Have a personal or library account? Click to login

Cisplatin and beyond: molecular mechanisms of action and drug resistance development in cancer chemotherapy

Open Access
|Mar 2019

References

  1. Rosenberg B, Van Camp L, Grimley EB, Thomson AJ. The inhibition of growth or cell division in Escherichia coli by different ionic species of platinum(IV) complexes. J Biol Chem 1967; 242: 1347-52. PMID: 5337590
  2. Rosenberg B. Van Camp L, Trosko JE, Mansour VH. Platinum compounds: a new class of potent antitumor agents. Nature 1969; 222: 385-6. PMID: 5782119
  3. Peyrone M. Über die einwirkungdes ammoniaks auf platichlorür. Annalen der chemie und pharmacie 1844; 51: 1-29. 10.1002/jlac.18440510102
  4. Rosenberg B. Some biological effects of platinum compounds. New agents for the control of tumours. Platinum Met Rev 1971; 15: 42-51.
  5. Apps MG, Choi EHY, Wheate NJ. The state-of-play and future of platinum drugs. Endocr Relat Cancer 2015; 22: R219-33. 10.1530/ERC-15-0237
  6. Dabrowiak JC. Metals in medicine 2nd edition. John Wiley & Sons Ltd; 2017. p. 94-5.
  7. Sooriyaarachchi M, Narendran A. Gailer J. Comparative hydrolysis and plasma protein binding of cisplatin and carboplatin in human plasma in vitro. Metallomics 2011; 3: 49-55. 10.1039/c0mt00058b
  8. Handing KB, Shabalin IG, Kassaar O, Khazaipoul S, Blindauer CA, Stewart AJ, et al. Circulatory zinc transport is controlled by distinct interdomain sites on mammalian albumins. Chem Sci Chem 2016; 7: 6635-48. 10.1039/c6sc02267g
  9. Hu W, Luo Q, Wu K, Li X, Wang F, Chen Y, et al. The anticancer drug cisplatin can crosslink the interdomain zinc site on human albumin. Chem Commun (Camb) 2011; 47: 6006-8. 10.1039/c1cc11627d
  10. Martinčič A, Cemazar M, Serša G, Kovač V, Milačič R, Ščančar J. A novel method for speciation of Pt in human serum incubated with cisplatin, oxaliplatin and carboplatin by conjoint liquid chromatography on monolithic disks with UV and ICP-MS detection. Talanta 2013; 116: 141-8. 10.1016/j.talanta.2013.05.016
  11. Eljack ND, Ma HY, Drucker J, Shen C, Hambley TW, New EJ, et al. Mechanisms of cell uptake and toxicity of the anticancer drug cisplatin. Metallomics 2014; 6: 2126-33. 10.1039/c4mt00238e
  12. Hall MD, Okabe M, Shen DW, Liang XJ, Gottesman MM. The role of cellular accumulation in determining sensitivity to platinum-based chemotherapy. Annu Rev Pharmacol Toxicol 2008; 48: 495-535. 10.1146/annurev.pharmtox.48.080907.180426
  13. Eljack ND, Ma MH, Drucker J, Shen C, Hambley TW, New JE, et al. Mechanisms of cell uptake and toxicity of the anticancer drug cisplatin. Metallomics 2014; 6: 2126-33. 10.1039/c4mt00238e
  14. Lasorsa A, Natile G, Rosato A, Tadini-Buoninsegni F, Arnesano F. Monitoring interactions inside cells by advanced spectroscopies: overview of copper transporters and cisplatin. Curr Med Chem 2018; 25: 462-77. 10.2174/0929867324666171110141311
  15. Holzer AK, Howell SB. The internalization and degradation of human copper transporter 1 following cisplatin exposure. Cancer Res 2006; 66: 10944-52. 10.1158/0008-5472.CAN-06-1710
  16. Ivy KD, Kaplan JH. A re-evaluation of the role of hCTR1, the human high-affinity copper transporter, in platinum-drug entry into human cells. Mol Pharmacol 2013; 83: 1237-46. 10.1124/mol.113.085068
  17. Arnesano F, Seintilla S, Natile G. Interaction between platinum complexes and a methionine motif found in copper transport proteins. Angew Chem Int Ed Engl 2007; 46: 9062-4. 10.1002/anie.200703271
  18. Yonezawa A, Masuda S, Yokoo S, Katsura T, Inui K. Cisplatin and oxaliplatin, but not carboplatin and nedaplatin, are substrates for human organic cation transporters (SLC22A1-3 and multidrug and toxin extrusion family). J Pharmacol Exp Ther 2006; 319: 879-86. 10.1124/jpet.106.110346
  19. Nieskens TTG, Peters JGP, Dabaghie D, Korte D, Jansen K, Van Asbeck AH, et al. Expression of organic anion transporter 1 or 3 in human kidney proximal tubule cells reduces cisplatin sensitivity. Drug Metab Dispos 2018; 46: 5929. 10.1124/dmd.117.079384
  20. Ciarimboli G. Membrane transporters as mediators of cisplatin side-effects. Anticancer Res 2014; 34: 547-50. PMID: 24403515.
