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Unusual DNA binding modes for metal anticancer complexes

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Pizarro, Ana M. and Sadler, P. J.. (2009) Unusual DNA binding modes for metal anticancer complexes. Biochimie, Vol.91 (No.10). pp. 1198-1211. ISSN 0300-9084

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Official URL: http://dx.doi.org/10.1016/j.biochi.2009.03.017

Abstract

DNA is believed to be the primary target for many metal-based drugs. For example, platinum-based anticancer drugs can form specific lesions on DNA that induce apoptosis. New platinum drugs can be designed that have novel modes of interaction with DNA, such as the trinuclear platinum complex BBR3464. Also it is possible to design inert platinum(IV) pro-drugs which are non-toxic in the dark, but lethal when irradiated with certain wavelengths of light. This gives rise to novel DNA lesions which are not as readily repaired as those induced by cisplatin, and provides the basis for a new type of photoactivated chemotherapy. Finally, newly emerging ruthenium(II) organometallic complexes not only bind to DNA coordinatively, but also by H-bonding and hydrophobic interactions triggered by the introduction of extended arene rings into their versatile structures. Intriguingly osmium (the heavier congener of ruthenium) reacts differently with DNA but can also give rise to highly cytotoxic organometallic complexes.

Item Type:	Journal Article
Subjects:	R Medicine > RC Internal medicine > RC0254 Neoplasms. Tumors. Oncology (including Cancer)
Divisions:	Faculty of Science > Chemistry
Library of Congress Subject Headings (LCSH):	Bioinorganic chemistry, Cancer -- Treatment, Metals in medicine, Antineoplastic agents -- Development, Organometallic compounds, Cisplatin -- Research, DNA-binding proteins
Journal or Publication Title:	Biochimie
Publisher:	Elsevier Masson
ISSN:	0300-9084
Date:	October 2009
Volume:	Vol.91
Number:	No.10
Page Range:	pp. 1198-1211
Identification Number:	10.1016/j.biochi.2009.03.017
Status:	Peer Reviewed
Access rights to Published version:	Open Access
Funder:	Engineering and Physical Sciences Research Council (EPSRC), Medical Research Council (Great Britain) (MRC), European Commission (EC), Körber-Stiftung (KS)
References:	[1] S. Komeda, T. Moulaei, K.K. Woods, M. Chikuma, N.P. Farrell, L.D. Williams, A Third Mode of DNA Binding: Phosphate Clamps by a Polynuclear Platinum Complex, J. Am. Chem. Soc. 128 (2006) 16092-16103. [2] B. Lippert, Cisplatin: Chemistry and Biochemistry of a Leading Anticancer Drug, Verlag Helvetica Chimica Acta, Zurich, 1999, 563 p. [3] P.J. Bednarski, F.S. Mackay, P.J. Sadler, Photoactivatable platinum complexes, Anti-Cancer Agents Med. Chem. 7 (2007) 75-93. [4] L. Ronconi, P.J. Sadler, Unprecedented carbon-carbon bond formation induced by photoactivation of a platinum(iv)-diazido complex, Chem. Commun. (2008) 235-237. [5] I.A. Phillips Hazel, L. Ronconi, J. Sadler Peter, Photoinduced reactions of cis,trans,cis-[Pt(IV)(N3)2(OH)2(NH3)2) with 1-methylimidazole, Chemistry 15 (2009) 1588-1596. [6] I. Bratsos, S. Jedner, T. Gianferrara, E. Alessio, Ruthenium anticancer compounds: challenges and expectations, Chimia 61 (2007) 692-697. [7] C.G. Hartinger, M.A. Jakupec, S. Zorbas-Seifried, et al., KP1019, a new redoxactive anticancer agent - preclinical development and results of a clinical phase I study in tumor patients, Chem. Biodiversity 5 (2008) 2140-2155. [8] A.F.A. Peacock, P.J. Sadler, Medicinal organometallic chemistry: designing metal arene complexes as anticancer agents, Chem. Asian J. 3 (2008) 1890- 1899. [9] B. Rosenberg, L. Vancamp, T. Krigas, Inhibition of Cell Division in Escherichia Coli by Electrolysis Products from a Platinum Electrode, Nature 205 (1965) 698-699. [10] H.C. Harder, B. Rosenberg, Inhibitory effects of antitumor platinum compounds on DNA, RNA, and protein syntheses in mammalian cells in vitro, Int. J. Cancer 6 (1970) 207-216. [11] J.A. Howle, G.R. Gale, Cis-dichlorodiammineplatinum(II). Persistent and selective inhibition of deoxyribonucleic acid synthesis in vivo, Biochem. Pharmacol. 19 (1970) 2757-2762. [12] R.J. Knox, F. Friedlos, D.A. Lydall, J.J. Roberts, Mechanism of cytotoxicity of anticancer platinum drugs: evidence that cis-diamminedichloroplatinum(II) and cis-diammine(1,1-cyclobutanedicarboxylato)platinum(II) differ only in the kinetics of their interaction with DNA, Cancer Res. 46 (1986) 1972-1979. [13] J.M. Pascoe, J.J. Roberts, Interactions between mammalian cell DNA and inorganic platinum compounds. I. DNA interstrand crosslinking and cytotoxic properties of platinum(II) compounds, Biochem. Pharmacol. 