Cubo, Leticia, Pizarro, Ana M., Quiroga, Adoracion G., Salassa, Luca, Navarro-Ranninger, Carmen and Sadler, P. J.. (2010) Photoactivation of trans diamine platinum complexes in aqueous solution and effect on reactivity towards nucleotides. Journal of Inorganic Biochemistry, Vol.104 (No.9). pp. 909-918. ISSN 0162-0134

Preview

PDF WRAP_Pizarro_Photoactivation_PMID_20546905_JInorgBiochem_Script_E-Repositories_(2).pdf - Accepted Version - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader Download (797Kb)

Abstract

We show that UVA irradiation (365 nm) of the Pt-IV complex trans,trans,trans-[(PtCl2)-Cl-IV(OH)(2)(dimethylamine) (isopropylamine)] (1), induces reduction to Pt-II photoproducts. For the mixed amine Pt-II complex, trans[(PtCl2)-Cl-II(isopropylamine)(methylamine)] (2), irradiation at 365 nm increases the rate and extent of hydrolysis, triggering the formation of diaqua species. Additionally, irradiation increases the extent of reaction of complex 2 with guanosine-5'-monophosphate and affords mainly the bis-adduct, while reactions with adenosine-5'-monophosphate and cytidine-5'-monophosphate give rise only to mono-nucleotide adducts. Density Functional Theory calculations have been used to obtain insights into the electronic structure of complexes 1 and 2, and their photophysical and photochemical properties. UVA-irradiation can contribute to enhanced cytotoxic effects of diamine platinum drugs with trans geometry.

