Identification of the molecular mechanisms underlying the cytotoxic action of a potent platinum metallointercalator

Journal of Chemical Biology

Volumn 5, Issue 2, 2012, Pages 51-61

  Wang, Shaoyu ^a   Higgins, Vincent J ^a,b   Aldrich Wright, Janice R ^a   Wu, Ming J ^a  

^a UNIVERSITY OF WESTERN SYDNEY   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

56MESS; Anticancer; Gene; Iron; Metallointercalators; Platinum

Indexed keywords

(5,6 DIMETHYL 1,10 PHENANTHROLINE)(1,2 DIAMINOCYCLOHEXANE)PLATINUM; AMINO ACID; ANTINEOPLASTIC AGENT; CISPLATIN; SULFUR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; COPPER METABOLISM; CYTOTOXICITY; DNA BINDING; DRUG MECHANISM; GENETIC ANALYSIS; GLUTATHIONE METABOLISM; HUMAN; HUMAN CELL; IC 50; IRON METABOLISM; MOUSE; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; TRANSCRIPTOMICS;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 84865502346     PISSN: 18646158     EISSN: 18646166     Source Type: Journal    
DOI: 10.1007/s12154-011-0070-x     Document Type: Article

References (80)

1. Alic N, Felder T, Temple MD, Gloeckner C, Higgins VJ, Briza P, Dawes IW (2004) Genomewide transcriptional responses to a lipid hydroperoxide: adaptation occurs without induction of oxidant defenses. Free Radic Biol Med 37:23-35
2. Ang WH, Khalaila I, Allardyce CS, Juillerat-Jeanneret L, Dyson PJ (2005) Rational design of platinum(IV) compounds to overcome glutathione-S-transferase mediated drug resistance. J Am Chem Soc 127:1382-1383
3. Askwith C, Kaplan J (1998) Iron and copper transport in yeast and its relevance to human disease. Trends Biochem Sci 23:135-138
4. Balendiran G, Dabur R, Fraser D (2004) The role of glutathione in cancer. Cell Biochem and Funct 22:343-352
5. Barabas K, Milner R, Lurie D, Adin C (2008) Cisplatin: a review of toxicities and therapeutic applications. Vet Comp Oncol 6:1-18
6. Basu A, Krishnamurthy S (2010) Cellular responses to cisplatininduced DNA damage. J Nucleic Acids. doi:10.4061/2010/201367
7. Boyer J, Allen WL, McLean EG, Wilson PM, McCulla A, Moore S, Longley DB, Caldas C, Johnston PG (2006) Pharmacogenomic identification of novel determinants of response to chemotherapy in colon cancer. Cancer Res 66:2765-2777
8. Brodie CR, Grant Collins J, Aldrich-Wright JR (2004) DNA binding and biological activity of some platinum(II) intercalating compounds containing methyl-substituted 1,10-phenanthrolines. Dalton Trans:1145-1152
9. Caba E, Dickinson DA, Warnes GR, Aubrecht J (2005) Differentiating mechanisms of toxicity using global gene expression analysis in Saccharomyces cerevisiae. Mutat Res 575:34-46
10. Calsou P, Barret J-M, Cros S, Salles B (1993) DNA excision- repair synthesis is enhanced in a murine leukemia L1210 cell line resistant to cisplatin. Eur J Biochem 211:403-409
11. Charizanis C, Juhnke H, Krems B, Entian K (1999) The mitochondrial cytochrome c peroxidase Ccp1 of Saccharomyces cerevisiae is involved in conveying an oxidative stress signal to the transcription factor Pos9 (Skn7). Mol Gen Genet 262:437-447
12. De Virgilio C, Bürckert N, Bell W, Jenö P, Boller TAW (1993) Disruption of TPS2, the gene encoding the 100-kDa subunit of the trehalose-6-phosphate synthase/phosphatase complex in Saccharomyces cerevisiae, causes accumulation of trehalose-6-phosphate and loss of trehalose-6-phosphate phosphatase activity. Eur J Biochem 212:315-323
13. Dillon CT (2011) Synchrontron radiation x-ray spectroscopy for investigations of introcellular metallointercalators: x-ray fluorescence imaging and x-ray absorption spectroscopy. In: Aldrich- Wright JR (ed) Metallointercalators, synthesis and techniques to probe their interactions with biomolecules. Springer, New York, pp 273-298