23 (1974) 1345- 1357. [14] A. Eastman, Characterization of the adducts produced in DNA by cisdiamminedichloroplatinum( II) and cis-dichloro(ethylenediamine)platinum(II), Biochemistry 22 (1983) 3927-3933. [15] A. Eastman, Reevaluation of interaction of cisdichloro( ethylenediamine)platinum(II) with DNA, Biochemistry 25 (1986) 3912-3915. [16] A.L. Pinto, S.J. Lippard, Binding of the antitumor drug cisdiamminedichloroplatinum( II) (cisplatin) to DNA, Biochim. Biophys. Acta 780 (1985) 167-180. [17] A. Eastman, The mechanism of action of cisplatin: from adducts to apoptosis, in: B. Lippert (Ed.), Cisplatin, Verlag Helvetica Chimica Acta, Zurich, 1999, pp. 111-134. [18] U.-M. Ohndorf, S.J. Lippard, Structural aspects of Pt-DNA adduct recognition by proteins, DNA Damage Recognition (2006) 239-261. [19] E.R. Jamieson, S.J. Lippard, Structure, recognition, and processing of cisplatin- DNA adducts, Chem. Rev. 99 (1999) 2467-2498. [20] M. Jennerwein, P.A. Andrews, Effect of intracellular chloride on the cellular pharmacodynamics of cis-diamminedichloroplatinum(II), Drug Metab. Dispos. 23 (1995) 178-184. [21] C.J. Boreham, J.A. Broomhead, D.P. Fairlie, A platinum-195 and nitrogen-15 NMR study of the anticancer drug cis-diamminedichloroplatinum(II) and its hydrolysis and oligomerization products, Aust. J. Chem. 34 (1981) 659-664. [22] S.E. Miller, D.A. House, The hydrolysis products of cisdichlorodiammineplatinum( II). 2. The kinetics of formation and anation of the cis-diamminedi(aqua)platinum(II) cation, Inorg. Chim. Acta 166 (1989) 189- 197. [23] S.J. Berners-Price, T.A. Frenkiel, U. Frey, J.D. Ranford, P.J. Sadler, Hydrolysis products of cisplatin: pKa determinations via [1H, 15N] NMR spectroscopy, J. Chem. Soc., Chem. Commun. (1992) 789-791. [24] M.S. Davies, S.J. Berners-Price, T.W. Hambley, Rates of Platination of AG and GA Containing Double-Stranded Oligonucleotides: Insights into Why Cisplatin Binds to GG and AG but Not GA Sequences in DNA, J. Am. Chem. Soc. 120 (1998) 11380-11390. [25] F. Legendre, V. Bas, J. Kozelka, J.C. Chottard, A complete kinetic study of GG versus AG plantination suggests that the doubly aquated derivatives of cisplatin are the actual DNA binding species, Chem. Eur. J. 6 (2000) 2002-2010. [26] J. Vinje, E. Sletten, J. Kozelka, Influence of dT20 and [d(AT)10]2 on cisplatin hydrolysis studied by two-dimensional [1H,15N] HMQC NMR spectroscopy, Chem. Eur. J. 11 (2005) 3863-3871. [27] M.S. Davies, S.J. Berners-Price, T.W. Hambley, Slowing of Cisplatin Aquation in the Presence of DNA but Not in the Presence of Phosphate: Improved Understanding of Sequence Selectivity and the Roles of Monoaquated and Diaquated Species in the Binding of Cisplatin to DNA, Inorg. Chem. 39 (2000) 5603-5613. [28] J. Kozelka, F. Legendre, F. Reeder, J.-C. Chottard, Kinetic aspects of interactions between DNA and platinum complexes, Coord. Chem. Rev. 190- 192 (1999) 61-81. [29] R.B. Martin, Platinum complexes: hydrolysis and binding to N(7) and N(1) of purines, in: B. Lippert (Ed.), Cisplatin, Verlag Helvetica Chimica Acta, Zurich, 1999, pp. 183-205. [30] S.J. Berners-Price, T.G. Appleton, , The chemistry of cisplatin in aqueous solution, in: L.R. Kelland, N.P. Farrell (Eds.), Platinum-Based Drugs in Cancer Therapy, Humana Press Inc., Totowa, 2000, pp. 3-35. [31] T.W. Hambley, Platinum binding to DNA: structural controls and consequences, J. Chem. Soc., Dalton Trans. (2001) 2711-2718. [32] J. Reedijk, Why does cisplatin reach guanine-N7 with competing S-donor ligands available in the cell?, Chem. Rev. 99 (1999) 2499-2510. [33] J.P. Caradonna, S.J. Lippard, M.J. Gait, M. Singh, The antitumor drug cisdichlorodiammineplatinum forms an intrastrand d(GpG) crosslink upon reaction with [d(ApGpGpCpCpT)]2, J. Am. Chem. Soc. 104 (1982) 5793-5795. [34] J. Filipski, K.W. Kohn, W.M. Bonner, The nature of inactivating lesions produced by platinum(II) complexes in phage l DNA, Chem. Biol. Interact. 32 (1980) 321-330. [35] A.M.J. Fichtinger-Schepman, J.L. Van der Veer, J.H.J. Den Hartog, P.H.M. Lohman, J. Reedijk, Adducts of the antitumor drug cisdiamminedichloroplatinum( II) with DNA: formation, identification, and quantitation, Biochemistry 24 (1985) 707-713. [36] A.M. Fichtinger-Schepman, A.T. van Oosterom, P.H. Lohman, F. Berends, cis- Diamminedichloroplatinum(II)-induced DNA adducts in peripheral leukocytes from seven cancer patients: quantitative immunochemical detection of the adduct induction and removal after a single dose of cisdiamminedichloroplatinum( II), Cancer Res. 47 (1987) 3000-3004. [37] T.W. Hambley, Modelling the interaction of cisplatin with DNA, Drug Design and Delivery 3 (1988) 153-158. [38] A.F. Struik, C.T.M. Zuiderwijk, J.H. Van Boom, L.I. Elding, J. Reedijk, Guanine-O6 methylation reduces the reactivity of d(GpG) towards platinum complexes, J. Inorg. Biochem. 