Skip to main content
SpringerLink
Log in

From cisplatin to artificial nucleases — the role of metal ion-nucleic acid interactions in biology

  • Mini-Review
  • Published:
Biometals Aims and scope Submit manuscript

Abstract

Metal ions and metal coordination compounds bind to nucleic acids in a variety of ways, ranging from weak electrostatic interactions via hydrogen bonding and/or van der Waals forces to strong covalent binding. Metal ions naturally take part in the formation and the degradation of nucleic acids, and the propensity of certain metal coordination compounds to bind to nucleic acids, notably DNA, is enploited in cancer chemotherapy. Moreover, metal compounds have a wide potential as chemical probes for nucleic acid structures and as tools for nucleic acid processing.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Admiraal G, van der Veer JL, de Graaff RAG, den Hartog JHJ, Reedijk J. 1987 Intrastrand bis(guanine) chelation of d(CpGpG) tocis-Platinum: an X-ray single crystal structure analysis.J Am Chem Soc 109, 592–594.

    Google Scholar 

  • Admiraal G, Alink M, Altona C, et al. 1992 Conformation of Pt(dien)[d(ApGpA)-N7(2)] in the solid state and in aqueous solution, as determined with single-crystal X-ray diffraction and high resolution NMR spectroscopy in solution.J Am Chem Soc 114, 930–938.

    Google Scholar 

  • Appleton TG, Connor JW, Hall JR, Prenzler PD. 1989 NMR study of the reactions of thecis-diamminediaquaplatinum(II) cation with glutathione and amino acids containing a thiol group.Inorg Chem 28, 2030–2037.

    Google Scholar 

  • Bailly C, Sun JS, Colson P, et al. 1992 Design of a sequence-specific DNA-cleaving molecule which conjugates a copper-chelating peptide, a netropsin residue, and an acridine chromophore.Bioconjugate Chem 3, 100–113.

    Google Scholar 

  • Baker AD, Morgan RJ, Strekas TC. 1991 Enantiomeric resolution of Ru(phen) 2+3 and Ru(bpy)2ppz 2+ on a DNA-hydroxylapatite column.J Am Chem Soc 113, 1411–1412.

    Google Scholar 

  • Bancroft DP, Lepre CA, Lippard SJ, 1990195Pt NMR kinetic and mechanistic studies ofcis-andtrans-diamminedichloroplatinum(II) binding to DNA.J Am Chem Soc 112, 6860–6871.

    Google Scholar 

  • Barton JK. 1986 Metals and DNA: molecular left-handed complements.Science 233, 727–734.

    PubMed  Google Scholar 

  • Basile LA, Barton JK. 1989 Metallonucleases: real and artificial.Met Ions Biol Syst 25, 31–103.

    Google Scholar 

  • Beese LS, Steitz TA. 1989 Structure ofE. coli DNA polymerase I, large fragment, and its functional implications. In: Eckstein F, Lilley DMJ, eds.Nucleic Acid and Molecular Biology. Vol. 3. Berlin: Springer; 28–43.

    Google Scholar 

  • Bohr VA, Reed E, Zhen W. 1991 Gene specific damage and repair of platinum adducts and crosslinks. In: Howell SB, ed.Platinum and Other Metal Coordination Compounds in Cancer Chemotherapy. New York: Plenum Press; 231–240.

    Google Scholar 

  • Brabec V, Kleinwächter V, Butour JL, Johnson NP. 1990 Biophysical studies of the modification of DNA by antitumor platinum coordination complexes.Biophys Chem 35, 129–141.

    PubMed  Google Scholar 

  • Bruhn SL, Toney JH, Lippard SJ. 1990 Biological processing of DNA modified by platinum compounds.Prog Inorg Chem 38, 477–516.

    Google Scholar 

  • Burnouf D, Gauthier C, Chottard JC, Fuchs RPP. 1990 Single d(ApG)-cis-diamminedichloroplatinum(II) adduct induced mutagenesis inE. coli.Proc Natl Acad Sci USA 87, 6087–6091.