  21. Calandrini V, Arnesano F, Galliani A, Nguyen TH, Ippoliti E, Carloni P, et al. Platination of the copper transporter ATP7A involved in anticancer drug resistance. Dalton Trans 2014; 43: 12085-94. 10.1039/c4dt01339e
  22. Aggarwal A, Bhatt M. Advances in treatment of Wilson disease. Tremor Other Hyperkinet Mov (NY) 2018; 8: 525. 10.7916/D841881D
  23. Ferreira CR, Gahl WA. Disorders of metal metabolism. Transl Sci Rare Dis 2017; 2: 101-39. 10.3233/TRD-170015
  24. Tadini-Buoninsegni F, Bartolommei G, Moncelli MR, Inesi G, Galliani A, Sinisi M, et al. Translocation of platinum anticancer drugs by human copper ATPases ATP7A and ATP7B. Angew Chem Int Ed Engl 2014; 53: 1297-301. 10.1002/anie.201307718
  25. Hishikawa Y, Abe S, Kinugasa S, Yoshimura H, Monden N, Igarashi M, et al. Overexpression of metallothionein correlates with chemo resistance to cisplatin and prognosis in oesophageal cancer. Oncology 1997; 54: 342-7. 10.1159/000227714
  26. Ishikawa T, Ali-Osman F. Glutathione-associated cis-diamminedichloroplatinum(II) metabolism and ATP-dependent efflux from leukaemia cells. Molecular characterization of glutathione-platinum complex and its biological significance. J Biol Chem 1993; 268: 20116-25. PMID: 8376370.
  27. Chen HH, Kuo MT. Role of glutathione in the regulation of cisplatin resistance in cancer chemotherapy. Met Based Drugs 2010; pii: 430939. 10.1155/2010/430939
  28. Sauzay C, White-Koning M, Hennebelle I, Deluche T, Delmas C, Imbs DC, et al. Inhibition of OCT2, MATE1 and MATE2-K as a possible mechanism of drug interaction between pazopanib and cisplatin. Pharmacol Res 2016; 110: 89-95. 10.1016/j.phrs.2016.05.012
  29. Sprowl JA, Ness RA, Sparreboom A. Polymorphic transporters and platinum pharmacodynamics. Drug Metab Pharmacokinet 2013; 28: 19-27. PMID: 22986709
  30. Filipski KK, Mathijssen RH, Mikkelsen TS, Schinkel AH, Sparreboom A. Contribution of organic cation transporter 2 (OCT2) to cisplatin-induced nephrotoxicity. Clin Pharmacol Ther 2009; 86: 396-402. 10.1038/clpt.2009.139
  31. Tzvetkov MV, Behrens G, O’Brien VP, Hohloch K, Brockmöller J, Benöhr P. Pharmacogenetic analyses of cisplatin-induced nephrotoxicity indicate a renoprotective effect of ERCC1 polymorphisms. Pharmacogenomics 2011; 12: 1417-27. 10.2217/pgs.11.93
  32. Hsu CM, Lin PM, Chang JG, Lin HC, Li SH, Lin SF, et al. Upregulated SLC22A3 has a potential for improving survival of patients with head and neck squamous cell carcinoma receiving cisplatin treatment. Oncotarget 2017; 8: 74348-58. 10.18632/oncotarget.20637
  33. Chen Y, Teranishi K, Li S, Yee SW, Hesselson S, Stryke D, et al. Genetic variants in multidrug and toxic compound extrusion-1, hMATE1, alter transport function. Pharmacogenomics J 2009; 9: 127-36. 10.1038/tpj.2008.19
  34. Au WW, Salama SA, Sierra-Torres CH. Functional characterization of polymorphisms in DNA repair genes using cytogenetic challenge assays. Environ Health Perspect 2003; 111: 1843-50. 10.1289/ehp.6632
  35. Osawa K. Gene polymorphisms and chemotherapy in non-small cell lung cancer. Zhongguo Fei Ai Za Zhi 2009; 12: 837-40. 10.3779/j.issn.1009-3419.2009.08.01