44 (1991) 249-260. [39] M.-H. Baik, R.A. Friesner, S.J. Lippard, Theoretical Study of Cisplatin Binding to Purine Bases: Why Does Cisplatin Prefer Guanine over Adenine?, J. Am. Chem. Soc. 125 (2003) 14082-14092. [40] S.T. Sullivan, A. Ciccarese, F.P. Fanizzi, L.G. Marzilli, A rare example of three abundant conformers in one retro model of the cisplatin-DNA d(GpG) intrastrand cross link. Unambiguous evidence that guanine O6 to carrier amine ligand hydrogen bonding is not important. Possible effect of the Lippard base pair step adjacent to the lesion on carrier ligand hydrogen bonding in DNA adducts, J. Am. Chem. Soc. 123 (2001) 9345-9355. [41] S.E. Sherman, D. Gibson, A.H.J. Wang, S.J. Lippard, X-ray structure of the major adduct of the anticancer drug cisplatin with DNA: cis- [Pt(NH3)2{d(pGpG)}], Science 230 (1985) 412-417. [42] P.M. Takahara, A.C. Rosenzweig, C.A. Frederick, S.J. Lippard, Crystal structure of double-stranded DNA containing the major adduct of the anticancer drug cisplatin, Nature 377 (1995) 649-652. [43] A. Gelasco, S.J. Lippard, NMR Solution Structure of a DNA Dodecamer Duplex Containing a cis-Diammineplatinum(II) D(GpG) Intrastrand Cross-Link, the Major Adduct of the Anticancer Drug Cisplatin, Biochemistry 37 (1998) 9230- 9239. [44] S.J. Brown, P.J. Kellett, S.J. Lippard, Ixr1, a yeast protein that binds to platinated DNA and confers sensitivity to cisplatin, Science 261 (1993) 603-605. [45] J.-C. Huang, D.B. Zamble, J.T. Reardon, S.J. Lippard, A. Sancar, HMG-domain proteins specifically inhibit the repair of the major DNA adduct of the anticancer drug cisplatin by human excision nuclease, Proc. Natl. Acad. Sci. USA 91 (1994) 10394-10398. [46] U.-M. Ohndorf, M.A. Rould, Q. He, C.O. Pabo, S.J. Lippard, Basis for recognition of cisplatin-modified DNA by high-mobility-group proteins, Nature 399 (1999) 708-712. [47] M. Kartalou, J.M. Essigmann, Recognition of cisplatin adducts by cellular proteins, Mutat. Res. Fund. Mol. Mech. Mut. 478 (2001) 1-21. [48] Y. Jung, S.J. Lippard, Direct Cellular Responses to Platinum-Induced DNA Damage, Chem. Rev. 107 (2007) 1387-1407. [49] E.R. Guggenheim, D. Xu, C.X. Zhang, P.V. Chang, S.J. Lippard, Photoaffinity isolation and identification of proteins in cancer cell extracts that bind to platinum-modified DNA, ChemBioChem 10 (2009) 141-157. [50] S.M. Cohen, E.R. Jamieson, S.J. Lippard, Enhanced binding of the TATAbinding protein to TATA boxes containing flanking cisplatin 1,2-cross-links, Biochemistry 39 (2000) 8259-8265. [51] P. Vichi, F. Coin, J.-P. Renaud, W. Vermeulen, J.H.J. Hoeijmakers, D. Moras, J.-M. Egly, Cisplatin- and UV-damaged DNA lure the basal transcription factor TFIID/TBP, Embo J. 16 (1997) 7444-7456. [52] Y. Jung, Y. Mikata, S.J. Lippard, Kinetic studies of the TATA-binding protein interaction with cisplatin-modified DNA, J. Biol. Chem. 276 (2001) 43589- 43596. [53] J. Naniwa, J. Kigawa, R. Akeshima, et al., Leptomycin B enhances CDDPsensitivity via nuclear accumulation of p53 protein in HPV-positive cells, Cancer Sci. 94 (2003) 1099-1103. [54] T. Imamura, H. Izumi, G. Nagatani, et al., Interaction with p53 enhances binding of cisplatin-modified DNA by high mobility group 1 protein, J. Biol. Chem. 276 (2001) 7534-7540. [55] W.I. Sundquist, S.J. Lippard, B.D. Stollar, Monoclonal antibodies to DNA modified with cis- or trans-diamminedichloroplatinum(II), Proc. Natl. Acad. Sci. USA 84 (1987) 8225-8229. [56] F.A. Blommaert, H.C.M. van Dijk-Knijnenburg, F.J. Dijt, L. den Engelse, R.A. Baan, F. Berends, A.M.J. Fichtinger-Schepman, Formation of DNA Adducts by the Anticancer Drug Carboplatin: Different Nucleotide Sequence Preferences in Vitro and in Cells, Biochemistry 34 (1995) 8474-8480. [57] C. Kloft, C. Eickhoff, K. Schulze-Forster, H.R. Maurer, W. Schunack, U. Jaehde, Development and application of a simple assay to quantify cellular adducts of platinum complexes with DNA, Pharm. Res. 16 (1999) 470-473. [58] C.P. Saris, P.J.M. van de Vaart, R.C. Rietbroek, F.A. Blommaert, In vitro formation of DNA adducts by cisplatin, lobaplatin and oxaliplatin in calf thymus DNA in solution and in cultured human cells, Carcinogenesis 17 (1996) 2763- 2769. [59] Y. Kidani, M. Noji, T. Tashiro, Antitumor activity of platinum(II) complexes of l,2-diammino-cyclohexane isomers, Jpn. J. Cancer Res. 71 (1980) 637-643. [60] O. Rixe, W. Ortuzar, M. Alvarez, et al., Oxaliplatin, tetraplatin, cisplatin, and carboplatin: spectrum of activity in drug-resistant cell lines and in the cell lines of the National Cancer Institute's Anticancer Drug Screen Panel, Biochem. Pharmacol. 