    PubMed  Google Scholar 

  • Chaney SG, Gibbons GR, Wyrick SD, Podhasky P. 1991 An unexpected biotransformation pathway for tetrachloro-(d,1,trans)-1,2-diaminocyclohexaneplatinum(IV) (Tetraplatin) in the L 1210 cell line.Cancer Res 51, 969–973.

    PubMed  Google Scholar 

  • Chen CHB, Sigman DS. 1987 Chemical conversion of a DNA-binding protein into a site-specific nuclease.Science 237, 1197–1201.

    PubMed  Google Scholar 

  • Chen X, Burrows CJ, Rokita SE. 1992 Conformationspecific detection of guanine in DNA: ends, mismatches, bulges, and loops.J Am Chem Soc 114, 322–325.

    Google Scholar 

  • Chow CS, Behlen LS, Uhlenbeck OC, Barton JK. 1992 Recognition of tertiary structure in tRNAs by Rh(phen)2phi3+, a new reagent for RNA structure-function mapping.Biochemistry 31, 972–982.

    PubMed  Google Scholar 

  • Ciccarelli RB, Solomon MJ, Varshavsky A, Lippard SJ. 1985In vivo effects ofcis-andtrans-diamminedichloroplatinum(II) on SV40 chromosomes: differential repair, DNA-protein cross-linking, and inhibition of replication.Biochemistry 24, 7533–7540.

    PubMed  Google Scholar 

  • Comess KM, Costello CE, Lippard SJ. 1990 Identification and characterization of a novel linkage isomerization in the reaction oftrans-diamminedichloroplatinum(II) with 5′-d(TCTACGCGTTCT).Biochemistry 29, 2102–2110.

    PubMed  Google Scholar 

  • Corey DR, Pei D, Schultz PG. 1989 Sequence-selective hydrolysis of duplex DNA by an oligonucleotidedirected nuclease.J Am Chem Soc 111, 8523–8525.

    Google Scholar 

  • Dahm, SAC, Uhlenbeck OC. 1991 Role of divalent metal ions in the hammerhead RNA cleavage reaction.Biochemistry 30, 9464–9469.

    PubMed  Google Scholar 

  • Dange V, Van Atta RB, Hecht SM. 1990 A Mn2+-dependent ribozyme.Science 248, 585–588.

    PubMed  Google Scholar 

  • Dieter-Wurm I, Sabat M, Lippert B. 1992 Model for a platinated DNA triplex: Watson-Crick and metalmodified Hoogsteen pairing.J Am Chem Soc 114, 357–359.

    Google Scholar 

  • Ding L, Etmad-Moghadam G, Meunier B. 1990 Oxidative cleavage of DNA mediated by hybrid metalloporphyrin-ellipticine molecules and functional metalloporphyrin precursors.Biochemistry 29, 7868–7875.

    PubMed  Google Scholar 

  • Eastman A. 1987 Glutathione-mediated activation of anticancer platinum(IV) complexes.Biochem Pharmacol 36, 4177–4178.

    PubMed  Google Scholar 

  • Eastman A, Barry M. 1991 Activation of a genetic program for cell death. In: Howell SB, ed.Platinum and Other Metal Coordination Compounds in Cancer Chemotherapy. New York: Plenum Press; 195–202.

    Google Scholar 

  • Enns RE, Howell SB. 1991 Isolation of a gene associated with resistance to Cisplatin. In: Howell SB, ed.Platinum and Other Metal Coordination Compounds in Cancer Chemotherapy. New York: Plenum Press; 213–220.

    Google Scholar 

  • Eriksson M, Leijon M, Hiort C, Nordén B, Gräslund A. 1992 Minor groove binding of [(Ru(phen)3]2+ to [d(CGCGATCGCG)]2 evidenced by two-dimensional nuclear magnetic resonance spectroscopy.J Am Chem Soc 114, 4933–4934.

