Biopolym. Cell. 2011; 27(4):264-272.
http://dx.doi.org/10.7124/bc.000108
Structure and Function of Biopolymers
Energy of intercalation of aromatic heterocyclic ligands into DNA and its partition into additive components
1Kostyukov V. V.
  1. Sevastopol National Technical University
    33, Universytetska Str., Sevastopol, Ukraine, 99053

Abstract

Aim. Partition of experimental Gibbs energy of complexation with double-stranded DNA into separate energy components for heterocyclic compounds: fascaplysin, ellipticine, trioxatriangulenum (TOTA), thionine (TH), and phenosafranine (PS). Methods. Molecular modeling (molecular dynamics simulation, quantum-mechanical calculations). Results. The energy contributions from different physical factors were calculated, a comparative analysis was performed. Conclusions. It was shown that the major factors stabilizing the intercalation complexes of aromatic compounds with DNA are hydrophobic and van der Waals interactions. The contributions from electrostatic interactions and hydrogen bonds in total and the entropic factors are energetically unfavorable. Electron transfer from DNA to ligand appears to be unlikely.
Keywords: double-stranded DNA, intercalation, aromatic ligand, energy contribution
Full text: (PDF, in Russian)

References

[1] Martinez R., Chacon-Garcia L. The search of DNA-intercalators as antitumoral drugs: what it worked and what did not work Curr. Med. Chem 2005 12, N 2 P. 127–151.
[2] Haq I. Thermodynamics of drug-DNA interactions Arch. Biochem. Biophys 2002 403, N 1 P. 1–15.
[3] Ren J., Jenkins T. C., Chaires J. B. Energetics of DNA intercalation reactions Biochemistry 2000 39, N 29 P. 8439–8447.
[4] Kostjukov V. V., Khomytova N. M., Evstigneev M. P. Partition of thermodynamic energies of drug-DNA complexation Biopolymers 2009 91, N 9 P. 773–790.
[5] Nakamoto K., Tsuboi M., Strahan G. D. Drug-DNA interactions. Structures and spectra New York: John Wiley & Sons, 2008 378 p.
[6] Reynisson J., Schuster G. B., Howerton S. B., Williams L. D., Barnett R. N., Cleveland C. L., Landman U., Harrit N., Chaires J. B. Intercalation of trioxatriangulenium ion in DNA: binding, electron transfer, X-ray crystallography, and electronic structure J. Am. Chem. Soc 2003 125, N 8 P. 2072–2083.
[7] Hormann A., Chaudhuri B., Fretz H. DNA binding properties of the marine sponge pigment fascaplysin Bioorg. Med. Chem 2001 9, N 4 P. 917–921.
[8] Saha I., Hossain M., Kumar G. S. Base pair specificity and energetics of binding of the phenazinium molecules phenosafranine and safranine-O to deoxyribonucleic acids: a comparative study Phys. Chem. Chem. Phys 2010 12, N 39 P. 12771–12779.
[9] Paul P., Hossain M., Yadav R. C., Kumar G. S. Biophysical studies on the base specificity and energetics of the DNA interaction of photoactive dye thionine: spectroscopic and calorimetric approach Biophys. Chem 2010 148, N 1–3 P. 93–103.
[10] Canals A., Purciolas M., Aymami J., Coll M. The anticancer agent ellipticine unwinds DNA by intercalative binding in an orientation parallel to base pairs Acta Crystallogr. D Biol. Crystallogr 2005 61, Pt 7 P. 1009–1012.
[11] Kostjukov V. V., Khomytova N. M., Davies D. B., Evstigneev M. P. Electrostatic contribution to the energy of binding of aromatic ligands with DNA Biopolymers 2008 89, N 8 P. 680– 690.
[12] Chaires J. B. Dissecting the free energy of drug binding to DNA Anticancer Drug Des 1996 11, N 8 P. 569–580.