52 (1996) 1855-1865. [61] R.B. Weiss, M.C. Christian, New cisplatin analogs in development: a review, Drugs 46 (1993) 360-377. [62] E. Raymond, S.G. Chaney, A. Taamma, E. Cvitkovic, Oxaliplatin: a review of preclinical and clinical studies, Ann. Oncol. 9 (1998) 1053-1071. [63] S.G. Chaney, A. Vaisman, Specificity of platinum-DNA adduct repair, J. Inorg. Biochem. 77 (1999) 71-81. [64] B. Spingler, D.A. Whittington, S.J. Lippard, 2.4 .ANG. Crystal Structure of an Oxaliplatin 1,2-d(GpG) Intrastrand Cross-Link in a DNA Dodecamer Duplex, Inorg. Chem. 40 (2001) 5596-5602. [65] S.G. Chaney, S.L. Campbell, E. Bassett, Y. Wu, Recognition and processing of cisplatin- and oxaliplatin-DNA adducts, Crit. Rev. Oncol. Hematol. 53 (2005) 3- 11. [66] Y. Wu, P. Pradhan, J. Havener, et al., NMR Solution Structure of an Oxaliplatin 1,2-d(GG) Intrastrand Cross-link in a DNA Dodecamer Duplex, J. Mol. Biol. 341 (2004) 1251-1269. [67] Y. Wu, D. Bhattacharyya, C.L. King, et al., Solution Structures of a DNA Dodecamer Duplex with and without a Cisplatin 1,2-d(GG) Intrastrand Cross- Link: Comparison with the Same DNA Duplex Containing an Oxaliplatin 1,2- d(GG) Intrastrand Cross-Link, Biochemistry 46 (2007) 6477-6487. [68] N. Farrell, T.T.B. Ha, J.P. Souchard, F.L. Wimmer, S. Cros, N.P. Johnson, Cytostatic trans-platinum(II) complexes, J. Med. Chem. 32 (1989) 2240-2241. [69] A. Zakovska, O. Novakova, Z. Balcarova, U. Bierbach, N. Farrell, V. Brabec, DNA interactions of antitumor trans-[PtCl2(NH3)(quinoline)], Eur. J. Biochem. 254 (1998) 547-557. [70] M. Coluccia, A. Boccarelli, M.A. Mariggio, et al., Platinum(II) complexes containing iminoethers: a trans platinum antitumor agent, Chem. Biol. Interact. 98 (1995) 251-266. [71] O. Novakova, J. Kasparkova, J. Malina, G. Natile, V. Brabec, DNA-protein cross-linking by trans-[PtCl2(E-iminoether)2]. A concept for activation of the trans geometry in platinum antitumor complexes, Nucleic Acids Res. 31 (2003) 6450-6460. [72] J.M. Perez, M.A. Fuertes, C. Alonso, C. Navarro-Ranninger, Current status of the development of trans-platinum antitumor drugs, Crit. Rev. Oncol. Hematol. 35 (2000) 109-120. [73] J. Kasparkova, O. Novakova, V. Marini, et al., Activation of Trans Geometry in Bifunctional Mononuclear Platinum Complexes by a Piperidine Ligand: Mechanistic Studies on Antitumor Action, J. Biol. Chem. 278 (2003) 47516- 47525. [74] N.P. Farrell, S.G. De Almeida, K.A. Skov, Bis(platinum) complexes containing two platinum cis-diammine units. Synthesis and initial DNA-binding studies, J. Am. Chem. Soc. 110 (1988) 5018-5019. [75] C. Sessa, G. Capri, L. Gianni, et al., Clinical and pharmacological phase I study with accelerated titration design of a daily times five schedule of BBR3464, a novel cationic triplatinum complex, Ann. Oncol. 11 (2000) 977-983. [76] V. Brabec, J. Kasparkova, O. Vrana, et al., DNA modifications by a novel bifunctional trinuclear platinum phase I anticancer agent, Biochemistry 38 (1999) 6781-6790. [77] P. Perego, C. Caserini, L. Gatti, et al., A novel trinuclear platinum complex overcomes cisplatin resistance in an osteosarcoma cell system, Mol. Pharmacol. 55 (1999) 528-534. [78] G. Pratesi, P. Perego, D. Polizzi, et al., A novel charged trinuclear platinum complex effective against cisplatin-resistant tumours: hypersensitivity of p53- mutant human tumour xenografts, Br. J. Cancer 80 (1999) 1912-1919. [79] C. Manzotti, G. Pratesi, E. Menta, et al., BBR 3464: a novel triplatinum complex, exhibiting a preclinical profile of antitumor efficacy different from cisplatin, Clin. Cancer Res. 6 (2000) 2626-2634. [80] J.D. Roberts, J. Peroutka, N. Farrell, Cellular pharmacology of polynuclear platinum anti-cancer agents, J. Inorg. Biochem. 77 (1999) 51-57. [81] M.S. Davies, D.S. Thomas, A. Hegmans, S.J. Berners-Price, N. Farrell, Kinetic and Equilibria Studies of the Aquation of the Trinuclear Platinum Phase II Anticancer Agent [{trans-PtCl(NH3)2}2{m-trans- Pt(NH3)2(NH2(CH2)6NH2)2}]4+ (BBR3464), Inorg. Chem. 41 (2002) 1101- 1109. [82] A. Hegmans, S.J. Berners-Price, M.S. Davies, D.S. Thomas, A.S. Humphreys, N. Farrell, Long Range 1,4 and 1,6-Interstrand Cross-Links Formed by a Trinuclear Platinum Complex. Minor Groove Preassociation Affects Kinetics and Mechanism of Cross-Link Formation as Well as Adduct Structure, J. Am. Chem. Soc. 126 (2004) 2166-2180. [83] H. Chen, J.A. Parkinson, R.E. Morris, P.J. Sadler, Highly Selective Binding of Organometallic Ruthenium Ethylenediamine Complexes to Nucleic Acids: Novel Recognition Mechanisms, J. Am. Chem. Soc. 125 (2003) 173-186. [84] N.J. Wheate, J.G. Collins, Multi-nuclear platinum complexes as anti-cancer drugs, Coord. Chem. Rev. 241 (2003) 133-145. [85] N.J. Wheate, J.G. Collins, Multi-nuclear platinum drugs: A new paradigm in chemotherapy, Curr. Med. Chem. Anti Canc. Agents 5 (2005) 267-279. [86] P.D. Braddock, T.A. Connors, M. Jones, A.R. Khokhar, D.H. Melzack, M.L. Tobe, Structure and activity relations of platinum complexes with antitumor activity, Chem. Biol. Interact. 