  36. de las Peñas R, Sanchez-Ronco M, Alberola V, Taron M. Camps C, Garcia-Carbonero R, et al. Polymorphisms in DNA repair genes modulate survival in cisplatin/gemcitabine-treated non-small-cell lung cancer patients. Ann Oncol 2006; 17(4): 668-75. 10.1093/annonc/mdj135
  37. Saldivar JS, Lu KH, Liang D, Gu J, Huang M, Vlastos AT, et al. Moving toward individualized therapy based on NER polymorphisms that predict platinum sensitivity in ovarian cancer patients. Gynecol Oncol 2007; 107(1 Suppl 1): S223-9. 10.1016/j.ygyno.2007.07.024
  38. Goričar K, Kovač V, Jazbec J, Zakotnik B, Lamovec J, Dolžan V. Genetic variability of DNA repair mechanisms and glutathione-S-transferase genes influences treatment outcome in osteosarcoma. Cancer Epidemiol 2015; 39: 182-8. 10.1016/j.canep.2014.12.009
  39. Deng JH, Deng J, Shi DH, Ouyang XN, P.-G. Niu PG. Clinical outcome of cisplatin-based chemotherapy is associated with the polymorphisms of GSTP1 and XRCC1 in advanced nonsmall cell lung cancer patients. Clin Transl Oncol 2015; 17: 720-6. 10.1007/s12094-015-1299-6
  40. Izquierdo MA, Scheffer GL, Flens MJ, Giaccone G, Broxterman HJ, Meijer CJ, et al. Broad distribution of the multidrug resistance-related vault lung resistance protein in normal human tissues and tumours. Am J Pathol 1996; 148: 877-87. PMID: 8774142.
  41. Sedláková I, Laco J, Caltová K, Červinka M, Tošner J, Řezáč A, et al. Clinical significance of the resistance proteins LRP, Pgp, MRP1, MRP3, and MRP5 in epithelial ovarian cancer. Int J Gynecol Cancer 2015; 25(2): 236-43. 10.1097/IGC.0000000000000354
  42. Zhao YN, He DN, Wang YD, Li JJ, Ha MW. Association of single nucleotide polymorphisms in the MVP gene with platinum resistance and survival in patients with epithelial ovarian cancer. Oncol Lett 2016; 11(4): 2925-33. 10.3892/ol.2016.4311
  43. Makrilia N, Syrigou E, Kaklamanos I, Manolopoulos L, Wasif Saif M. Hypersensitivity reactions associated with platinum antineoplastic agents: a systematic review. Metal-Based Drugs 2010; 2010: 1-11. 10.1155/2010/207084
  44. Lafay-Cousin L, Sung L, Carret AS, Hukin J, Wilson B, Johnston DL, et al. Carboplatin hypersensitivity reaction in paediatric patients with low-grade glioma: a Canadian paediatric brain tumour consortium experience. Cancer 2008; 112: 892-9. 10.1002/cncr.23249
  45. Markman M, Moon J, Wilczynski S, Lopez AM, Rowland KM Jr, Michelin DP, et al. Single agent carboplatin versus carboplatin plus PEGylated liposomal doxorubicin in recurrent ovarian cancer: final survival results of a SWOG (S0200) phase 3 randomized trial. Gynecol Oncol 2010; 116: 323-5. 10.1016/j.ygyno.2009.11.026
  46. van Meerten E, Franckena M, Wiemer E, van Doorn L, Kraan J, Westermann A, et al. Phase I study of cisplatin, hyperthermia, and lapatinib in patients with recurrent carcinoma of the uterine cervix in a previously irradiated area. Oncologist 2015; 20: 241-2. 10.1634/theoncologist.2014-0365
  47. Landon CD. Enhancing cisplatin delivery and anti-tumour efficacy using hyperthermia. [Dissertation]. Durcham: Duke University; 2013.
