine in patients with advanced non-small-cell lung cancer. Br J Clin Pharmacol, in press
  44. Yang LY, Li L, Jiang H, Shen Y, Plunkett W. Expression of ERCC1 antisense RNA abrogates gemcitabine-mediated cytotoxic synergism with cisplatin in human colon tumor cells defective in mismatch repair but proficient in nucleotide excision repair. Clin. Cancer Res. 2000;6:773–781
  45. van Moorsel CJA, Lakerveld B, Smid K, et al. Effects of gemcitabine on cis-platinum-DNA adduct formation and repair in a panel of gemcitabine and cisplatin sensitive or resistant human ovarian cancer cell lines, submitted
  46. Rowinsky EK, Donehower RC. The clinical pharmacology and use of antimicrotubule agents in cancer chemotherapeutics. Pharmacol. Ther. 1991;52:35–84
  47. Rowinsky EK, Gilbert MR, McGuire WP, et al.  Sequences of taxol and cisplatin: a phase I and pharmacologic study. J. Clin. Oncol. 1991;9:1692–1703
  48. Parker R, Lee KB, Dabholkar M, Bostick-Bruton F, Simms M, Reed E. Influence of taxol:cisplatin sequencing on cisplatin–DNA adduct repair in human ovarian cancer cells. Proc. Am. Assoc. Cancer Res. 1993;34:356; (abs)
  49. Kamazawa S, Kigawa J, Minagawa Y, et al.  Cellular efflux pump and interaction between cisplatin and paclitaxel in ovarian cancer cells. Oncology. 2000;59:329–335
  50. de Graaff M, Maliepaard M, Pluim D, Floot BJ, Slaper-Cortenbach IC, Schellens JH. In vitro antagonistic cytotoxic interactions between platinum drugs and taxanes on bone marrow progenitor cell CFU-GM. Anticancer Drugs. 1999;10:213–218
  51. Engblom P, Rantanen V, Kulmala J, Helenius H, Grenman S. Additive and supra-additive cytotoxicity of cisplatin–taxane combinations in ovarian carcinoma cell lines. Br. J. Cancer. 1999;79:286–292
  52. Pronk LC, Schellens JH, Planting AS, et al.  Phase I and pharmacologic study of docetaxel and cisplatin in patients with advanced solid tumors. J. Clin. Oncol. 1997;15:1071–1079
  53. Schellens JHM, Ma J, Bruno R, et al.  Pharmacokinetics of cisplatin and taxotere (docetaxel) and WBC DNA-adduct formation of cisplatin in the sequence taxotere/cisplatin and cisplatin/taxotere in a phase I/II study in solid tumor patients. Proc. Am. Assoc. Clin. Oncol. 1994;13:132; (abs)
  54. Ma J, Verweij J, Planting AST, et al.  Docetaxel and paclitaxel inhibit DNA-adduct formation and intracellular accumulation of cisplatin in human leukocytes. Cancer Chemother. Pharmacol. 1996;37:382–384
  55. Eng WK, Faucette L, Johnson RK, et al.  Evidence that DNA topoisomerase I is necessary for the cytotoxic effects of camptothecin. Mol. Pharmacol. 1988;34:755–760
  56. Hsiang YH, Lihou MG, Liu LF. Arrest of replication forks by drug-stabilized topoisomerase I-DNA cleavable complexes as a mechanism of cell killing by camptothecin. Cancer Res. 1989;49:5077–5082
  57. Schiller JH, Kim K, Hutson P, et al.  Phase II study of topotecan in patients with extensive-stage small-cell carcinoma of the lung: an Eastern Cooperative Oncology Group Trial. J. Clin. Oncol. 1996;14:2345–2352
  58. Ardizzoni A, Hansen H, Dombernowsky P, et al.  Topotecan, a new active drug in the second-line treatment of small-cell lung cancer: a phase II study in patients with refractory and sensitive disease. J. Clin. Oncol. 1997;15:2090–2096
  59. Creemers GJ, Bolis G, Gore M, et al.  Topotecan, an active drug in the second-line treatment of epithelial ovarian cancer: results of a large European phase II study. J. Clin. Oncol. 1996;14:3056–3061
  60. Hoskins P, Eisenhauer E, Beare S, et al.  Randomized phase II study of two schedules of topotecan in previously treated patients with ovarian cancer: a National Cancer Institute of Canada Clinical Trials Group study. J. Clin. Oncol. 1998;16:2233–2237