14. Djinovic K, Gatti G, Coda A, Antolini L, Pelosi G, Desideri A, Falconi M, Marmocchi F, Rotilio GMB (1992) Crystal structure of yeast Cu, Zn superoxide dismutase. Crystallographic refinement at 2.5 A resolution. J Mol Biol 225:791-809
15. Eastman A (1999) The mechanism of action of cisplatin: from adducts to apoptosis. In: Lippert B (ed) Cisplatin: chemistry and biochemistry of a leading anticancer drug. VHCA, Zürich, pp 111- 134
16. Einhorn LH (2002) Curing metastatic testicular cancer. Proc Natl Acad Sci USA 99:4592-4595
17. Farquharson MJ, Al-Ebraheem A, Falkenberg G, Leek R, Harris AL, Bradley DA (2008) The distribution of trace elements Ca, Fe, Cu and Zn and the determination of copper oxidation state in breast tumour tissue using muSRXRF and muXANES. Phys Med Biol 53:3023-3037
18. Fisher DM, Bednarski PJ, Grünert R, Turner P, Fenton RR, Aldrich-Wright JR (2007) Chiral platinum(II) metallointercalators with potent in vitro cytotoxic activity. ChemMedChem 2:488- 495
19. Fisher DM, Fenton RR, Aldrich-Wright JR (2008) In vivo studies of a platinum(II) metallointercalator. Chem Commun 43:5613- 5615
20. Freshney R (2005) Culture of animal cells: a manual of basic technique, 5th edn. Wiley-Liss, New York, pp 359-373
21. Fu D, Beeler TJ, Dunn TM (1995) Sequence, mapping and disruption of CCC2, a gene that cross complements the Ca2+517 - sensitive phenotype of csg1 mutants and encodes a P-type ATPase belonging to the Cu2+518 -ATPase subfamily. Yeast 11:283-292
22. Gasch A, Spellman P, Kao C, Carmel-Harel O, Eisen M, Storz G, Botstein D, Brown P (2000) Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 11:4241-4257
23. Gasch AP, Huang M, Metzner S, Botstein D, Elledge SJ, Brown PO (2001) Genomic expression responses to DNA-damaging agents and the regulatory role of the yeast ATR homolog Mec1p. Mol Biol Cell 12:2987-3003
24. Georgatsou E, Alexandraki D (1994) Two distinctly regulated genes are required for ferric reduction, the first step of iron uptake in Saccharomyces cerevisiae. Mol Cell Biol 14:3065-3073
25. Gibson G, Muse SV (2009) A prime of genome science, 3rd edn. Sinauer, Sunderland, pp 191-258
26. Godwin AK, Meister A, O'dwyer PJ, Huang CS, Hamilton TC, Anderson ME (1992) High resistance to cisplatin in human ovarian cancer cell lines is associated with marked increase of glutathione synthesis. Proc Natl Acad Sci USA 89:3070-3074
27. Grant CM (2001) Role of the glutathione/glutaredoxin and thioredoxin systems in yeast growth and response to stress conditions. Mol Microbiol 39:533-541
28. Hansen J, Johannesen PF (2000) Cysteine is essential for transcriptional regulation of the sulfur assimilation genes in Saccharomyces cerevisiae. Mol Gen Genet 263:535-542
29. Head JF, Wang F, Elliott RL (1997) Antineoplastic drugs that interfere with iron metabolism in cancer cells. Adv Enzyme Regul 37:147-169
30. Heymann P, Ernst JF, Winkelmann G (2000) Identification and substrate specificity of a ferrichrome-type siderophore transporter (Arn1p) in Saccharomyces cerevisiae. FEMS Microbiol Lett 186:221-227
31. Ho PS, Hoffman BM, Solomon N, Kang CH, Margoliash E (1984) Kinetics and energetics of intramolecular electron transfer in yeast cytochrome c peroxidase. Biochemistry 23:4122-4128
32. Hu GF (1998) Copper stimulates proliferation of human endothelial cells under culture. J Cell Biochem 69:326-335
33. Ionescu JG, Novotny J, Stejskal V, Latsch A, Blaurock-Busch E, Eisenmann-Klein M (2006) Increased levels of transition metals in breast cancer tissue. Neuroendocrin Lett 21:36-39
34. Ishida S, McCormick F, Smith-McCune K, Hanahan D (2010) Enhancing tumor-specific uptake of the anticancer drug cisplatin with a copper chelator. Cancer Cell 17:574-583
35. Jaramillo D, Buck DP, Collins JG, Fenton RR, Stootman FH, Wheate NJ, Aldrich-Wright JR (2006) Synthesis, characterisation and biological activity of chiral platinum(II) complexes. Eur J Inorg Chem 2006:839-849