  48. Rose PG, Bundy BN, Watkins EB, Thigpen JT, Deppe G, Maiman MA, et al. Concurrent cisplatin-based radiotherapy and chemotherapy for locally advanced cervical cancer. N Engl J Med 1999; 340: 3144-53. 10.1056/NEJM199904153401502
  49. Biston MC, Joubert A, Adam JF, Elleaume H, Bohic S, Charvet AM, et al. Cure of Fisher rats bearing radio resistant F98 glioma treated with cis-platinum and irradiated with monochromatic synchrotron X-rays. Cancer Res 2004; 64: 2317-23. 10.1158/0008-5472.CAN-03-3600
  50. Coluccia D, Figueiredo CA, Wu MY, Riemenschneider AN, Diaz R, Luck A, et al. Enhancing glioblastoma treatment using cisplatin-gold-nanoparticle conjugates and targeted delivery with magnetic resonance-guided focused ultrasound. Nanomedicine 2018; 14: 1137-48. 10.1016/j.nano.2018.01.021
  51. Schumann C, Chan S, Millar JA, Bortnyak Y, Carey K, Fedchyk A, et al. Intraperitoneal nanotherapy for metastatic ovarian cancer based on siRNA-mediated suppression of DJ-1 protein combined with a low dose of cisplatin. Nanomedicine 2018; 14: 1395-405. 10.1016/j.nano.2018.03.005
  52. Setua S, Ouberai M, Piccirillo SG, Watts C, Welland M. Cisplatin-tethered gold nanospheres for multimodal chemo-radiotherapy of glioblastoma. Nanoscale 2014; 6: 10865-73. 10.1039/c4nr03693j
  53. Shahin SA, Wang R, Simargi SI, Glackin CA. Hyaluronic acid conjugated nanoparticle delivery of siRNA against TWIST reduces tumour burden and enhances sensitivity to cisplatin in ovarian cancer. Nanomedicine 2017; 13: 965-76. 10.1016/j.nano.2018.04.00
  54. Joybari AY, Sarbaz S, Azadeh P, Mirafsharieh SA, Rahbari A, Farasatinasab M, et al. Oxaliplatin-induced renal tubular vacuolization. Ann Pharmacother 2014; 4: 796-800. 10.1177/1060028014526160
  55. Hellberg V, Wallin I, Eriksson S, Hernlund E, Jerremalm E, Berndtsson M, et al. Cisplatin and oxaliplatin toxicity: importance of cochlear kinetics as a determinant for ototoxicity. J Natl Cancer Inst 2009; 101: 37-47. 10.1093/jnci/djn418
  56. Hosnedlova B, Kepinska M, Skalickova S, Fernandez C, Ruttkay-Nedecky B, Peng Q, et al. Nano-selenium and its nanomedicine applications: a critical review. Int J Nanomedicine 2018; 13: 2107-28. 10.2147/IJN.S157541
  57. Boulikas T, Stathopoulos GP, Volakakis N, Vougiouka M. Systemic Lipoplatin infusion results in preferential tumor uptake in human studies. Anticancer Res 2005; 25: 3031-40. PMID: 16080562
  58. Serinan E, Altun Z, Aktaş S, Çeçen E, Olgun N. Comparison of cisplatin with lipoplatin in terms of ototoxicity. J Int Adv Otol 2018; 14: 211-5. 10.5152/iao.2018.4097
  59. Serša G, Čemažar M, Miklavčič D. Antitumor effectiveness of electrochemotherapy with cis-diamminedichloroplatinum(II) in mice. Cancer Res 1995; 55: 3450-5. PMID: 7614485
  60. Serša G, Stabuc B, Cemazar M, Miklavcic D, Rudolf Z. Electrochemotherapy with cisplatin: Clinical experience in malignant melanoma patients. Clin Cancer Res 2000; 6: 863-7. PMID: 107417
  61. Gehl J, Sersa G, Wichmann Matthiessen L, Muir T, Soden D, Occhini A, et al. Updated standard operating procedures for electrochemotherapy of cutaneous tumours and skin metastases. Acta Oncol 2018, 57: 874-882. 10.1080/0284186X.2018.1454602
  62. Kranjc S, Cemazar M, Sersa G, Scancar J, Grabner S. In vitro and in vivo evaluation of electrochemotherapy with trans-platinum analogue trans-[PtCl2(3-Hmpy)2]. Radiol Oncol 2017; 51: 295-306. 10.1515/raon-2017-0034
  63. Grabner S, Modec B, Bukovec N, Bukovec P, Čemažar M, Kranjc S, et al. Cytotoxic trans-platinum(II) complex with 3-hydroxymethylpyridine: Synthesis, X-ray structure and biological activity evaluation. J Inorg Biochem 2016; 161: 40-51. 10.1016/j.jinorgbio.2016.04.031
