Different Effects of Cisplatin and Transplatin on the Higher-Order Structure of DNA and Gene Expression

Overview

Journal Int J Mol Sci

Publisher MDPI

Specialties Biochemistry
Chemistry
Molecular Biology

Date 2019 Dec 22

PMID 31861648

Citations 4

Authors

Toshifumi Kishimoto

Yuko Yoshikawa

Kenichi Yoshikawa

Seiji Komeda

Affiliations

Soon will be listed here.

Abstract

Despite the effectiveness of cisplatin as an anticancer agent, its trans-isomer, transplatin, is clinically ineffective. Although both isomers target nuclear DNA, there is a large difference in the magnitude of their biological effects. Here, we compared their effects on gene expression in an in vitro luciferase assay and quantified their effects on the higher-order structure of DNA using fluorescence microscopy (FM) and atomic force microscopy (AFM). The inhibitory effect of cisplatin on gene expression was about 7 times that of transplatin. Analysis of the fluctuation autocorrelation function of the intrachain Brownian motion of individual DNA molecules showed that cisplatin increases the spring and damping constants of DNA by one order of magnitude and these visco-elastic characteristics tend to increase gradually over several hours. Transplatin had a weaker effect, which tended to decrease with time. These results agree with a stronger inhibitory effect of cisplatin on gene expression. We discussed the characteristic effects of the two compounds on the higher-order DNA structure and gene expression in terms of the differences in their binding to DNA.

Citing Articles

Characteristic effect of hydroxyurea on the higher-order structure of DNA and gene expression.

Ogawa H, Nishio T, Yoshikawa Y, Sadakane K, Kenmotsu T, Koga T Sci Rep. 2024; 14(1):13826.

PMID: 38879539 PMC: 11180115. DOI: 10.1038/s41598-024-64538-y.

Historical Perspective and Current Trends in Anticancer Drug Development.

Gach-Janczak K, Drogosz-Stachowicz J, Janecka A, Wtorek K, Mirowski M Cancers (Basel). 2024; 16(10).

PMID: 38791957 PMC: 11120596. DOI: 10.3390/cancers16101878.

Quantum Chemical Investigation of the Interaction of Thalidomide Monomeric, Dimeric, Trimeric, and Tetrameric Forms with Guanine DNA Nucleotide Basis in DMSO and Water Solution: A Thermodynamic and NMR Spectroscopy Analysis.

Da Silva H, Hernandes I, De Almeida W ACS Omega. 2023; 8(40):37521-37539.

PMID: 37841183 PMC: 10568699. DOI: 10.1021/acsomega.3c05922.

Design and synthesis of thiadiazolo-carboxamide bridged β-carboline-indole hybrids: DNA intercalative topo-IIα inhibition with promising antiproliferative activity.

Tokala R, Sana S, Lakshmi U, Sankarana P, Sigalapalli D, Gadewal N Bioorg Chem. 2020; 105:104357.

PMID: 33091673 PMC: 7543778. DOI: 10.1016/j.bioorg.2020.104357.

References

Farrell N, Kelland L, Roberts J, Van Beusichem M . 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. 1992; 52(18):5065-72. View

Kasparkova J, Thibault T, Kostrhunova H, Stepankova J, Vojtiskova M, Muchova T . Different affinity of nuclear factor-kappa B proteins to DNA modified by antitumor cisplatin and its clinically ineffective trans isomer. FEBS J. 2014; 281(5):1393-1408. DOI: 10.1111/febs.12711. View

Reedijk J . New clues for platinum antitumor chemistry: kinetically controlled metal binding to DNA. Proc Natl Acad Sci U S A. 2003; 100(7):3611-6. PMC: 152970. DOI: 10.1073/pnas.0737293100. View

Coluccia M, Boccarelli A, Mariggio M, Cardellicchio N, Caputo P, Intini F . Platinum(II) complexes containing iminoethers: a trans platinum antitumour agent. Chem Biol Interact. 1995; 98(3):251-66. DOI: 10.1016/0009-2797(95)03650-4. View

Sandman K, Marla S, Zlokarnik G, Lippard S . Rapid fluorescence-based reporter-gene assays to evaluate the cytotoxicity and antitumor drug potential of platinum complexes. Chem Biol. 1999; 6(8):541-51. DOI: 10.1016/S1074-5521(99)80086-6. View