11 (1975) 145-161. [87] V.H. Bramwell, D. Crowther, S. O'Malley, et al., Activity of JM9 in advanced ovarian cancer: a phase I-II trial, Cancer Treat. Rep. 69 (1985) 409-416. [88] P.J. Creaven, L. Pendyala, S. Madajewicz, Clinical development of iproplatin (CHIP), Drugs Exp. Clin. Res. 12 (1986) 287-292. [89] H. Anderson, J. Wagstaff, D. Crowther, et al., Comparative toxicity of cisplatin, carboplatin (CBDCA) and iproplatin (CHIP) in combination with cyclophosphamide in patients with advanced epithelial ovarian cancer, Eur. J. Cancer Clin. Oncol. 24 (1988) 1471-1479. [90] P.D. Bonomi, D.M. Finkelstein, J.C. Ruckdeschel, et al., Combination chemotherapy versus single agents followed by combination chemotherapy in stage IV non-small-cell lung cancer: a study of the Eastern Cooperative Oncology Group, J. Clin. Oncol. 7 (1989) 1602-1613. [91] R.J. Schilder, F.P. LaCreta, R.P. Perez, et al., Phase I and pharmacokinetic study of ormaplatin (tetraplatin, NSC 363812) administered on a day 1 and day 8 schedule, Cancer Res. 54 (1994) 709-717. [92] N. Farrell, L.R. Kelland, J.D. Roberts, M. Van Beusichem, Activation of the trans geometry in platinum antitumor complexes: a survey of the cytotoxicity of trans complexes containing planar ligands in murine L1210 and human tumor panels and studies on their mechanism of action, Cancer Res. 52 (1992) 5065- 5072. [93] H. Choy, Satraplatin: an orally available platinum analog for the treatment of cancer, Expert Rev. Anticancer Ther. 6 (2006) 973-982. [94] C.N. Sternberg, P. Whelan, J. Hetherington, et al., Phase III Trial of Satraplatin, an Oral Platinum plus Prednisone vs. Prednisone alone in Patients with Hormone-Refractory Prostate Cancer, Oncology 68 (2005) 2-9. [95] J. Turanek, A. Kasna, D. Zaluska, et al., New platinum(IV) complex with adamantylamine ligand as a promising anti-cancer drug: comparison of in vitro cytotoxic potential towards A2780/cisR cisplatin-resistant cell line within homologous series of platinum(IV) complexes, Anti-Cancer Drugs 15 (2004) 537-543. [96] F. Zak, J. Turanek, A. Kroutil, et al., Platinum(IV) Complex with Adamantylamine as Nonleaving Amine Group: Synthesis, Characterization, and in Vitro Antitumor Activity against a Panel of Cisplatin-Resistant Cancer Cell Lines, J. Med. Chem. 47 (2004) 761-763. [97] A. Kozubik, V. Horvath, L. Svihalkova-Sindlerova, et al., High effectiveness of platinum(IV) complex with adamantylamine in overcoming resistance to cisplatin and suppressing proliferation of ovarian cancer cells in vitro, Biochem. Pharmacol. 69 (2005) 373-383. [98] P. Sova, J. Chladek, F. Zak, et al., Pharmacokinetics and tissue distribution of platinum in rats following single and multiple oral doses of LA-12 [(OC-6-43)- bis(acetato)(1-adamantylamine)amminedichloroplatinum(IV)], Int. J. Pharm. 288 (2005) 123-129. [99] P. Sova, A. Mistr, A. Kroutil, F. Zak, P. Pouckova, M. Zadinova, Preclinical anti-tumor activity of a new oral platinum(IV) drug LA-12, Anti-Cancer Drugs 16 (2005) 653-657. [100] P. Sova, A. Mistr, A. Kroutil, F. Zak, P. Pouckova, M. Zadinova, Comparative anti-tumor efficacy of two orally administered platinum(IV) drugs in nude mice bearing human tumor xenografts, Anti-Cancer Drugs 17 (2006) 201-206. [101] S. Choi, R.B. Cooley, A.S. Hakemian, et al., Mechanism of two-electron oxidation of deoxyguanosine 5'-monophosphate by a platinum(IV) complex, J. Am. Chem. Soc. 126 (2004) 591-598. [102] S. Choi, S. Mahalingaiah, S. Delaney, N.R. Neale, S. Masood, Substitution and Reduction of Platinum(IV) Complexes by a Nucleotide, Guanosine 5'- Monophosphate, Inorg. Chem. 38 (1999) 1800-1805. [103] S. Choi, L. Orbai, E.J. Padgett, S. Delaney, A.S. Hakemian, A Platinum(IV) Complex Oxidizes Guanine to 8-Oxo-Guanine in DNA and RNA, Inorg. Chem. 40 (2001) 5481-5482. [104] S. Choi, R.B. Cooley, A. Voutchkova, C.H. Leung, L. Vastag, D.E. Knowles, Oxidation of Guanosine Derivatives by a Platinum(IV) Complex: Internal Electron Transfer through Cyclization, J. Am. Chem. Soc. 127 (2005) 1773- 1781. [105] S. Choi, L. Vastag, C.