    Google Scholar 

  • Faggiani R, Lock CJL, Lippert B. 1981 An unexpected G-G base pairing caused by the coordination of platinum(II) at theN(7) position of 9-ethylguanine.J Am Chem Soc 102, 5418–5419.

    Google Scholar 

  • Farrell N. 1989Transition Metal Complexes as Drugs and Chemotherapeutic Agents. Dordrecht: Kluwer.

    Google Scholar 

  • Farrell N, Ha TTB, Souchard JP, Wimmer FL, Cros S, Johnson NP. 1989 Cytostatictrans-platinum(II) complexes.J Med Chem 32, 2240–2241.

    PubMed  Google Scholar 

  • Farrell N, Qu Y, Hacker MP. 1990 Cytotoxicity and antiturnor activity of bis(platinum) complexes. A novel class of platinum complexes active in cell lines resistant of both cisplatin and 1,2-diaminocyclohexane complexes.J Med Chem 33, 2179–2183.

    PubMed  Google Scholar 

  • Fichtinger-Schepman AMJ, van der Veer JL, den Hartog JHJ, Lohman PHM, Reedijk J. 1985 Adducts of the antitumor drugcis-diamminedichloroplatinum(II) with DNA: formation, identification and quantitation.Biochemistry 24, 707–713.

    PubMed  Google Scholar 

  • Fichtinger-Schepman AMJ, van der Velde-Visser SD, van Dijk-Knijnenburg HCM, van Oosterom AT, Baan RA, Berends F. 1990 Kinetics of the formation and removal of cisplatin-DNA adducts in blood cells and tumor tissue of cancer patients receiving chemotherapy: comparison within vitro adduct formation.Cancer Res 50, 7887–7894.

    PubMed  Google Scholar 

  • Frommer G, Lippert B. 1990 Head-tail oriented nucleobases (B=guanine, cytosine) incis-A2PtB2 resisting cyanide substitution. Implications for the nature of strongly DNA-bound cisplatin.Inorg Chem 29, 3259–3260.

    Google Scholar 

  • Giandomenico CM, Abrams MJ, Murrer BA, et al. 1991 Synthesis and reactions of a new class of orally active Pt(IV) antitumor complexes. In: Howell SB, ed.Platinum and Other Metal Coordination Compounds in Cancer Chemotherapy. New York: Plenum Press; 93–100.

    Google Scholar 

  • Grover N, Thorp HH. 1991 Efficient electrocatalytic and stoichiometric oxidative cleavage of DNA of oxoruthenium(IV).J Am Chem Soc 113, 7030–7031.

    Google Scholar 

  • Guo Q, Lu M, Churchill MEA, Tullius TD, Kallenbach NR. 1990 Asymmetric structure of three-arm DNA junction.Biochemistry 29, 10927–10934.

    PubMed  Google Scholar 

  • Haiduc I, Silvestru C. 1990 Metal compounds in cancer chemotherapy.Coord Chem Rev 99, 253–296.

    Google Scholar 

  • Han H, Rifkind JM, Mildran AS. 1991 Role of divalent cations in the 3′, 5′-exonuclease reaction of DNA polymerase I.Biochemistry 30, 11104–11108.

    PubMed  Google Scholar 

  • Hemminki K, Thilly WG. 1988 Binding of cisplatin to specific sequences of human DNAin vitro.Mutat Res 202, 133–138.

    PubMed  Google Scholar 

  • Hendry P, Sargeson AM. 1990 Metal ion promoted reactions of phosphate derivatives.Prog Inorg Chem 38, 201–258.

    Google Scholar 

  • Herman F, Kozelka J, Stoven V, et al. 1990 A d(GpG)-platinated decanucleotide duplex is kinked.Eur J Biochem 194, 119–133.

    PubMed  Google Scholar 

  • Hertzberg RP, Dervan PB. 1982 Cleavage of double helical DNA by (methidiumpropyl-EDTA) iron(II).J Am Chem Soc 104, 313–315.