  64. Sancho-Martínez SM, Prieto-García L, Prieto M, López-Novoa JM, López-Hernández FJ. Subcellular targets of cisplatin cytotoxicity: an integrated view. Pharmacol Ther 2012; 136: 35-55. 10.1016/j.pharmthera.2012.07.003
  65. Rebillard A, Tekpli X, Meurette O, Sergent O, LeMoigne-Muller G, Vernhet L, et al. Cisplatin-induced apoptosis involves membrane fluidification via inhibition of NHE1 in human colon cancer cells. Cancer Res 2007; 67: 7865-74. 10.1158/0008-5472.CAN-07-0353
  66. Bose RN, Yang WW, Evanics F. Structural perturbation of a C4 zinc-finger module by cis-diamminedichloroplatinum(II): insights into the inhibition of transcription processes by the antitumor drug. Inorganica Chim Acta 2005; 358: 2844-54. org/10.1016/j.ica.2004.06.052
  67. Huang X, Huang R, Gou S, Wang Z, Liao Z, Wang H. Combretastatin A-4 analogue: a dual-targeting and tubulin inhibitor containing antitumor Pt(IV) moiety with a unique mode of action. Bioconjugate Chem 2016; 27: 2132-48. 10.1021/acs.bioconjchem.6b00353
  68. Ishikawa T, Ali-Osman F. Glutathione-associated cis-diamminedichloro-platinum(II) metabolism and ATP-dependent efflux from leukaemia cells. Molecular characterization of glutathione-platinum complex and its biological significance. J Biol Chem 1993; 268: 20116-25. PMID: 8376370
  69. Hostetter AA, Osborn MF, DeRose VJ. RNA-Pt adducts following cisplatin treatment of Saccharomyces cerevisiae. ACS Chem Biol 2012; 7: 218-25. 10.1021/cb200279p
  70. Wolters DA, Stefanopoulou M, Dyson PJ, Groessl M. Combination of metallomics and proteomics to study the effects of the metallodrug RAPTA-T on human cancer cells. Metallomics 2012; 4: 1185-96. 10.1039/c2mt20070h
  71. Palermo G, Magistrato A, Riedel T, von Erlach T, Davey CA, Dyson PJ, et al. Fighting cancer with transition metal complexes: from naked DNA to protein and chromatin targeting strategies. Chem Med Chem 2016; 11: 1199-210. 10.1002/cmdc.201500478
  72. Zou T, Lum CT, Lok CN, Zhang JJ, Che CM. Chemical biology of anticancer gold(III) and gold(I) complexes. Chem Soc Rev 2015; 44: 8786-801. 10.1039/c5cs00132c
  73. Molter A, Kathrein S, Kircher B, Mohr F. Anti-tumour active gold(I), palladium(II) and ruthenium(II) complexes with thio- and selenoureato ligands: a comparative study. Dalton Trans 2018; 47: 5055. 10.1039/C7DT04180B
  74. Tshuva EY, Miller M. Coordination complexes of titanium(IV) for anticancer therapy. Met Ions Life Sci 2018; 18. 10.1515/9783110470734-014
  75. Cini M, Bradshaw TD, Woodward S. Using titanium complexes to defeat cancer: the view from the shoulders of titans. Chem Soc Rev 2017; 4: 1040-51. 10.1039/c6cs00860g
  76. Meléndez E. Titanium complexes in cancer treatment. Crit Rev Oncol Hematol 2002; 42: 309-15. 10.1016/S1040-8428(01)00224-4
  77. Ang DL, Gordon CP, Aldrich-Wright JR. Transition metal intercalators as anticancer agents - recent advances. Int J Mol Sci 2016; 17: 1-17. 10.3390/ijms17111818
DOI: https://doi.org/10.2478/raon-2019-0018 | Journal eISSN: 1581-3207 | Journal ISSN: 1318-2099
Language: English
Page range: 148 - 158
Submitted on: Jul 20, 2018
Accepted on: Sep 5, 2018
Published on: Mar 28, 2019
Published by: Association of Radiology and Oncology
In partnership with: Paradigm Publishing Services
Publication frequency: 4 issues per year

© 2019 Tomaz Makovec, published by Association of Radiology and Oncology
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.