[13] Kostjukov V. V., Khomytova N. M., Evstigneev M. P. Hydration change on complexation of aromatic ligands with DNA: molecular dynamics simulations Biopolym. Cell 2010 26, N 1 P. 36–44.
[14] Sharp K. A., Nicholls A., Fine R. F., Honig B. Reconciling the magnitude of the microscopic and macroscopic hydrophobic effects Science 1991 252, N 5002 P. 106–109.
[15] Kostjukov V. V., Khomytova N. M., Evstigneev M. P. Referencing of hydrophobic contribution to the free energy of the complexation reactions of aromatic molecules in solution Ukr. Chem. J 2010 76, N 8 P. 96–101.
[16] Kostjukov V. V., Khomytova N. M., Lantushenko A. O., Evstigneev M. P. Hydrophobic contribution to the free energy of complexation of aromatic ligands with DNA Biopolym. Cell 2009 25, N 2 P. 133–141.
[17] Kostyukov V. V., Khomutova N. M., Evstigneev M. P. Contribution of changes in translational, rotational, and vibrational degrees of freedom to the energy of complex formation of aromatic ligands with DNA Biophysics 2009 54, N 4 P. 606– 615.
[18] Reha D., Kabelac M., Ryjacek F., Sponer J., Sponer J. E., Elstner M., Suhai S., Hobza P. Intercalators. 1. Nature of stacking interactions between intercalators (ethidium, daunomycin, ellipticine, and 4',6-diaminide-2-phenylindole) and DNA base pairs. Ab initio quantum chemical, density functional theory, and empirical potential study J. Am. Chem. Soc 2002 124, N 13 P. 3366–3376.
[19] Butchosa C., Simon S., Voityuk A. A. Electron transfer from aromatic amino acids to guanine and adenine radical cations in pi stacked and T-shaped complexes Org. Biomol. Chem 2010 8, N 8:1870–1875.
[20] Baginski M., Fogolari F., Briggs J. M. Electrostatic and nonelectrostatic contributions to the binding free energies of anthracycline antibiotics to DNA J. Mol. Biol 1997 274, N 2 P. 253–267.
[21] Patel N., Bergman J., Graslund A. 1H-NMR studies of the interaction between a self-complementary deoxyoligonucleotide duplex and indolo[2,3-b]quinoxaline derivatives active against herpes virus Eur. J. Biochem 1991 197, N 3 P. 597–604.
[22] Muller W., Crothers D. M. Studies of the binding of actinomycin and related compounds to DNA J. Mol. Biol 1968 35, N 2 P. 251–290.
[23] Kohn K. W., Waring M. J., Glaubiger D., Friedman C. A. Intercalative binding of ellipticine to DNA Cancer Res 1975 35, N 1 P. 71–76.
[24] Saha I., Kumar G. S. Spectroscopic characterization of the interaction of phenosafranin and safranin O with double stranded, heat denatured and single stranded calf thymus DNA J. Fluoresc 2011 21, N 1 P. 247–255.
[25] Ha J.-H., Spolar R. S., Record M. T. Jr. Role of the hydrophobic effect in stability of site-specific protein-DNA complexes J. Mol. Biol 1989 209, N 4 P. 801–816.
[26] Kolar M., Kubar T., Hobza P. Sequence-dependent configurational entropy change of DNA upon intercalation J. Phys. Chem. B 2010 114, N 42 P. 13446–13454.
[27] Baranovsky S. F., Bolotin P. A., Evstigneev M. P., Chernyshev D. N. Complexation of heterocyclic ligands with DNA in aqueous solution J. Appl. Spectrosc 2008 75, N 2 P. 251–260.
[28] Dodin G., Schwaller M.-A., Aubard J., Paoletti C. Binding of ellipticine base and ellipticinium cation to calf-thymus DNA. A thermodynamic and kinetic study Eur. J. Biochem 1988 176, N 2 P. 371–376.
[29] Dolenc J., Oostenbrink C., Koller J., van Gunsteren W. F. Molecular dynamics simulations and free energy calculations of netropsin and distamycin binding to an AAAAA DNA binding site Nucl. Acids Res 2005 33, N 2 P. 725–733.