Biopolym. Cell. 2010; 26(1):36-44.
http://dx.doi.org/10.7124/bc.000142
Structure and Function of Biopolymers
Hydration change on complexation of aromatic ligands with DNA: molecular dynamics simulations
1Kostjukov V. V., 1Khomutova N. M., 1Evstigneev M. P.
  1. Sevastopol National Technical University
    33, Universytetska Str., Sevastopol, Ukraine, 99053

Abstract

Aim. Analysis of the hydration changes at formation of DNA complexes with biologically active aromatic compounds (BAC): antibiotics actinomycin D, daunomycin, nogalamycin, novantrone and mutagens ethidium bromide and proflavine. Methods. Molecular dynamics simulations. Results. The hydration indexes for double-helical DNA and ligands in a free and complexed states were calculated. A critical analysis of modern ideas about changing water environment at binding of aromatic ligands to DNA was performed. Conclusions. It is shown that upon binding of aromatic BAC with DNA a significant (from 2.6 for novantrone to 13.1 for actinomycin D) liberation of water molecules out of hydration shells with the disruption of hydrogen bonds takes place.
Keywords: double-helical DNA, aromatic ligand, hydration index, water release
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References

[1] Brana M. F., Cacho M., Gradillas A., de Pascual-Teresa B., Ramos A. Intercalators as anticancer drugs Curr. Pharm. Des 2001 7, N 17 P. 1745–1780.
[2] Haq I. Thermodynamics of Drug-DNA interactions Arch. Biochem. Biophys 2002 403, N 1 P. 1–15.
[3] Neto J. R., Colombo M. F. Water regulation of actinomycin-D binding to DNA: the interplay among drug affinity, DNA long-range conformation, and hydration Biopolymers 2000 53, N 1 P. 46–59.
[4] Kostjukov V. V., Lantushenko A. O., Davies D. B., Evstigneev M. P. On the origin of the decrease in stability of the DNA hairpin d(GCGAAGC) on complexation with aromatic drugs Biophys. Chem 2007 129, N 1 P. 56–59.
[5] Yu H. J., Ren J. S., Chaires J. B., Qu X. G. Hydration of drugDNA complexes: greater water uptake for adriamycin compared to daunomycin J. Med. Chem 2008 51, N 19 P. 5909–5911.
[6] 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.
[7] Qu X., Chaires J. B. Hydration changes for DNA intercalation reactions J. Am. Chem. Soc 2001 123, N 1 P. 1–3.
[8] 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.
[9] Berman H. M., Westbrook J., Feng Z., Gilliland G., Bhat T. N., Weissig H., Shindyalov I. N., Bourne P. E. The protein data bank Nucl. Acids Res 2000 28, N 1 P. 235–242.
[10] 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.
[11] Brunger A. T. X-PLOR. A system for X-ray crystallography and NMR. Yale: Univ. Press, 1992 382 p.
[12] Chalikian T. V., Sarvazyan A. P., Breslauer K. J. Hydration and partial compressibility of biological compounds. Biophys. Chem 1994 51, N 2 P. 89–107.
[13] Teplukhin A. V., Poltev V. I., Chuprina V. P. Dependence of the hydration shell structure in the minor groove of the DNA double helix on the groove width as revealed by Monte Carlo simulation Biopolymers 1991 31, N 12 P. 1445–1453.
[14] Reha D., Kabelac M., Ryjacek F., Sponer J., 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 J. Amer. Chem. Soc 2002 124, N 13 P. 3366–3376.
[15] 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.
[16] Mukherjee A., Lavery R., Bagchi B., Hynes J. T. On the molecular mechanism of drug intercalation into DNA: a simulation study of the intercalation pathway, free energy, and DNA structural changes J. Am. Chem. Soc 2008 130, N 30 P. 9747–9755.
[17] Degtyareva N. N., Wallace B. D., Bryant A. R., Loo K. M., Petty J. T. Hydration changes accompanying the binding of minor groove ligands with DNA Biophys. J 2007 92, N 3 P. 959–965.
[18] Maleev V., Semenov M., Kruglova E. B., Bolbukh T., Gasan A., Bereznyak E., Shestopalova A. Spectroscopic and calorimetric study of DNA interaction with a new series of actinocin derivatives. J. Mol. Struct. 2003; 645, N 2 P. 145– 158.
[19] Chalikian T. V., Breslauer K. J. Volumetric properties of nucleic acids Biopolymers 1998 48, N 4 P. 264–280.
[20] Marky L. A., Macgregor R. B. J. Hydration of dAdT polymers: role of water in the thermodynamics of ethidium and propidium intercalation Biochemistry 1990 29, N 20 P. 4805–4811.
[21] Han F., Chalikian T. V. Hydration changes accompanying nucleic acid intercalation reactions: volumetric characterizations J. Amer. Chem. Soc 2003 125, N 24 P. 7219– 7229.
[22] Shi X., Macgregor R. B. J. Volume and hydration changes of DNA-ligand interactions Biophys. Chem 2007 125, N 2 P. 471–482.
[23] Sidorova N. Y., Rau D. C. The osmotic sensitivity of netropsin analog binding to DNA Biopolymers 1995 35, N 4 P. 377–384.
[24] Shaikh S. A., Ahmed S. R., Jayaram B. A molecular thermodynamic view of DNA-drug interactions: a case of 25 minorgroove binders Arch. Biochem. Biophys 2004 429, N 1 P. 81–99.
[25] 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. 242–249.
[26] Zavitsas A. A. Properties of water solutions of electrolytes and nonelectrolytes J. Phys. Chem. B 2001 105, N 32 P.7805–7817.