36. Jauniaux JC, Urrestarazu LA, Wiame JM (1978) Arginine metabolism in Saccharomyces cerevisiae: subcellular localization of the enzymes. J Bacteriol 133:1096-1107
37. Johnson SW, Ferry KV, Hamilton TC (1998) Recent insights into platinum drug resistance in cancer. Drug Resist Update 1:243-254
38. Jones EW, Fink GR (1982) Regulation of amino acid and nucleotide biosynthesis in yeast. In: Strathern JN, Jones EW, Broach JR (eds) The molecular biology of the yeast Saccharomyces: metabolism and gene expression. CSHL, New York, pp 181-299
39. Kabat GC, Rohan T (2007) Does excess iron play a role in breast carcinogenesis? An unresolved hypothesis. Cancer Cause Control 18:1047-1053
40. Kelland LR (2007) The resurgence of platinum-based cancer chemotherapy. Nat Rev Cancer 7:573-584
41. Kemp JD (1997) Iron deprivation and cancer: a view beginning with studies of monoclonal antibodies against the transferrin receptor. Histol Histopathol 12:291-296
42. Kemp S, Wheate NJ, Buck DP, Nikac M, Collins JG, Aldrich- Wright JR (2007) The effect of ancillary ligand chirality and phenanthroline functional group substitution on the cytotoxicity of platinum(II)-based metallointercalators. J Inorg Biochem 101:1049-1058
43. Kemp S, Wheate NJ, Wang S, Collins J, Ralph S, Day A, Higgins VJ, Aldrich-Wright JR (2007) Encapsulation of platinum(II)-based DNA intercalators within cucurbit[6,7,8]urils. J Biol Inorg Chem 12:969-979
44. Kicic A, Chua ACG, Baker E (2001) Effect of iron chelators on proliferation and iron uptake in hepatoma cells. Cancer 92:3093- 3110
45. Krause-Heuer AM, Grünert R, Kühne S, Buczkowska M, Wheate NJ, Le Pevelen DD, Boag LR, Fisher DM, Kasparkova J, Malina J, Bednarski PJ, Brabec V, Aldrich-Wright JR (2009) Studies of the mechanism of action of platinum(II) complexes with potent cytotoxicity in human cancer cells. J Med Chem 52:5474-5484
46. Kuras L, Barbey R, Thomas D (1997) Assembly of a bZIP-bHLH transcription activation complex: formation of the yeast Cbf1- Met4-Met28 complex is regulated through Met28 stimulation of Cbf1 DNA binding. EMBO J 16:2441-2451
47. Le NT, Richardson DR (2002) The role of iron in cell cycle progression and the proliferation of neoplastic cells. Biochim Biophys Acta 1603:31-46
48. Lee J, Straffon MJ, Jang T, Higgins VJ, Grant CM, Dawes IW (2001) The essential 582 and ancillary role of glutathione in Saccharomyces cerevisiae analysed using a grande gsh1 disruptant strain. FEMS Yeast Res 1:57-65
49. Lesuisse E, Blaiseau PL, Dancis A, Camadro J (2001) Siderophore uptake and use by the yeast Saccharomyces cerevisiae. Microbiology 147:289-298
50. Lim AL, Powers-Lee SG (1996) Requirement for the carboxylterminal domain of Saccharomyces cerevisiae carbamoylphosphate synthetase. J Biol Chem 271:11400-11409
51. Mai B, Breeden L (1997) Xbp1, a stress-induced transcriptional repressor of the Saccharomyces cerevisiae Swi4/Mbp1 family. Mol Cell Biol 17:6491-6501
52. Margiotta N, Ostuni R, Gandin V, Marzano C, Piccinonna S, Natile G (2009) Synthesis, characterization, and cytotoxicity of dinuclear platinum- bisphosphonate complexes to be used as prodrugs in the local treatment of bone tumours. Dalton Trans 48:10904-10913
53. McFadyen WD, Wakelin LPG, Roos IAG, Leopold VA (1985) Activity of platinum(II) intercalating agents against murine leukemia L1210. J Med Chem 28:1113-1116
54. Meister A, Anderson ME (1983) Glutathione. Annu Rev Biochem 52:711-760
55. Moretto J, Chauffert B, Ghiringhelli F, Aldrich-Wright JR, Bouyer F (2010) Discrepancy between in vitro and in vivo antitumor effect of a new platinum(II) metallointercalator. Invest New Drugs 29:1164-1176