    Google Scholar 

  • Hollis LS, Amundsen AR, Stern EW. 1989 Chemical and biological properties of a new series ofcis-diammineplatinum(II) antitumor agents containing three nitrogen donors:cis-[Pt(NH3)2(N-donor)Cl]+.J Med Chem 32, 128–136.

    PubMed  Google Scholar 

  • Howell SB, ed. 1991Platinum and Other Metal Coordination Compounds in Cancer Chemotherapy. New York: Plenum Press.

    Google Scholar 

  • Jones MM, Beaty JA. 1991 Rate of displacement of guanosine by cyanide fromcis-diamminebis(guanosine)platinum(II) chloride determined by using13C NMR spectroscopy.Inorg Chem 30, 1584–1587.

    Google Scholar 

  • Jou R, Cowan JA. 1991 Ribonuclease H activation by inert transition-metal complexes. Mechanistic probes for metallocofactors: insight on the metallobiochemistry of divalent magnesium ion.J Am Chem Soc 113, 6685–6686.

    Google Scholar 

  • Kawanishi S, Yamamoto K. 1991 Mechanism of site-specific DNA damage induced by methylhydrazines in the presence of copper(II) or managanese(III).Biochemistry 30, 3069–3075.

    PubMed  Google Scholar 

  • Keppler BK. 1990 Metal complexes as anticancer agents. The future role of inorganic chemistry in cancer chemotherapy.New J Chem 14, 389–403.

    Google Scholar 

  • Köpf-Maier P, Köpf H. 1988 Transition and main-group metal cyclopentadienyl complexes: preclinical studies on a series of antitumor agents of different structural type.Struct Bond 70, 105–185.

    Google Scholar 

  • Krizanovic O, Pesch FJ, Lippert B. 1989 Nucleobase displacement fromtrans-diammineplatinum(II) complexes. A rationale for the inactivity oftrans-DDP as an antitumor agent?Inorg Chim Acta 165, 145–146.

    Google Scholar 

  • Kuo LY, Kanatzidis MG, Sabat M, Tipton AL, Marks TJ. 1991 Metallocene antitumor agents. Solution and solidstate molybdocene coordination chemistry of DNA constituents.J Am Chem Soc 113, 9027–9045.

    Google Scholar 

  • Lempers ELM, Reedijk J. 1991 Interactions of platinum amine compounds with sulfur-containing biomolecules and DNA fragments.Adv Inorg Chem 37, 175–217.

    Google Scholar 

  • Lepre CA, Chassot L, Costello CE, Lippard SJ. 1990 Synthesis and characterization oftrans-[Pt(NH3)2Cl20 adducts of d(CCTCGAGTCTCC)·d(GGAGACTCG AGG).Biochemistry 29, 811–823.

    PubMed  Google Scholar 

  • Lilley DMJ. 1990 The structure of the helical four-way junction in DNA, and its role in genetic recombination. In: Eckstein F, Lilley DMJ, eds.Nucleic Acids and Molecular Biology. Vol. 4. Berlin: Springer; 55–77.

    Google Scholar 

  • Lim MC, Martin RB. 1976 The nature ofcis-amine Pd(II) and antitumorcis-amine Pt(II) complexes in aqueous solutions.J Inorg Nucl Chem 38, 1911–1914.

    Google Scholar 

  • Lippert B. 1989 Platinum nucleobase chemistry.Prog Inorg Chem 37, 1–97.

    Google Scholar 

  • Lippert B, Lock CJL, Speranzini RA. 1981 Crystal structures oftrans-dichloroammine(1-methylcytosine-N3)platinum(II)hemihydrate andtrans-diamminebis(1-methylcytosine-N3)platinum(II)dinitrate. Evidence for the unexpected lability of NH3 in acis-diammineplatinum(II) complex.Inorg Chem 20, 808–813.