-H. Leung, A.M. Beard, D.E. Knowles, J.A. Larrabee, Kinetics and Mechanism of the Oxidation of Guanosine Derivatives by Pt(IV) Complexes, Inorg. Chem. 45 (2006) 10108-10114. [106] J.L. Van der Veer, G.J. Ligtvoet, J. Reedijk, Reactions of platinum(IV) amine compounds with 9-methylhypoxanthine at high temperature result in both platinum(II) and platinum(IV) amine adducts, J. Inorg. Biochem. 29 (1987) 217- 223. [107] R.M. Roat, J. Reedijk, Reaction of mertrichloro( diethylenetriamine)platinum(IV) chloride, (mer-[Pt(dien)Cl3]Cl), with purine nucleosides and nucleotides results in formation of platinum(II) as well as platinum(IV) complexes, J. Inorg. Biochem. 52 (1993) 263-274. [108] S.G. Chaney, G.R. Gibbons, S.D. Wyrick, P. Podhasky, An unexpected biotransformation pathway for tetrachloro-(d,l-trans)-1,2- diaminocyclohexaneplatinum(IV)(tetraplatin) in the L1210 cell line, Cancer Res. 51 (1991) 969-973. [109] V. Brabec, O. Vrana, V. Kleinwachter, Tetravalent platinum complexes can exert their antitumor effect via direct reaction with DNA, Stud. Biophys. 114 (1986) 199-207. [110] O. Novakova, J. Kasparkova, O. Vrana, P.M. van Vliet, J. Reedijk, V. Brabec, Correlation between Cytotoxicity and DNA Binding of Polypyridyl Ruthenium Complexes, Biochemistry 34 (1995) 12369-12378. [111] M. Defais, M. Germanier, N.P. Johnson, Detection of DNA strand breaks in Escherichia coli treated with platinum(IV) antitumor compounds, Chem. Biol. Interact. 74 (1990) 343-352. [112] M.D. Hall, T.W. Hambley, Platinum(IV) antitumour compounds: their bioinorganic chemistry, Coord. Chem. Rev. 232 (2002) 49-67. [113] E. Rotondo, V. Fimiani, A. Cavallaro, T. Ainis, Does the antitumoral activity of platinum(IV) derivatives result from their in vivo reduction?, Tumori 69 (1983) 31-36. [114] E.E. Blatter, J.F. Vollano, B.S. Krishnan, J.C. Dabrowiak, Interaction of the antitumor agents cis,cis,trans-Pt(IV)(NH3)2Cl2(OH)2 and cis,cis,trans- Pt(IV)[(CH3)2CHNH2]2Cl2(OH)2 and their reduction products with PM2 DNA, Biochemistry 23 (1984) 4817-4820. [115] J.L. Van der Veer, A.R. Peters, J. Reedijk, Reaction products from platinum(IV) amine compounds and 5'-GMP are mainly bis(5'-GMP)platinum(II) amine adducts, J. Inorg. Biochem. 26 (1986) 137-142. [116] A. Eastman, Glutathione-mediated activation of anticancer platinum(IV) complexes, Biochem. Pharmacol. 36 (1987) 4177-4178. [117] L. Pendyala, J.W. Cowens, G.B. Chheda, S.P. Dutta, P.J. Creaven, Identification of cis-dichloro-bis-isopropylamine platinum(II) as a major metabolite of iproplatin in humans, Cancer Res. 48 (1988) 3533-3536. [118] S.G. Chaney, S. Wyrick, G.K. Till, In vitro biotransformations of tetrachloro(d,ltrans)- 1,2-diaminocyclohexaneplatinum(IV) (tetraplatin) in rat plasma, Cancer Res. 50 (1990) 4539-4545. [119] N.A. Kratochwil, P.J. Bednarski, H. Mrozek, A. Vogler, J.K. Nagle, Photolysis of an iodoplatinum(IV) diamine complex to cytotoxic species by visible light, Anti-Cancer Drug Des. 11 (1996) 155-171. [120] N.A. Kratochwil, P.J. Bednarski, Relationships between reduction properties and cancer cell growth inhibitory activities of cis-dichloro- and cis-diiodo- Pt(IV)-ethylenediamines, Archiv der Pharmazie 332 (1999) 279-285. [121] P. Müller, PhD Thesis, University of Edinburgh (2002). [122] J. Kasparkova, F.S. Mackay, V. Brabec, P.J. Sadler, Formation of platinated GG cross-links on DNA by photoactivation of a platinum(IV) azide complex, J. Biol. Inorg. Chem. 8 (2003) 741-745. [123] P. Heringova, J. Woods, F.S. Mackay, J. Kasparkova, P.J. Sadler, V. Brabec, Transplatin Is Cytotoxic When Photoactivated: Enhanced Formation of DNA Cross-Links, J. Med. Chem. 49 (2006) 7792-7798. [124] F.S. Mackay, J.A. Woods, P. Heringova, et al., A potent cytotoxic photoactivated platinum complex, Proc. Natl. Acad. Sci. USA 104 (2007) 20743-20748. [125] A.D. Kelman, M.J. Clarke, S.D. Edmonds, H.J. Peresie, Biological activity of ruthenium purine complexes, J. Clin. Hematol. Oncol. 7 (1977) 274-288. [126] M.J. Clarke, Oncological implication of the chemistry of ruthenium, Met. Ions Biol. Syst. 11 (1980) 231-283. [127] G. Mestroni, E. Alessio, M. Calligaris, et al., Chemical, biological and antitumor properties of ruthenium(II) complexes with dimethyl sulfoxide, Prog. Clin. Biochem. Med. 10 (1989) 71-87. [128] G. Sava, A. Bergamo, S. Zorzet, et al., Influence of chemical stability on the activity of the antimetastasis ruthenium compound NAMI-A, Eur. J. Cancer 38 (2002) 427-435. [129] A. Bergamo, R. Gagliardi, V. Scarcia, et al., In vitro cell cycle arrest, in vivo action on solid metastasizing tumors, and host toxicity of the antimetastatic drug NAMI-A and cisplatin, J. Pharmacol. Exp. Ther. 289 (1999) 