56. Odani T, Shimma Y, Wang XHYJ (1997) Mannosylphosphate transfer to cell wall mannan is regulated by the transcriptional level of the MNN4 gene in Saccharomyces cerevisiae. FEBS Lett 420:186-190
57. Protchenko O, Philpott C (2003) Regulation of intracellular heme levels by HMX1, a homologue of heme oxygenase, in Saccharomyces cerevisiae. J Biol Chem 278:36582-36587
58. Rabik CA, Dolan ME (2007) Molecular mechanisms of resistance and toxicity associated with platinating agents. Cancer Treat Rev 33:9-23
59. Reizenstein P (1991) Iron, free radicals and cancer: a review. Med Oncol Tumor Pharmacother 8:229-233
60. Richardson J, Thomas KA, Rubin BH, Richardson DC (1975) Crystal structure of bovine Cu, Zn superoxide dismutase at 3 A resolution: chain tracing and metal ligands. Proc Nat Acad Sci 72:1349-1353
61. Richon VM, Schulte N, Eastman A (1987) Multiple mechanisms of resistance to cis diamminedichloroplatinum(II) in murine leukemia L1210 Cells. Cancer Res 47:2056-2061
62. Robbins E, Pederson T (1970) Iron: its intracellular localization and possible role in cell division. Proc Natl Acad Sci USA 66:1244-1251
63. Rodriguez-Manzaneque MT, Ros J, Cabiscol E, Sorribas A, Herrero E (1999) Grx5 glutaredoxin plays a central role in protection against protein oxidative damage in Saccharomyces cerevisiae. Mol Cell Biol 19:8180-8190
64. Rutherford JC, Jaron S, Winge DR (2003) Aft1p and Aft2p mediate iron-responsive gene expression in yeast through related promoter elements. J Biol Chem 278:27636-27643
65. Seligman P, Schleicher R, Siriwardana G, Domenico J, Gelfand E (1993) Effects of agents that inhibit cellular iron incorporation on bladder cancer cell proliferation. Blood 82:1608-1617
66. Siddik Z (2003) Cisplatin: mode of cytotoxic action and molecular basis of 623 resistance. Oncogene 22:7265-7279
67. Sies H (1999) Glutathione and its role in cellular functions. Free Radic Biol Med 27:916-921
68. Simon J, Bedalov A (2004) Yeast as a model system for anticancer drug discovery. Nat Rev Cancer 4:1-8
69. Stearman R, Yuan DS, Yamaguchi-Iwai Y, Klausner RD, Dancis A (1996) A permease-oxidase complex involved in high-affinity iron uptake in yeast. Science 271:1552-1557
70. Teixeira M, Monteiro P, Jain P, Tenreiro S, Fernandes A, Mira N, Alenquer M, Freitas A, Oliveira A, Sa-Correia I (2006) The YEASTRACT database: a tool for the analysis of transcription regulatory associations in Saccharomyces cerevisiae. Nucleic Acids Res 34:D446-451
71. Thomas-Chollier M, Sand O, Turatsinze J, Janky R, Defrance M, Vervisch E, Brohe'e S, van Helden J (2008) RSAT: regulatory sequence analysis tools. Nucleic Acids Res 36:W119-W127
72. Toyokuni S (1996) Iron-induced carcinogenesis: the role of redox regulation. Free Radic Bio Med 20:553-566
73. van Helden J (2003) Regulatory sequence analysis tools. Nucleic Acids Res 31:3593-3596
74. Van Ho A, Ward DM, Kaplan J (2002) Transition metal transport in yeast. Annu Rev Microbiol 56:237-261
75. van Loon AP, Pesold-Hunt B, Schatz G (1986) A yeast mutant lacking mitochondrial manganese superoxide dismutase is hypersensitive to oxygen. Proc Natl Acad Sci USA 83:3820-3824
76. Wang D, Lippard SJ (2005) Cellular processing of platinum anticancer drugs. Nat Rev Drug Discov 4:308-320
77. Weinberg ED (1999) Iron therapy and cancer. Kidney Int 55:S131- S134
78. Wheate NJ, Collins JG (2005) Multi-nuclear platinum drugs: a new paradigm in chemotherapy. Curr Med Chem - Anti-Cancer Agents 5:267-279
79. Wheate NJ, Taleb RI, Krause-Heuer AM, Cook RL, Wang S, Higgins VJ, Aldrich-Wright JR (2007) Novel platinum(II)-based anticancer complexes and molecular hosts as their drug delivery vehicles. Dalton Trans 43:5055-5064
80. Yamaguchi-Iwai Y, Ueta R, Fukunaka A, Sasaki R (2002) Subcellular localization Aft1 transcription factor responds to iron status in Saccharomyces cerevisiae. J Biol Chem 277:18914-18918