    Google Scholar 

  • Lippert B, Schöllhorn H, Thewalt U. 1986 Metal-stabilized rare tautomers of nucleobases. 1. Iminooxo form of cytosine: formation through metal migration and estimation of the geometry of the free tautomer.J Am Chem Soc 108, 6616–6621.

    Google Scholar 

  • Lippert B, Schöllhorn H, Thewalt U. 1992 Metal-stabilized rare tautomers of nucleobases. 4. On the question of adenine tautomerization by a coordinated platinum(II).Inorg Chim Acta 198–200, 723–732.

    Google Scholar 

  • Lorberth J, El-Essawi M, Massa W, Labib L. 1988 Trimethylplatin-Theophyllin-Hexamer: ein neuartiger Pt6-Heterocyclus mit Pt-N-und Pt-O-Klammern.Angew Chem 100, 1194–1195;Angew Chem Int Ed Engl 27, 1160–1161.

    Google Scholar 

  • Mack DP, Iverson BL, Dervan PB. 1988 Design and chemical synthesis of a sequence-specific DNA-cleaving protein.J Am Chem Soc 110, 7572–7574.

    Google Scholar 

  • Mack DP, Dervan PB. 1990 Nickel-mediated sequencespecific oxidative cleavage of DNA by a designed metalloprotein.J Am Chem Soc 112, 4604–4606.

    Google Scholar 

  • McCall GH, Rabow LE, Ashley GW, Wu SH, Kozarich JW, Stubbe J. 1992 New insight into the mechanism of base propenal formation during bleomycin-mediated DNA degradation.J Am Chem Soc 114, 4958–4967.

    Google Scholar 

  • McLaughlin ML, Cronan JM, Jr, Schaller TR, Snelling RD. 1990 DNA-metal binding by antitumor-active metallocene dichlorides from inductively coupled plasma spectroscopy analysis: titanocene dichloride forms DNA-Cp2Ti or DNA-CpTi adducts depending on pH.J Am Chem Soc 112, 8949–8952.

    Google Scholar 

  • Menzer S, Sabat M, Lippert B. 1992 Ag(I) modified base pairs involving complementary (G,C) and noncomplementary (A,C) nucleobases. On the possible role of aqua ligands in metal-modified nucleobase pairs.J Am Chem Soc 114, 4644–4649.

    Google Scholar 

  • Miller SE, House DA. 1991 The hydrolysis products ofcis-diamminedichloroplatinum(II). 5. The anation kinetics ofcis-Pt(X)(NH3)2(OH2)+(X=Cl, OH) with glycine, monohydrogen malonate and chloride.Inorg Chim Acta 187, 125–132.

    Google Scholar 

  • Modak AS, Gard JK, Merriman MC, Winkeler KA, Bashkin JK, Stern MK. 1991 Toward chemical ribonucleases. 2. Synthesis and characterization of nucleoside-bipyridine conjugates. Hydrolytic cleavage of RNA by their copper(II) complexes.J Am Chem Soc 113, 283–291.

    Google Scholar 

  • Müller F, Holler E. 1989 The effect ofcis-platinum on nucleotide metabolism.Inorg Chim Acta 159, 121–124.

    Google Scholar 

  • Nielsen PE, Jeppesen C, Buchardt O. 1988 Uranyl salts as photochemical agents for cleavage of DNA and probing of protein-DNA contacts.FEBS Lett 235, 122–124.

    PubMed  Google Scholar 

  • Pei D, Schultz PG. 1990 Site-specific cleavage of duplex DNA with a λ-repressor-staphylococcal nuclease hybrid.J Am Chem Soc 112, 4579–4580.

    Google Scholar 

  • Pil PM, Lippard SJ. 1992 Specific binding of chromosomal protein HMG1 to DNA damaged by the anticancer drug cisplatin.Science 156, 234–237.

    Google Scholar 

  • Pratviel G, Pitié M, Bernadou J, Meunier B. 1991 Furfural als Indikator einer DNA-Spaltung durch Hydroxylierung des C5′-Kohlenstoffatoms von Desoxyribose.Angew Chem 103, 718–720;Angew Chem Int Ed Engl 30. 702–704.