559-564. [130] G. Sava, I. Capozzi, K. Clerici, G. Gagliardi, E. Alessio, G. Mestroni, Pharmacological control of lung metastases of solid tumors by a novel ruthenium complex, Clin. Exp. Metastasis 16 (1998) 371-379. [131] L. Morbidelli, S. Donnini, S. Filippi, et al., Antiangiogenic properties of selected ruthenium(III) complexes that are nitric oxide scavengers, Br. J. Cancer 88 (2003) 1484-1491. [132] J.M. Rademaker-Lakhai, D. Van Den Bongard, D. Pluim, J.H. Beijnen, J.H.M. Schellens, A Phase I and Pharmacological Study with Imidazolium-trans- DMSO-imidazole-tetrachlororuthenate, a Novel Ruthenium Anticancer Agent, Clin. Cancer Res. 10 (2004) 3717-3727. [133] A. Vacca, M. Bruno, A. Boccarelli, et al., Inhibition of endothelial cell functions and of angiogenesis by the metastasis inhibitor NAMI-A, Br. J. Cancer 86 (2002) 993-998. [134] W.H. Ang, E. Daldini, C. Scolaro, R. Scopelliti, L. Juillerat-Jeannerat, P.J. Dyson, Development of Organometallic Ruthenium-Arene Anticancer Drugs That Resist Hydrolysis, Inorg. Chem. 45 (2006) 9006-9013. [135] E. Alessio, G. Mestroni, A. Bergamo, G. Sava, Ruthenium antimetastatic agents, Curr. Top. Med. Chem. 4 (2004) 1525-1535. [136] F.T. Garzon, M.R. Berger, B.K. Keppler, D. Schmaehl, Comparative antitumor activity of ruthenium derivatives with 5'-deoxy-5-fluorouridine in chemically induced colorectal tumors in SD rats, Cancer Chemoth. Pharmacol. 19 (1987) 347-349. [137] M.R. Berger, F.T. Garzon, B.K. Keppler, D. Schmaehl, Efficacy of new ruthenium complexes against chemically induced autochthonous colorectal carcinoma in rats, Anticancer Res. 9 (1989) 761-765. [138] M.H. Seelig, M.R. Berger, B.K. Keppler, Antineoplastic activity of three ruthenium derivatives against chemically induced colorectal carcinoma in rats, J. Cancer Res. Clin. Oncol. 118 (1992) 195-200. [139] M. Galanski, V.B. Arion, M.A. Jakupec, B.K. Keppler, Recent developments in the field of tumor-inhibiting metal complexes, Current Pharmaceutical Design 9 (2003) 2078-2089. [140] C.G. Hartinger, S. Zorbas-Seifried, M.A. Jakupec, B. Kynast, H. Zorbas, B.K. Keppler, From bench to bedside - preclinical and early clinical development of the anticancer agent indazolium trans-[tetrachlorobis(1H-indazole)ruthenate(III)] (KP1019 or FFC14A), J. Inorg. Biochem. 100 (2006) 891-904. [141] J. Reedijk, Metal-ligand exchange kinetics in platinum and ruthenium complexes. Significance for effectiveness as anticancer drugs, Platinum Met. Rev. 52 (2008) 2-11. [142] M.J. Clarke, F. Zhu, D.R. Frasca, Non-Platinum Chemotherapeutic Metallopharmaceuticals, Chem. Rev. 99 (1999) 2511-2533. [143] V.B. Arion, E. Reisner, M. Fremuth, et al., Synthesis, X-ray Diffraction Structures, Spectroscopic Properties, and in vitro Antitumor Activity of Isomeric (1H-1,2,4-Triazole)Ru(III) Complexes, Inorg. Chem. 42 (2003) 6024-6031. [144] A. Egger, V.B. Arion, E. Reisner, et al., Reactions of Potent Antitumor Complex trans-[RuIIICl4(indazole)2]- with a DNA-Relevant Nucleobase and Thioethers: Insight into Biological Action, Inorg. Chem. 44 (2005) 122-132. [145] M.A. Jakupec, E. Reisner, A. Eichinger, et al., Redox-Active Antineoplastic Ruthenium Complexes with Indazole: Correlation of in Vitro Potency and Reduction Potential, J. Med. Chem. 48 (2005) 2831-2837. [146] E. Reisner, V.B. Arion, M.F.C. Guedes da Silva, et al., Tuning of Redox Potentials for the Design of Ruthenium Anticancer Drugs - an Electrochemical Study of [trans-RuCl4L(DMSO)]- and [trans-RuCl4L2]- Complexes, where L = Imidazole, 1,2,4-Triazole, Indazole, Inorg. Chem. 43 (2004) 7083-7093. [147] O.M. Ni Dhubhghaill, W.R. Hagen, B.K. Keppler, K.-G. Lipponer, P.J. Sadler, Aquation of the anticancer complex trans-[RuCl4(Him)2]- (Him = imidazole), J. Chem. Soc., Dalton Trans. (1994) 3305-3310. [148] B. Cebrian-Losantos, E. Reisner, C.R. Kowol, et al., Synthesis and Reactivity of the Aquation Product of the Antitumor Complex trans-[RuIIICl4(indazole)2], Inorg. Chem. 47 (2008) 6513-6523. [149] S. Kapitza, M. Pongratz, M.A. Jakupec, et al., Heterocyclic complexes of ruthenium(III) induce apoptosis in colorectal carcinoma cells, J. Cancer Res. Clin. Oncol. 