  61. Bookman MA, Malmstrom H, Bolis G, et al.  Topotecan for the treatment of advanced epithelial ovarian cancer: an open-label phase II study in patients treated after prior chemotherapy that contained cisplatin or carboplatin and paclitaxel. J. Clin. Oncol. 1998;16:3345–3352
  62. Rougier P, Bugat R, Douillard JY, et al.  Phase II study of irinotecan in the treatment of advanced colorectal cancer in chemotherapy-naive patients and patients pretreated with fluorouracil-based chemotherapy. J. Clin. Oncol. 1997;15:251–260
  63. Douillard JY, Cunningham D, Roth AD, et al.  Irinotecan combined with fluorouracil compared with fluorouracil alone as first-line treatment for metastatic colorectal cancer: a multicentre randomised trial. Lancet. 2000;355:1041–1047
  64. Cheng MF, Chatterjee S, Berger NA. Schedule-dependent cytotoxicity of topotecan alone and in combination chemotherapy regimens. Oncol. Res. 1994;6:269–279
  65. Chou TC, Motzer RJ, Tong Y, Bosl GJ. Computerized quantitation of synergism and antagonism of taxol, topotecan, and cisplatin against human teratocarcinoma cell growth: a rational approach to clinical protocol design. J. Natl. Cancer Inst. 1994;86:1517–1524
  66. Kaufmann SH, Peereboom D, Buckwalter CA, et al.  Cytotoxic effects of topotecan combined with various anticancer agents in human cancer cell lines. J. Natl. Cancer Inst. 1996;88:734–741
  67. Jonsson E, Fridborg EH, Nygren P, Larsson R. Synergistic interactions of combinations of topotecan with standard drugs in primary cultures of human tumor cells from patients. Eur. J. Clin. Pharmacol. 1998;54:509–514
  68. Janss AJ, Cnaan A, Zhao H, et al.  Synergistic cytotoxicity of topoisomerase I inhibitors with alkylating agents and etoposide in human brain tumor cell lines. Anti-Cancer Drugs. 1998;9:641–652
  69. Ma J, Maliepaard M, Nooter K, et al.  Synergistic cytotoxicity of cisplatin and topotecan or SN-38 in a panel of eight solid-tumor cell lines in vitro. Cancer Chemother. Pharmacol. 1998;41:307–316
  70. Romanelli S, Perego P, Pratesi G, Carenini N, Tortoreto M, Zunino F. In vitro and in vivo interaction between cisplatin and topotecan in ovarian carcinoma systems. Cancer Chemother. Pharmacol. 1998;41:385–390
  71. Rowinsky EK, Kaufmann SH, Baker SD, et al.  Sequences of topotecan and cisplatin: phase I, pharmacologic, and in vitro studies to examine sequence dependence. J. Clin. Oncol. 1996;14:3074–3084
  72. De Jonge MJA, Loos WJ, Gelderblom H, et al.  Phase I pharmacological study of oral topotecan and intravenous cisplatin: sequence dependent hematologic side effects. J. Clin. Oncol. 2000;18:2104–2115
  73. Kano Y, Suzuki K, Akutsu M, et al.  Effects of CPT-11 in combination with other anti-cancer agents in culture. Int. J. Cancer. 1992;50:604–610
  74. Fukuda M, Nishio K, Kanzawa F, et al.  Synergism between cisplatin and topoisomerase I inhibitors, NB-506 and SN-38, in human small cell lung cancer cells. Cancer Res. 1996;56:789–793
  75. Masumoto N, Nakano S, Esaki T, Fujishima H, Tatsumoto T, Niho Y. Inhibition of cis-diamminedichloroplatinum (II) induced DNA interstrand cross-link removal by 7-ethyl-10-hydroxy-camptothecin in HST-1 human squamous carcinoma cells. Int. J. Cancer. 1995;62:70–75
  76. Masuda M, Fukuoka M, Kudoh S, et al.  Phase I and pharmacologic study of irinotecan in combination with cisplatin for advanced lung cancer. Br. J. Cancer. 1993;68:777–782
  77. De Jonge MJA, Verweij J, Planting AST, et al.  Drug-administration sequence does not change pharmacodynamics and kinetics of irinotecan and cisplatin. Clin. Cancer Res. 1999;5:2012–2017
  78. De Jonge MJA, Verweij J, de Bruijn P, et al.  Pharmacokinetic, metabolic, and pharmacodynamic profiles in a dose-escalating study of irinotecan and cisplatin. J. Clin. Oncol. 2000;18:195–203
  79. Goldwasser F, Valenti M, Torres R, Kohn KW, Pommier Y. Potentiation of cisplatin cytotoxicity by 9-aminocamptothecin. Clin. Cancer Res. 1996;2:687–693
