Abstract
In the reaction of the anticancer drug cis-diamminedichloroplatinum(II) (cis-DDP) with DNA, bifunctional intrastrand and interstrand cross-links are formed. In this work, we show that at 37 degrees C interstrand cross-links (ICL) are labile and rearrange into intrastrand cross-links. The ICL instability was first studied with a 10 base pairs (bp) double-stranded oligonucleotide containing a unique site-specific ICL resulting from chelation of the N7 position of two guanine residues on the opposite strands of DNA at the d(GC/GC) site by a cis-diammineplatinum(II) residue. The bonds between the platinum and the N7 of guanine residues within the interstrand adduct are cleaved. In 50 mM NaCl or NaClO4, this cleavage results in the formation of monofunctional adducts which subsequently form intrastrand cross-links. One cleavage reaction takes place per cross-linked duplex in either of both DNA strands. Whereas the starting cross-linked 10 bp duplex is hydrogen bonded, the two complementary DNA strands separate after the cleavage of the ICL. Under these conditions, the cleavage reaction is irreversible allowing its rate measurement (t1/2= 29+/-2 h) and closure of monofunctional adducts to intrastrand cross-links occurs within single-stranded DNA. Within a longer cross-linked oligonucleotide (20 bp), ICL are apparently more stable (t1/2= 120+/-12 h) as a consequense of monofunctional adducts closure back to ICL. We propose that the ICL cleavage is reversible in DNA and that these adducts rearrange finally into intrastrand cross-links. Our results could explain an 'ICL unhooking' in previously reported in vivo repair studies [Zhenet al. (1993)Carcinogenesis14, 919-924].
Full Text
The Full Text of this article is available as a PDF (143.7 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bernges F., Holler E. The reaction of platinum(II) complexes with DNA. Kinetics of intrastrand crosslink formation in vitro. Nucleic Acids Res. 1991 Apr 11;19(7):1483–1489. doi: 10.1093/nar/19.7.1483. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brabec V., Reedijk J., Leng M. Sequence-dependent distortions induced in DNA by monofunctional platinum(II) binding. Biochemistry. 1992 Dec 15;31(49):12397–12402. doi: 10.1021/bi00164a014. [DOI] [PubMed] [Google Scholar]
- Caporino P. P. How effective are chemical and biological sterilization indicators? J Healthc Mater Manage. 1991 Jan-Feb;9(1):32-4, 36, 38-44. [PubMed] [Google Scholar]
- Chu G. Cellular responses to cisplatin. The roles of DNA-binding proteins and DNA repair. J Biol Chem. 1994 Jan 14;269(2):787–790. [PubMed] [Google Scholar]
- Corda Y., Job C., Anin M. F., Leng M., Job D. Spectrum of DNA--platinum adduct recognition by prokaryotic and eukaryotic DNA-dependent RNA polymerases. Biochemistry. 1993 Aug 24;32(33):8582–8588. doi: 10.1021/bi00084a027. [DOI] [PubMed] [Google Scholar]
- Dalbiès R., Payet D., Leng M. DNA double helix promotes a linkage isomerization reaction in trans-diamminedichloroplatinum(II)-modified DNA. Proc Natl Acad Sci U S A. 1994 Aug 16;91(17):8147–8151. doi: 10.1073/pnas.91.17.8147. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eastman A. Reevaluation of interaction of cis-dichloro(ethylenediamine)platinum(II) with DNA. Biochemistry. 1986 Jul 1;25(13):3912–3915. doi: 10.1021/bi00361a026. [DOI] [PubMed] [Google Scholar]