    Google Scholar 

  • Pyle AM, Barton JK. 1990 Probing nucleic acids with transition metal complexes.Prog Inorg Chem 38, 413–475.

    Google Scholar 

  • Raudaschl-Sieber G, Lippert B. 1985 Reaction of cyanide with Pt-nucleobase complexes: preparative, spectroscopic, and structural studies. Unexpected stability of Pt-thymine and Pt-uracil complexes.Inorg Chem 24, 2426–2432.

    Google Scholar 

  • Roberts JJ, Knox RJ, Friedlos F, Lydall DA. 1986 DNA as the target for the cytotoxic and antitumor action of platinum co-ordination complexes: comparativein vitro andin vivo studies of cisplatin and carboplatin. In: McBrien DCH, Slater TF, eds.Biochemical Mechanisms of Platinum Antitumor Drugs. Oxford: IRL Press; 29–64.

    Google Scholar 

  • Rosenberg B, Van Camp L, Trosko JE, Mansour VH. 1969 Platinum compounds: a new class of potent antitumor agents.Nature 222, 385–386.

    PubMed  Google Scholar 

  • Rubin JR, Haromy TP, Sundaralingam M. 1991 Structure of the anti-cancer drug complex tetrakis(μ-acetato)-bis-(1-methyladenosine)dirhodium(II)monohydrate.Acta Crystallogr C47, 1712–1714.

    Google Scholar 

  • Schöllhorn H, Thewalt U, Lippert B. 1989 Metal-stabilized rare tautomers of nucleobases. 2,2-Oxo-4-hydroxo form of uracil: crystal structures and solution behaviour of two Platinum(II) complexes containing iminol tautomers of 1-methyluracil.J Am Chem Soc 111, 7213–7221.

    Google Scholar 

  • Schwartz A, Sip M, Leng M. 1990 Sodium cyanide: a chemical probe of the conformation of DNA modifed by the antitumor drugcis-diamminedichloroplatinum(II).J Am Chem Soc 112, 3673–3674.

    Google Scholar 

  • Sherman SE, Lippard SJ. 1987 Structural aspects of platinum anticancer drug interactions with DNA.Chem Rev 87, 1153–1181.

    Google Scholar 

  • Sherman SE, Gibson D, Wang AHJ, Lippard SJ. 1985 X-ray structure of the major adduct of the anticancer drug Cisplatin with DNA:cis-[Pt(NH3)2 {d(pGpG)}].Science 230, 412–417.

    PubMed  Google Scholar 

  • Sigman DS. 1990 Chemical nucleases.Biochemistry 29, 9097–9105.

    PubMed  Google Scholar 

  • Sip M, Schwartz A, Vovelle F, Ptak M, Leng M. 1992 Distortions induced in DNA bycis-platinum interstrand adducts.Biochemistry 31, 2508–2513.

    PubMed  Google Scholar 

  • Strobel SA, Dervan PB. 1990 Site-specific cleavage of a yeast chromosome by oligonucleotide-directed triplehelix formation.Science 249, 73–75.

    PubMed  Google Scholar 

  • Stubbe J, Kozarich JW. 1987 Mechanism of bleomycin-induced DNA degradation.Chem Rev 87, 1007–1136.

    Google Scholar 

  • Tullius TD. 1989 Structural studies of DNA through cleavage by the hydroxyl radical. In: Eckstein F, Lilley DMJ, eds.Nucleic Acids and Molecular Biology. Vol. 3. Berlin: Springer; 1–12.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Fachbereich Chemie, Universität Dortmund, D-4600, Dortmund, Germany

    Bernhard Lippert

Authors
  1. Bernhard Lippert
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lippert, B. From cisplatin to artificial nucleases — the role of metal ion-nucleic acid interactions in biology. Biometals 5, 195–208 (1992). https://doi.org/10.1007/BF01061218

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01061218

Keywords

Search

Navigation