  80. Bendixen C, Thomsen B, Alsner J, Westergaard O. Camptothecin-stabilized topoisomerase I-DNA adducts cause premature termination of transcription. Biochemistry. 1990;29:5613–5619
  81. Zeghari-Squalli N, Raymond E, Cvitokovic E, Goldwasser F. Cellular pharmacology of the combination of the DNA topoisomerase I inhibitor SN-38 and the diaminocyclohexane platinum derivative oxaliplatin. Clin. Cancer Res. 1999;5:1189–1196
  82. Kanzawa F, Koizumi F, Koh Y, et al.  In vitro synergistic interactions between the cisplatin analogue nedaplatin and the DNA topoisomerase I inhibitor irinotecan and the mechanism of this interaction. Clin. Cancer Res. 2001;7:202–209
  83. Zdraveski ZZ, Mello JA, Farinelli CK, Essigmann JM, Marinus MG. MutS preferentially recognizes cisplatin- over oxaliplatin-modified DNA. J. Biol. Chem. 2002;277:1255–1260
  84. Van Waardenburg RCAM, de Jong LA, van Delft F, et al.  The homologous recombination pathway is essential for the synergistic cytotoxicity between cisplatin and topoisomerase I inhibitors in lower and higher eukaryotes. Proc. Am. Assoc. Cancer Res. 2001;42:3582; (abs)
  85. Van Waardenburg RCAM, de Jong LA, Maliepaard M, Verseyden C, Pluim D, Schellens JHM. Synergistic cytotoxicity between platinum drugs and topoisomerase I inhibitors is induced by direct interaction between topoisomerase I and platinum-DNA adducts, submitted
  86. Ross WE. DNA topoisomerases as targets for cancer therapy. Biochem. Pharmacol. 1985;34:4191–4195
  87. Katz EJ, Vick JS, Kling KM, Andrews PA, Howell SB. Effect of topoisomerase modulators on cisplatin cytotoxicity in human ovarian carcinoma cells. Eur. J. Cancer. 1990;26:724–727
  88. Eder JP, Teicher BA, Holden SA, Senator L, Cathcart KNS, Schnipper LE. Ability of four potential topoisomerase II inhibitors to enhance the cytotoxicity of cis-diamminedichlorplatinum (II) in chinese hamster ovary cells and in an epipodophyllotoxin resistant subline. Cancer Chemother. Pharmacol. 1990;26:423–428
  89. Ali-Osman F, Berger MS, Rajagopal S, Spence A, Livingston RB. Topoisomerase II inhibition and altered kinetics of formation and repair of nitrosourea and cisplatin-induced DNA interstrand cross-links and cytotoxicity in human glioblastoma cells. Cancer Res. 1993;53:5663–5668
  90. Adjei AA, Budihardjo II, Rowinsky EK, et al.  Cytotoxic synergy between pyrazoloacridine (NSC 366140) and cisplatin in vitro: inhibition of platinum-DNA adduct removal. Clin. Cancer Res. 1997;3:761–770
  91. Ellis GK, Crowley J, Livingston RB, Goodwin JW, Hutchins L, Allen A. Cisplatin and novobiocin in the treatment of non-small cell lung cancer. A Southwest Oncology Group study. Cancer. 1991;67:2969–2973
  92. Eder JP, Wheeler CA, Teicher BA, Schnipper LE. A phase I clinical trial of novobiocin, a modulator of alkylating agent cytotoxicity. Cancer Res. 1991;51:510–513
  93. Sibghatullah , Husain I, Carlton W, Sancar A. Human nucleotide excision repair in vitro: repair of pyrimidine dimers, psoralen and cisplatin adducts by HeLa cell-free extract. Nucleic Acids Res. 1989;17:4471–4484
  94. Larminat F, Bohr VA. Role of the human ERCC-1 gene in gene-specific repair of cisplatin-induced DNA damage. Nucleic Acids Res. 1994;22:3005–3010
  95. Schellens JH, Ma J, Planting AS, et al.  Relationship between the exposure to cisplatin, DNA-adduct formation in leucocytes and tumour response in patients with solid tumours. Br. J. Cancer. 1996;73:1569–1575
  96. Abratt RP, Sandler A, Crino L, et al.  Combined cisplatin and gemcitabine for non-small cell lung cancer: influence of scheduling on toxicity and drug delivery. Sem. Oncol. 1998;25:35–43

PII: S0305-7372(02)00093-2

Cancer Treatment Reviews
Volume 28, Issue 6 , Pages 291-303 , December 2002