- Eastman A. The formation, isolation and characterization of DNA adducts produced by anticancer platinum complexes. Pharmacol Ther. 1987;34(2):155–166. doi: 10.1016/0163-7258(87)90009-x. [DOI] [PubMed] [Google Scholar]
- Fichtinger-Schepman A. M., van der Veer J. L., den Hartog J. H., Lohman P. H., Reedijk J. Adducts of the antitumor drug cis-diamminedichloroplatinum(II) with DNA: formation, identification, and quantitation. Biochemistry. 1985 Jan 29;24(3):707–713. doi: 10.1021/bi00324a025. [DOI] [PubMed] [Google Scholar]
- Fichtinger-Schepman A. M., vd Veer J. L., Lohman P. H., Reedijk J. A simple method for the inactivation of monofunctionally DNA-bound cis-diamminedichloroplatinum (II). J Inorg Biochem. 1984 Jun;21(2):103–112. doi: 10.1016/0162-0134(84)85043-6. [DOI] [PubMed] [Google Scholar]
- Gaucheron F., Malinge J. M., Blacker A. J., Lehn J. M., Leng M. Possible catalytic activity of DNA in the reaction between the antitumor drug cis-diamminedichloroplatinum(II) and the intercalator N-methyl-2,7-diazapyrenium. Proc Natl Acad Sci U S A. 1991 May 1;88(9):3516–3519. doi: 10.1073/pnas.88.9.3516. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huang H., Zhu L., Reid B. R., Drobny G. P., Hopkins P. B. Solution structure of a cisplatin-induced DNA interstrand cross-link. Science. 1995 Dec 15;270(5243):1842–1845. doi: 10.1126/science.270.5243.1842. [DOI] [PubMed] [Google Scholar]
- Lambert B., Jestin J. L., Bréhin P., Oleykowski C., Yeung A. T., Mailliet P., Prétot C., Le Pecq J. B., Jacquemin-Sablon A., Chottard J. C. Binding of the Escherichia coli UvrAB proteins to the DNA mono- and diadducts of cis-[N-2-amino-N-2-methylamino-2,2,1-bicycloheptane]dichloroplatinum(II ) and cisplatin. Analysis of the factors controlling recognition and proof of monoadduct-mediated UvrB-DNA cross-linking. J Biol Chem. 1995 Sep 8;270(36):21251–21257. doi: 10.1074/jbc.270.36.21251. [DOI] [PubMed] [Google Scholar]
- Lemaire M. A., Schwartz A., Rahmouni A. R., Leng M. Interstrand cross-links are preferentially formed at the d(GC) sites in the reaction between cis-diamminedichloroplatinum (II) and DNA. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1982–1985. doi: 10.1073/pnas.88.5.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lown J. W., Begleiter A., Johnson D., Morgan A. R. Studies related to antitumor antibiotics. Part V. Reactions of mitomycin C with DNA examined by ethidium fluorescence assay. Can J Biochem. 1976 Feb;54(2):110–119. doi: 10.1139/o76-018. [DOI] [PubMed] [Google Scholar]
- Malinge J. M., Pérez C., Leng M. Base sequence-independent distorsions induced by interstrand cross-links in cis-diamminedichloroplatinum (II)-modified DNA. Nucleic Acids Res. 1994 Sep 25;22(19):3834–3839. doi: 10.1093/nar/22.19.3834. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Malinge J. M., Sip M., Blacker A. J., Lehn J. M., Leng M. Formation of a DNA monofunctional cis-platinum adduct cross-linking the intercalating drug N-methyl-2,7-diazapyrenium. Nucleic Acids Res. 1990 Jul 11;18(13):3887–3891. doi: 10.1093/nar/18.13.3887. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marrot L., Leng M. Chemical probes of the conformation of DNA modified by cis-diamminedichloroplatinum(II). Biochemistry. 1989 Feb 21;28(4):1454–1461. doi: 10.1021/bi00430a005. [DOI] [PubMed] [Google Scholar]
