The Cellular Distribution and Oxidation State of Platinum(II) and Platinum(IV) Antitumour Complexes in Cancer Cells

Overview

Journal J Biol Inorg Chem

Publisher Springer

Specialty Biochemistry

Date 2003 Jul 29

PMID 12884089

Citations 40

Authors

Matthew D Hall

Carolyn T Dillon

Mei Zhang

Philip Beale

Zhonghou Cai

Barry Lai

Anton P J Stampfl

Trevor W Hambley

Affiliations

Soon will be listed here.

Abstract

The cellular distribution of platinum in A2780 ovarian cancer cells treated with cisplatin and platinum(IV) complexes with a range of reduction potentials has been examined using elemental analysis (synchrotron radiation-induced X-ray emission). The cellular distribution of platinum(IV) drugs after 24 h is similar to that of cisplatin, consistent with the majority of administered platinum(IV) drugs being reduced. Micro-X-ray absorption near-edge spectra of cells treated with cisplatin and platinum(IV) complexes confirmed the reduction of platinum(IV) to platinum(II). In cells treated, the most difficult to reduce complex, cis, trans, cis-[PtCl(2)(OH)(2)(NH(3))(2)], platinum(IV) was detected in the cells along with platinum(II). The observations are in accordance with the relative ease of reduction of the platinum(IV) complexes used and support the requirement of reduction for activation of platinum(IV) complexes.

Citing Articles

Promising Anticancer Prodrugs Based on Pt(IV) Complexes with Bis-organosilane Ligands in Axial Positions.

Navas F, Chocarro-Calvo A, Iglesias-Hernandez P, Fernandez-Garcia P, Morales V, Garcia-Martinez J J Med Chem. 2024; 67(8):6410-6424.

PMID: 38592014 PMC: 11056991. DOI: 10.1021/acs.jmedchem.3c02393.

Mesoporous Silica Nanoparticles Enhance the Anticancer Efficacy of Platinum(IV)-Phenolate Conjugates in Breast Cancer Cell Lines.

Predarska I, Saoud M, Draca D, Morgan I, Komazec T, Eichhorn T Nanomaterials (Basel). 2022; 12(21).

PMID: 36364539 PMC: 9659259. DOI: 10.3390/nano12213767.

A platinum-ruthenium hybrid prodrug with multi-enzymatic activities for chemo-catalytic therapy of hypoxic tumors.

Yang G, Su X, Liang B, Pan Z, Cao Q, Mao Z Chem Sci. 2022; 13(38):11360-11367.

PMID: 36320579 PMC: 9533400. DOI: 10.1039/d2sc03375e.

NanoSIMS combined with fluorescence microscopy as a tool for subcellular imaging of isotopically labeled platinum-based anticancer drugs.

Legin A, Schintlmeister A, Jakupec M, Galanski M, Lichtscheidl I, Wagner M Chem Sci. 2022; 5(8):3135-3143.

PMID: 35919909 PMC: 9273000. DOI: 10.1039/c3sc53426j.

Tumor microenvironment-activated single-atom platinum nanozyme with HO self-supplement and O-evolving for tumor-specific cascade catalysis chemodynamic and chemoradiotherapy.

Xu Q, Zhang Y, Yang Z, Jiang G, Lv M, Wang H Theranostics. 2022; 12(11):5155-5171.

PMID: 35836808 PMC: 9274735. DOI: 10.7150/thno.73039.

References

Choi S, Delaney S, Orbai L, Padgett E, Hakemian A . A platinum(IV) complex oxidizes guanine to 8-oxo-guanine in DNA and RNA. Inorg Chem. 2001; 40(22):5481-2. DOI: 10.1021/ic015549t. View

Khan M, Sadler P . Distribution of a platinum anti-tumour drug in HeLa cells by analytical electron microscopy. Chem Biol Interact. 1978; 21(2-3):227-32. DOI: 10.1016/0009-2797(78)90021-2. View

Giandomenico C, Abrams M, Murrer B, Vollano J, Rheinheimer M, Wyer S . Carboxylation of Kinetically Inert Platinum(IV) Hydroxy Complexes. An Entr.acte.ee into Orally Active Platinum(IV) Antitumor Agents. Inorg Chem. 2009; 34(5):1015-21. DOI: 10.1021/ic00109a004. View

Spurr A . A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res. 1969; 26(1):31-43. DOI: 10.1016/s0022-5320(69)90033-1. View