Item Type:	Journal Article
Subjects:	Q Science > QD Chemistry
Divisions:	Faculty of Science > Chemistry
Library of Congress Subject Headings (LCSH):	Irradiation, Platinum compounds, Antineoplastic agents, Photochemistry
Journal or Publication Title:	Journal of Inorganic Biochemistry
Publisher:	Elsevier Science Inc
ISSN:	0162-0134
Date:	September 2010
Volume:	Vol.104
Number:	No.9
Number of Pages:	10
Page Range:	pp. 909-918
Identification Number:	10.1016/j.jinorgbio.2010.04.009
Status:	Peer Reviewed
Publication Status:	Published
Access rights to Published version:	Open Access
Funder:	Engineering and Physical Sciences Research Council (EPSRC), Spain. Ministerio de Educación y Ciencia (MEC), Medical Research Council (Great Britain) (MRC), Universidad Autónoma de Madrid (UAM), Seventh Framework Programme (European Commission) (FP7/2007-2013)
Grant number:	SAF2006-03296 (MEC), SAF2009-09431 (MEC), G0701062 (MRC), G006792 (EPSRC), 220281 PHOTORUACD (FP7)
References:	[1] Y. Jung, S.J. Lippard, Direct Cellular Responses to Platinum-Induced DNA Damage, Chem. Rev. 107 (2007) 1387-1407. [2] D. Wang, S.J. Lippard, Cellular processing of platinum anticancer drugs, Nat. Rev. Drug Discovery 4 (2005) 307-320. [3] S.J. Berners-Price, T.G. Appleton, The chemistry of cisplatin in aqueous solution, Platinum-Based Drugs Cancer Ther. (2000) 3-35. [4] 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. [5] C. Manzotti, G. Pratesi, E. Menta, R.D. Domenico, E. Cavalletti, H.H. Fiebig, L.R. Kelland, N. Farrell, D. Polizzi, R. Supino, G. Pezzoni, F. Zunino, BBR 3464: a novel triplatinum complex, exhibiting a preclinical profile of antitumor efficacy different from cisplatin, Clin. Cancer Res. 6 (2000) 2626-2634. [6] Y. Najajreh, E. Khazanov, S. Jawbry, Y. Ardeli-Tzaraf, J.M. Perez, J. Kasparkova, V. Brabec, Y. Barenholz, D. Gibson, Cationic Nonsymmetric Transplatinum Complexes with Piperidinopiperidine Ligands. Preparation, Characterization, in Vitro Cytotoxicity, in Vivo Toxicity, and Anticancer Efficacy Studies, J. Med. Chem. 49 (2006) 4665-4673. [7] M. Coluccia, A. Nassi, F. Loseto, A. Boccarelli, M.A. Mariggio, D. Giordano, F.P. Intini, P. Caputo, G. Natile, A trans-platinum complex showing higher antitumor activity than the cis congeners, J. Med. Chem. 36 (1993) 510-512. [8] E.I. Montero, S. Diaz, A.M. Gonzalez-Vadillo, J.M. Perez, C. Alonso, C. Navarro-Ranninger, Preparation and Characterization of Novel trans-[PtCl2(amine)(isopropylamine)] Compounds: Cytotoxic Activity and Apoptosis Induction in ras-Transformed Cells, J. Med. Chem. 42 (1999) 4264-4268. [9] G. Natile, M. Coluccia, Current status of trans-platinum compounds in cancer therapy, Coord. Chem. Rev. 216-217 (2001) 383-410. [10] G. Natile, M. Coluccia, in: A. Sigel, H. Sigel (Eds.), Met. Ions Biol. Syst., vol. 42, Marcel Dekker, Inc., New York, Basel, Hong Kong, 2004, pp. 209-250. [11] U. Kalinowska-Lis, J. Ochocki, K. Matlawska-Wasowska, Trans geometry in platinum antitumor complexes, Coord. Chem. Rev. 252 (2008) 1328-1345. [12] M.J. Cleare, J.D. Hoeschele, Antitumor activity of Group VIII transition metal complexes. I. Platinum(II) complexes, Bioinorganic Chemistry 2 (1973) 187-210. [13] L. Cubo, D.S. Thomas, J. Zhang, A.G. Quiroga, C. Navarro-Ranninger, S.J. Berners-Price, [1H,15N] NMR studies of the aquation of cis-diamine platinum(II) complexes, Inorg. Chim. Acta 362 (2009) 1022-1026. [14] P.J. Bednarski, F.S. Mackay, P.J. Sadler, Photoactivatable platinum complexes, Anti-Cancer Agents Med. Chem. 7 (2007) 75-93. [15] P.J. Bednarski, R. Gruenert, M. Zielzki, A. Wellner, F.S. Mackay, P.J. Sadler, Light-Activated Destruction of Cancer Cell Nuclei by Platinum Diazide Complexes, Chem. Biol. 13 (2006) 61-67. [16] F.S. Mackay, J.A. Woods, H. Moseley, J. Ferguson, A. Dawson, S. Parsons, P.J. Sadler, A photoactivated trans-diammine platinum complex as cytotoxic as cisplatin, Chem.