- Maxam A. M., Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. doi: 10.1073/pnas.74.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mello J. A., Lippard S. J., Essigmann J. M. DNA adducts of cis-diamminedichloroplatinum(II) and its trans isomer inhibit RNA polymerase II differentially in vivo. Biochemistry. 1995 Nov 14;34(45):14783–14791. doi: 10.1021/bi00045a020. [DOI] [PubMed] [Google Scholar]
- Paquet F., Pérez C., Leng M., Lancelot G., Malinge J. M. NMR solution structure of a DNA decamer containing an interstrand cross-link of the antitumor drug cis-diamminedichloroplatinum (II). J Biomol Struct Dyn. 1996 Aug;14(1):67–77. doi: 10.1080/07391102.1996.10508930. [DOI] [PubMed] [Google Scholar]
- Payet D., Gaucheron F., Sip M., Leng M. Instability of the monofunctional adducts in cis-[Pt(NH3)2(N7-N-methyl-2-diazapyrenium)Cl](2+)-modified DNA: rates of cross-linking reactions in cis-platinum-modified DNA. Nucleic Acids Res. 1993 Dec 25;21(25):5846–5851. doi: 10.1093/nar/21.25.5846. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pil P. M., Lippard S. J. Specific binding of chromosomal protein HMG1 to DNA damaged by the anticancer drug cisplatin. Science. 1992 Apr 10;256(5054):234–237. doi: 10.1126/science.1566071. [DOI] [PubMed] [Google Scholar]
- Roberts J. J., Friedlos F. Quantitative estimation of cisplatin-induced DNA interstrand cross-links and their repair in mammalian cells: relationship to toxicity. Pharmacol Ther. 1987;34(2):215–246. doi: 10.1016/0163-7258(87)90012-x. [DOI] [PubMed] [Google Scholar]
- Roberts J. J., Pascoe J. M. Cross-linking of complementary strands of DNA in mammalian cells by antitumour platinum compounds. Nature. 1972 Feb 4;235(5336):282–284. doi: 10.1038/235282a0. [DOI] [PubMed] [Google Scholar]
- Segal E., Le Pecq J. B. Role of ligand exchange processes in the reaction kinetics of the antitumor drug cis-diamminedichloroplatinum(II) with its targets. Cancer Res. 1985 Feb;45(2):492–498. [PubMed] [Google Scholar]
- Sip M., Schwartz A., Vovelle F., Ptak M., Leng M. Distortions induced in DNA by cis-platinum interstrand adducts. Biochemistry. 1992 Mar 10;31(9):2508–2513. doi: 10.1021/bi00124a010. [DOI] [PubMed] [Google Scholar]
- Van Houten B., Illenye S., Qu Y., Farrell N. Homodinuclear (Pt,Pt) and heterodinuclear (Ru,Pt) metal compounds as DNA-protein cross-linking agents: potential suicide DNA lesions. Biochemistry. 1993 Nov 9;32(44):11794–11801. doi: 10.1021/bi00095a007. [DOI] [PubMed] [Google Scholar]
- Yang D., van Boom S. S., Reedijk J., van Boom J. H., Wang A. H. Structure and isomerization of an intrastrand cisplatin-cross-linked octamer DNA duplex by NMR analysis. Biochemistry. 1995 Oct 3;34(39):12912–12920. doi: 10.1021/bi00039a054. [DOI] [PubMed] [Google Scholar]
- Zhen W., Evans M. K., Haggerty C. M., Bohr V. A. Deficient gene specific repair of cisplatin-induced lesions in Xeroderma pigmentosum and Fanconi's anemia cell lines. Carcinogenesis. 1993 May;14(5):919–924. doi: 10.1093/carcin/14.5.919. [DOI] [PubMed] [Google Scholar]
- Zhen W., Link C. J., Jr, O'Connor P. M., Reed E., Parker R., Howell S. B., Bohr V. A. Increased gene-specific repair of cisplatin interstrand cross-links in cisplatin-resistant human ovarian cancer cell lines. Mol Cell Biol. 1992 Sep;12(9):3689–3698. doi: 10.1128/mcb.12.9.3689. [DOI] [PMC free article] [PubMed] [Google Scholar]