131 (2005) 101-110. [150] S. Kapitza, M.A. Jakupec, M. Uhl, B.K. Keppler, B. Marian, The heterocyclic ruthenium(III) complex KP1019 (FFC14A) causes DNA damage and oxidative stress in colorectal tumor cells, Cancer Lett. 226 (2005) 115-121. [151] R.E. Morris, R.E. Aird, P.d.S. Murdoch, et al., Inhibition of Cancer Cell Growth by Ruthenium(II) Arene Complexes, J. Med. Chem. 44 (2001) 3616-3621. [152] R.E. Aird, J. Cummings, A.A. Ritchie, et al., In vitro and in vivo activity and cross resistance profiles of novel ruthenium (II) organometallic arene complexes in human ovarian cancer, Br. J. Cancer 86 (2002) 1652-1657. [153] S.J. Dougan, M. Melchart, A. Habtemariam, S. Parsons, P.J. Sadler, Phenylazopyridine and Phenylazo-pyrazole Chlorido Ruthenium(II) Arene Complexes: Arene Loss, Aquation, and Cancer Cell Cytotoxicity, Inorg. Chem. 45 (2006) 10882-10894. [154] F. Wang, J. Bella, J. A. Parkinson, J. P.J. Sadler, Competitive reactions of a ruthenium arene anticancer complex with histidine, cytochrome c and an oligonucleotide, J. Biol. Inorg. Chem. 10 (2005) 147-155. [155] M. Melchart, A. Habtemariam, S. Parsons, P.J. Sadler, Chlorido-, aqua-, 9- ethylguanine- and 9-ethyladenine-adducts of cytotoxic ruthenium arene complexes containing O,O-chelating ligands, J. Inorg. Biochem. 101 (2007) 1903-1912. [156] F. Wang, H. Chen, J.A. Parkinson, P.d.S. Murdoch, P.J. Sadler, Reactions of a Ruthenium(II) Arene Antitumor Complex with Cysteine and Methionine, Inorg. Chem. 41 (2002) 4509-4523. [157] H. Chen, J.A. Parkinson, O. Novakova, et al., Induced-fit recognition of DNA by organometallic complexes with dynamic stereogenic centers, Proc. Natl. Acad. Sci. USA 100 (2003) 14623-14628. [158] R. Fernandez, M. Melchart, A. Habtemariam, S. Parsons, P.J. Sadler, Use of chelating ligands to tune the reactive site of half-sandwich ruthenium(II)-arene anticancer complexes, Chem. Eur. J. 10 (2004) 5173-5179. [159] V. Marini, P. Christofis, O. Novakova, J. Kasparkova, N. Farrell, V. Brabec, Conformation, protein recognition and repair of DNA interstrand and intrastrand cross-links of antitumor trans-[PtCl2(NH3)(thiazole)], Nucleic Acids Res. 33 (2005) 5819-5828. [160] S.J. Berners-Price, P.J. Sadler, Coordination chemistry of metallodrugs: insights into biological speciation from NMR spectroscopy, Coord. Chem. Rev. 151 (1996) 1-40. [161] H.-K. Liu, S.J. Berners-Price, F. Wang, et al., Diversity in guanine-selective DNA binding modes for an organometallic ruthenium arene complex, Angew. Chem. Int. Ed. 45 (2006) 8153-8156. [162] L.H.-K. Liu, F. Wang, J.A. Parkinson, J. Bella, P.J. Sadler, Ruthenation of duplex and single-stranded d(CGGCCG) by organometallic anticancer complexes, Chem. Eur. J. 12 (2006) 6151-6165. [163] O. Novakova, H. Chen, O. Vrana, A. Rodger, P.J. Sadler, V. Brabec, DNA Interactions of Monofunctional Organometallic Ruthenium(II) Antitumor Complexes in Cell-free Media, Biochemistry 42 (2003) 11544-11554. [164] A. Gelasco, S.J. Lippard, Anticancer activity of cisplatin and related complexes, 1 (1999) 1-43. [165] T. Bugarcic, O. Novakova, A. Halamikova, et al., Cytotoxicity, Cellular Uptake, and DNA Interactions of New Monodentate Ruthenium(II) Complexes Containing Terphenyl Arenes, J. Med. Chem. 51 (2008) 5310-5319. [166] M. Melchart, A. Habtemariam, O. Novakova, et al., Bifunctional Amine- Tethered Ruthenium(II) Arene Complexes Form Monofunctional Adducts on DNA, Inorg. Chem. 46 (2007) 8950-8962. [167] J. Kasparkova, J. Zehnulova, N. Farrell, V. Brabec, DNA Interstrand Cross-links of the Novel Antitumor Trinuclear Platinum Complex BBR3464. Conformation, recognition by high mobility group domain proteins, and nucleotide excision repair, J. Biol. Chem. 277 (2002) 48076-48086. [168] A.F.A. Peacock, A. Habtemariam, R. Fernandez, V. Walland, F.P.A. Fabbiani, S. Parsons, R.E. Aird, D.I. Jodrell, P.J. Sadler, Tuning the Reactivity of Osmium(II) and Ruthenium(II) Arene Complexes under Physiological Conditions, J. Am. Chem. Soc. 128 (2006) 1739-1748. [169] A.F.A. Peacock, M. Melchart, R.J. Deeth, A. Habtemariam, S. Parsons, P.J. Sadler, Osmium(II) and ruthenium(II) arene maltolato complexes: rapid hydrolysis and nucleobase binding, Chem. Eur. J. 13 (2007) 2601-2613. [170] A.F.A. Peacock, A. Habtemariam, S.A. Moggach, A. Prescimone, S. Parsons, P.J. Sadler, Chloro half-sandwich osmium(II) complexes: influence of chelated N,N-ligands on hydrolysis, guanine binding, and cytotoxicity, Inorg. Chem. 46 (2007) 4049-4059. [171] A.F.A. Peacock, S. Parsons, P.J. Sadler, Tuning the Hydrolytic Aqueous Chemistry of Osmium Arene Complexes with N,O-Chelating Ligands to Achieve Cancer Cell Cytotoxicity, J. Am. Chem. Soc. 129 (2007) 3348-3357. [172] S.H. van Rijt, A.F.A. Peacock, R.D.L. Johnstone, S. Parsons, P.J. Sadler, Organometallic Osmium(II) Arene Anticancer Complexes Containing Picolinate Derivatives, Inorg. Chem. 48 (2009) 1753-1762. [173] H. Kostrhunova, J. Florian, O. Novakova, A.F.A. Peacock, P.J. Sadler, V. Brabec, DNA Interactions of Monofunctional Organometallic Osmium(II) Antitumor Complexes in Cell-Free Media, J. Med. Chem. 51 (2008) 3635-3643.
URI:	http://wrap.warwick.ac.uk/id/eprint/3369