--Eur. J. 12 (2006) 3155-3161. [17] F.S. Mackay, J.A. Woods, P. Heringova, J. Kasparkova, A.M. Pizarro, S.A. Moggach, S. Parsons, V. Brabec, P.J. Sadler, A potent cytotoxic photoactivated platinum complex, Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 20743-20748. [18] M. Pujol, V. Girona, M. Trillas, X. Domenech, Kinetics of cisplatin photoaquation in aqueous solution, J. Chem. Res., Synop. (1991) 258-259. [19] H.C. Fry, C. Deal, E. Barr, S.D. Cummings, Photoactivation of dichloro(ethylenediamine)platinum(II), J. Photochem. Photobiol., A 150 (2002) 37-40. [20] J.R. Perumareddi, A.W. Adamson, Photochemistry of complex ions. V. Photochemistry of some square-planar platinum(II) complexes, J. Phys. Chem. 72 (1968) 414-420. [21] 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. [22] V. Balzani, V. Carassiti, Photochemistry of some square-planar and octahedral platinum complexes, J. Phys. Chem. 72 (1968) 383-388. [23] V. Balzani, V. Carassiti, in: V. Balzani, V. Carassiti (Eds.), Photochemistry of Coordination Compounds, Academic Press Inc., London and New York, 1970, pp. 245-269. [24] L. Cubo, A.G. Quiroga, J. Zhang, D.S. Thomas, A. Carnero, C. Navarro-Ranninger, S.J. Berners-Price, Influence of amine ligands on the aquation and cytotoxicity of trans-diamine platinum(ii) anticancer complexes, Dalton Trans. (2009) 3457-3466. [25] J.M. Perez, L.R. Kelland, E.I. Montero, F.E. Boxall, M.A. Fuertes, C. Alonso, C. Navarro-Ranninger, Antitumor and cellular pharmacological properties of a novel platinum(IV) complex: trans-[PtCl(2)(OH)(2)(dimethylamine) (isopropylamine)], Mol. Pharmacol. 63 (2003) 933-944. [26] T.-L. Hwang, A.J. Shaka, Water suppression that works. Excitation sculpting using arbitrary waveforms and pulsed field gradients, J. Magn. Reson. 112 (1995) 275-279. [27] M.J. Frisch, GAUSSIAN 03 (Revision C.02), Gaussian, Inc., Wallingford, CT, 2004. [28] J.P. Perdew, K. Burke, M. Ernzerhof, Generalized gradient approximation made simple, Phys. Rev. Lett. 77 (1996) 3865-3868. [29] P.J. Hay, W.R. Wadt, Ab initio effective core potentials for molecular calculations. Potentials for the transition metal atoms scandium to mercury, J. Chem. Phys. 82 (1985) 270-283. [30] A.D. McLean, G.S. Chandler, Contracted Gaussian basis sets for molecular calculations. I. Second row atoms, Z = 11-18, J. Chem. Phys. 72 (1980) 5639-5648. [31] M. Cossi, N. Rega, G. Scalmani, V. Barone, Energies, structures, and electronic properties of molecules in solution with the C-PCM solvation model, J. Comput. Chem. 24 (2003) 669-681. [32] M.E. Casida, C. Jamorski, K.C. Casida, D.R. Salahub, Molecular excitation energies to high-lying bound states from time-dependent density-functional response theory: characterization and correction of the time-dependent local density approximation ionization threshold, J. Chem. Phys. 108 (1998) 4439-4449. [33] R.E. Stratmann, G.E. Scuseria, M.J. Frisch, An efficient implementation of time-dependent density-functional theory for the calculation of excitation energies of large molecules, J. Chem. Phys. 109 (1998) 8218-8224. [34] M. Head-Gordon, A.M. Grana, D. Maurice, C.A. White, Analysis of Electronic Transitions as the Difference of Electron Attachment and Detachment Densities, J. Phys. Chem. 99 (1995) 14261-14270. [35] W.R. Browne, N.M. O'Boyle, J.J. McGarvey, J.G. Vos, Elucidating excited state electronic structure and intercomponent interactions in multicomponent and supramolecular systems, Chem. Soc. Rev. 34 (2005) 641-663. [36] L. Salassa, C. Garino, G. Salassa, C. Nervi, R. Gobetto, C. Lamberti, D. Gianolio, R. Bizzarri, P.J. Sadler, Ligand-selective photodissociation from [Ru(bpy)(4AP)4]2+: a spectroscopic and computational study, Inorg. Chem. 48 (2009) 1469-1481. [37] N.M. O'Boyle, J.G. Vos, GaussSum, Dublin City University. Available at http://gausssum.sourceforge.net, 2005. [38] R. Kuroda, S. Neidle, I.M. Ismail, P.J. Sadler, Crystal and molecular structure of three isomers of dichlorodiamminedihydroxoplatinum(IV): cis-trans isomerization on recrystallization from water, Inorg. Chem. 22 (1983) 3620-3624. [39] C.F.J. Barnard, J.F. Vollano, P.A. Chaloner, S.Z. Dewa, Studies on the Oral Anticancer Drug JM-216: Synthesis and Characterization of Isomers and Related Complexes, Inorg. Chem. 35 (1996) 3280-3284. [40] J.R.L. Priqueler, I.S. Butler, F.D. Rochon, An overview of 195Pt nuclear magnetic resonance spectroscopy, Appl. Spectrosc. Rev. 41 (2006) 185-226. [41] B.M. Still, P.G.A. Kumar, J.R. Aldrich-Wright, W.S. Price, 195Pt NMR - theory and application, Chem. Soc. Rev. 36 (2007) 665-686. [42] P.S. Pregosin, Platinum-195 nuclear magnetic resonance, Coord. Chem. Rev. 44 (1982) 247-291. [43] A. Vlcek, S. Zalis, Modeling of charge-transfer