Paquet F, Boudvillain M, Lancelot G, Leng M . NMR solution structure of a DNA dodecamer containing a transplatin interstrand GN7-CN3 cross-link. Nucleic Acids Res. 1999; 27(21):4261-8. PMC: 148702. DOI: 10.1093/nar/27.21.4261. View

Jamieson E, Lippard S . Structure, Recognition, and Processing of Cisplatin-DNA Adducts. Chem Rev. 2001; 99(9):2467-98. DOI: 10.1021/cr980421n. View

Brabec V, Reedijk J, Leng M . Sequence-dependent distortions induced in DNA by monofunctional platinum(II) binding. Biochemistry. 1992; 31(49):12397-402. DOI: 10.1021/bi00164a014. View

Farrell N, Ha T, Souchard J, Wimmer F, Cros S, Johnson N . Cytostatic trans-platinum(II) complexes. J Med Chem. 1989; 32(10):2240-1. DOI: 10.1021/jm00130a002. View

10.

Kida N, Katsuda Y, Yoshikawa Y, Komeda S, Sato T, Saito Y . Characteristic effect of an anticancer dinuclear platinum(II) complex on the higher-order structure of DNA. J Biol Inorg Chem. 2010; 15(5):701-7. DOI: 10.1007/s00775-010-0637-y. View

11.

Zelazowski A, Garvey J, Hoeschele J . In vivo and in vitro binding of platinum to metallothionein. Arch Biochem Biophys. 1984; 229(1):246-52. DOI: 10.1016/0003-9861(84)90150-4. View

12.

Tashiro T, Kawada Y, Sakurai Y, KIDANI Y . Antitumor activity of a new platinum complex, oxalato (trans-l-1,2-diaminocyclohexane)platinum (II): new experimental data. Biomed Pharmacother. 1989; 43(4):251-60. DOI: 10.1016/0753-3322(89)90004-8. View

13.

Takahara P, Rosenzweig A, Frederick C, Lippard S . Crystal structure of double-stranded DNA containing the major adduct of the anticancer drug cisplatin. Nature. 1995; 377(6550):649-52. DOI: 10.1038/377649a0. View

14.

Bustamante C, Smith S, Liphardt J, Smith D . Single-molecule studies of DNA mechanics. Curr Opin Struct Biol. 2000; 10(3):279-85. DOI: 10.1016/s0959-440x(00)00085-3. View

15.

Coste F, Malinge J, Serre L, Shepard W, Roth M, Leng M . Crystal structure of a double-stranded DNA containing a cisplatin interstrand cross-link at 1.63 A resolution: hydration at the platinated site. Nucleic Acids Res. 1999; 27(8):1837-46. PMC: 148391. DOI: 10.1093/nar/27.8.1837. View

16.

Campbell M, Miller P . Transplatin-conjugated triplex-forming oligonucleotides form adducts with both strands of DNA. Bioconjug Chem. 2009; 20(12):2222-30. PMC: 2796241. DOI: 10.1021/bc900008s. View

17.

Johnson N, Hoeschele J, Rahn R, ONeill J, Hsie A . Mutagenicity, cytotoxicity, and DNA binding of platinum(II)-chloroammines in Chinese hamster ovary cells. Cancer Res. 1980; 40(5):1463-8. View

18.

Hofr C, Brabec V . Thermal and thermodynamic properties of duplex DNA containing site-specific interstrand cross-link of antitumor cisplatin or its clinically ineffective trans isomer. J Biol Chem. 2000; 276(13):9655-61. DOI: 10.1074/jbc.M010205200. View

19.

Brabec V, Leng M . DNA interstrand cross-links of trans-diamminedichloroplatinum(II) are preferentially formed between guanine and complementary cytosine residues. Proc Natl Acad Sci U S A. 1993; 90(11):5345-9. PMC: 46713. DOI: 10.1073/pnas.90.11.5345. View

20.

Wang M, Yin H, Landick R, Gelles J, Block S . Stretching DNA with optical tweezers. Biophys J. 1997; 72(3):1335-46. PMC: 1184516. DOI: 10.1016/S0006-3495(97)78780-0. View