Hall M, Foran G, Zhang M, Beale P, Hambley T . XANES determination of the platinum oxidation state distribution in cancer cells treated with platinum(IV) anticancer agents. J Am Chem Soc. 2003; 125(25):7524-5. DOI: 10.1021/ja0354770. View

Molenaar C, Teuben J, Heetebrij R, Tanke H, Reedijk J . New insights in the cellular processing of platinum antitumor compounds, using fluorophore-labeled platinum complexes and digital fluorescence microscopy. J Biol Inorg Chem. 2000; 5(5):655-65. DOI: 10.1007/s007750000153. View

Chaney S, Wyrick S, Till G . In vitro biotransformations of tetrachloro(d,l-trans)-1,2-diaminocyclohexaneplatinum(IV) (tetraplatin) in rat plasma. Cancer Res. 1990; 50(15):4539-45. View

Dillon C, Lay P, Cholewa M, Legge G, Bonin A, Collins T . Microprobe X-ray absorption spectroscopic determination of the oxidation state of intracellular chromium following exposure of V79 Chinese hamster lung cells to genotoxic chromium complexes. Chem Res Toxicol. 1997; 10(5):533-5. DOI: 10.1021/tx970010m. View

Schilder R, Lacreta F, Perez R, Johnson S, Brennan J, Rogatko A . Phase I and pharmacokinetic study of ormaplatin (tetraplatin, NSC 363812) administered on a day 1 and day 8 schedule. Cancer Res. 1994; 54(3):709-17. View

10.

Pendyala L, Cowens J, CHHEDA G, Dutta S, Creaven P . Identification of cis-dichloro-bis-isopropylamine platinum(II) as a major metabolite of iproplatin in humans. Cancer Res. 1988; 48(12):3533-6. View

11.

Ortega R, Moretto P, Fajac A, Benard J, Llabador Y, Simonoff M . Quantitative mapping of platinum and essential trace metal in cisplatin resistant and sensitive human ovarian adenocarcinoma cells. Cell Mol Biol (Noisy-le-grand). 1996; 42(1):77-88. View

12.

Dillon C, Lay P, Kennedy B, Stampfl A, Cai Z, Ilinski P . Hard X-ray microprobe studies of chromium(VI)-treated V79 Chinese hamster lung cells: intracellular mapping of the biotransformation products of a chromium carcinogen. J Biol Inorg Chem. 2002; 7(6):640-5. DOI: 10.1007/s00775-002-0343-5. View

13.

Braddock P, Connors T, Jones M, Khokhar A, Melzack D, Tobe M . Structure and activity relationships of platinum complexes with anti-tumour activity. Chem Biol Interact. 1975; 11(3):145-61. DOI: 10.1016/0009-2797(75)90095-2. View

14.

Rosenberg B, VANCAMP L, KRIGAS T . INHIBITION OF CELL DIVISION IN ESCHERICHIA COLI BY ELECTROLYSIS PRODUCTS FROM A PLATINUM ELECTRODE. Nature. 1965; 205:698-9. DOI: 10.1038/205698a0. View

15.

McKeage M, Raynaud F, Ward J, Berry C, Odell D, Kelland L . Phase I and pharmacokinetic study of an oral platinum complex given daily for 5 days in patients with cancer. J Clin Oncol. 1997; 15(7):2691-700. DOI: 10.1200/JCO.1997.15.7.2691. View

16.

Gibbons G, Wyrick S, Chaney S . Rapid reduction of tetrachloro(D,L-trans)1,2-diaminocyclohexaneplatinum(IV) (tetraplatin) in RPMI 1640 tissue culture medium. Cancer Res. 1989; 49(6):1402-7. View

17.

Platts J, Hibbs D, Hambley T, Hall M . Calculation of the hydrophobicity of platinum drugs. J Med Chem. 2001; 44(3):472-4. DOI: 10.1021/jm001080k. View

18.

Poon G, Mistry P, Raynaud F, HARRAP K, Murrer B, Barnard C . Determination of metabolites of a novel platinum anticancer drug JM216 in human plasma ultrafiltrates. J Pharm Biomed Anal. 1995; 13(12):1493-8. DOI: 10.1016/0731-7085(95)01571-x. View

19.

Ilinski P, Lai B, Cai Z, Yun W, Legnini D, Talarico T . The direct mapping of the uptake of platinum anticancer agents in individual human ovarian adenocarcinoma cells using a hard X-ray microprobe. Cancer Res. 2003; 63(8):1776-9. View

20.

Wong E, Giandomenico C . Current status of platinum-based antitumor drugs. Chem Rev. 2001; 99(9):2451-66. DOI: 10.1021/cr980420v. View