transitions and excited states in d6 transition metal complexes by DFT techniques, Coord. Chem. Rev. 251 (2007) 258-287. [44] L. Salassa, C. Garino, G. Salassa, R. Gobetto, C. Nervi, Mechanism of ligand photodissociation in photoactivable [Ru(bpy)2L2]2+ complexes: a density functional theory study, J. Am. Chem. Soc. 130 (2008) 9590-9597. [45] L. Salassa, H.I.A. Phillips, P.J. Sadler, Decomposition pathways for the photoactivated anticancer complex cis,trans,cis-[Pt(N3)2(OH)2(NH3)2]: insights from DFT calculations, Phys. Chem. Chem. Phys. 11 (2009) 10311-10316. [46] S. Betanzos-Lara, L. Salassa, A. Habtemariam, P.J. Sadler, Photocontrolled nucleobase binding to an organometallic RuII arene complex, Chem. Commun. (2009) 6622-6624. [47] H.I.A. Phillips, L. Ronconi, P.J. Sadler, Photoinduced reactions of cis,trans,cis-[PtIV(N3)2(OH)2(NH3)2] with 1-methylimidazole, Chem.--Eur. J. 15 (2009) 1588-1596. [48] A.T.M. Marcelis, C.G. Van Kralingen, J. Reedijk, The interactions of cis- and trans-diammineplatinum compounds with 5'-guanosine monophosphate and 5'-deoxyguanosine monophosphate. A proton NMR investigation, J. Inorg. Biochem. 13 (1980) 213-222. [49] M.I. Djuran, S.U. Milinkovic, Z.D. Bugarcic, 1H NMR investigation of competitive binding of sulfur-containing peptides and guanosine 5'-monophosphate to a monofunctional platinum(II) complex, J. Coord. Chem. 44 (1998) 289-297. [50] B. Lippert, in: K.D. Karlin (Ed.), Progress in Inorganic Chemistry, vol. 54, John Wiley & Sons, Inc., Hoboken, New Jersey, 2005, pp. 385-447. [51] E. Pantoja, A. Alvarez-Valdes, J.M. Perez, C. Navarro-Ranninger, J. Reedijk, Synthesis and characterization of new cis-[PtCl2(isopropylamine)(amine')] compounds: cytotoxic activity and reactions with 5'-GMP compared with their trans-platinum isomers, Inorg. Chim. Acta 339 (2002) 525-531. [52] S.J. Barton, K.J. Barnham, U. Frey, A. Habtemariam, R.E. Sue, P.J. Sadler, [1H,15N] NMR kinetic studies of reactions of cis- and trans-[PtCl2(15NH3)(c-C6H1115NH2)] with guanosine 5'-monophosphate, Aust. J. Chem. 52 (1999) 173-177. [53] C.G. Barry, C.S. Day, U. Bierbach, Duplex-Promoted Platination of Adenine-N3 in the Minor Groove of DNA: Challenging a Longstanding Bioinorganic Paradigm, J. Am. Chem. Soc. 127 (2005) 1160-1169. [54] M.S. Ali, S.R. Ali Khan, H. Ojima, I.Y. Guzman, K.H. Whitmire, Z.H. Siddik, A.R. Khokhar, Model platinum nucleobase and nucleoside complexes and antitumor activity: X-ray crystal structure of [PtIV(trans-1R,2R-diaminocyclohexane)trans(acetate)2(9-ethylguanine)Cl]NO3.H2O, J. Inorg. Biochem. 99 (2005) 795-804. [55] Y. Liu, M.F. Sivo, G. Natile, E. Sletten, Antitumor trans platinum adducts of GMP and AMP, Met.-Based Drugs 7 (2000) 169-176. [56] U. Bierbach, N. Farrell, Modulation of Nucleotide Binding of trans Platinum(II) Complexes by Planar Ligands. A Combined Proton NMR and Molecular Mechanics Study, Inorg. Chem. 36 (1997) 3657-3665. [57] M.D. Reily, L.G. Marzilli, Anti-Cancer platinum drug adducts with AMP: novel direct proton and platinum-195 and NMR evidence for slowly interconverting "head-to-tail" rotamers. Potential role of amine ligand bulk and NH groups in guanine selectivity and anti-cancer activity, J. Am. Chem. Soc. 108 (1986) 6785-6793. [58] A. Anzellotti, S. Stefan, D. Gibson, N. Farrell, Donor atom preferences in substitution reactions of trans-platinum mononucleobase compounds: Implications for DNA-protein selectivity, Inorg. Chim. Acta 359 (2006) 3014-3019. [59] K.S. Schmidt, J. Reedijk, K. Weisz, E.M.B. Janke, J.E. Sponer, J. Sponer, B. Lippert, Loss of Hoogsteen Pairing Ability upon N1 Adenine Platinum Binding, Inorg. Chem. 41 (2002) 2855-2863. [60] O. Krizanovic, M. Sabat, R. Beyerle-Pfnuer, B. Lippert, Metal-modified nucleobase pairs: mixed adenine, thymine complexes of trans-a2platinum(II) (a = ammonia, methylamine) with Watson-Crick and Hoogsteen orientations of the bases, J. Am. Chem. Soc. 115 (1993) 5538-5548. [61] V. Brabec, M. Leng, DNA interstrand cross-links of trans-diamminedichloroplatinum(II) are preferentially formed between guanine and complementary cytosine residues, Proc. Natl. Acad. Sci. U. S. A. 90 (1993) 5345-5349.
URI:	http://wrap.warwick.ac.uk/id/eprint/5371

Data sourced from Thomson Reuters' Web of Knowledge

Request changes to a record

Actions (login required)

View Item