Review Special Issues

Thermal analysis of ligand-DNA interaction: determination of binding parameters

  • Received: 22 July 2015 Accepted: 26 August 2015 Published: 02 September 2015
  • The review discusses the methods of thermodynamic analysis of reactions of non-covalent binding of biologically active compounds with DNA, which is a key constituent of cell chromatin. Knowledge of thermodynamic profile of ligand binding with nucleic acids is important for understanding the mechanism of medico-biological action of the currently existing drugs and for designing of new drugs with improved medical effect. Thermodynamic analysis of ligand binding with DNA is based on analysis of experimentally measured changes of Gibbs free energy (ΔG), enthalpy (ΔH), entropy (ΔS) and heat capacity (ΔCр). Right selection of the methods of measurement of these parameters and understanding of limitations of currently existing approaches for numerical data analysis are crucially important for correct interpretation of the obtained results and getting insight into the mechanism of drug-DNA interaction. In the present work the currently existing methods of determination of thermodynamic parameters of ligand binding with DNA were divided into two main groups. The first group is associated with the approaches used in cases when the heating of the system does not cause melting of the biopolymer. The main focus is given to the second group of the methods which are based on description of helix-coil transition of DNA-ligand complexes with further comparison of the same transition for «free» biopolymer. The methods of computation of the binding parameters utilizing the Ising-type models and models based on the equations of chemical equilibrium are discussed.

    Citation: Ekaterina Bereznyak, Natalia Gladkovskaya, Evgeniy Dukhopelnykov, Anastasiya Gerus, Anastasiya Lantushenko, Maxim Evstigneev. Thermal analysis of ligand-DNA interaction: determination of binding parameters[J]. AIMS Biophysics, 2015, 2(4): 423-440. doi: 10.3934/biophy.2015.4.423

    Related Papers:

  • The review discusses the methods of thermodynamic analysis of reactions of non-covalent binding of biologically active compounds with DNA, which is a key constituent of cell chromatin. Knowledge of thermodynamic profile of ligand binding with nucleic acids is important for understanding the mechanism of medico-biological action of the currently existing drugs and for designing of new drugs with improved medical effect. Thermodynamic analysis of ligand binding with DNA is based on analysis of experimentally measured changes of Gibbs free energy (ΔG), enthalpy (ΔH), entropy (ΔS) and heat capacity (ΔCр). Right selection of the methods of measurement of these parameters and understanding of limitations of currently existing approaches for numerical data analysis are crucially important for correct interpretation of the obtained results and getting insight into the mechanism of drug-DNA interaction. In the present work the currently existing methods of determination of thermodynamic parameters of ligand binding with DNA were divided into two main groups. The first group is associated with the approaches used in cases when the heating of the system does not cause melting of the biopolymer. The main focus is given to the second group of the methods which are based on description of helix-coil transition of DNA-ligand complexes with further comparison of the same transition for «free» biopolymer. The methods of computation of the binding parameters utilizing the Ising-type models and models based on the equations of chemical equilibrium are discussed.


    加载中
    [1]  Finley A, Copeland RA (2014) Small molecule control of chromatin remodeling. Chem Biol 21: 1196–1210. doi: 10.1016/j.chembiol.2014.07.024
    [2]  Prinjha R, Tarakhovsky A (2013) Chromatin targeting drugs in cancer and immunity. Genes Dev 27: 1731–1738. doi: 10.1101/gad.221895.113
    [3]  Rabbani A, Finn RM, Ausio J (2005) The anthracycline antibiotics: antitumor drugs that alter chromatin structure. Bioessays 27: 50–56. doi: 10.1002/bies.20160
    [4]  Majumder P, Pradhan SK, Devi PG, et al. (2007) Chromatin as a target for the DNA-binding anticancer drugs. Subcell Biochem 41: 145–189. doi: 10.1007/1-4020-5466-1_8
    [5]  Banerjee A, Majumder P, Sanyal S, et al. (2014) The DNA intercalators ethidium bromide and propidium iodide also bind to core histones. FEBS Open Bio 4: 251–259. doi: 10.1016/j.fob.2014.02.006
    [6]  Hajihassan Z, Rabbani-Chadegani A (2009) Studies on the binding affinity of anticancer drug mitoxantrone to chromatin, DNA and histone proteins. J Biomed Sci 16: 31. doi: 10.1186/1423-0127-16-31
    [7]  Rabbani-Chadegani A, Chamani E, Hajihassan Z (2009) The effect of vinca alkaloid anticancer drug, vinorelbine, on chromatin and histone proteins in solution. Eur J Pharmacol 613: 34–38. doi: 10.1016/j.ejphar.2009.04.040
    [8]  Rabbani-Chadegani A, Keyvani-Ghamsari S, Zarkar N (2011) Spectroscopic studies of dactinomycin and vinorelbine binding to deoxyribonucleic acid and chromatin. Spectrochim Acta A Mol Biomol Spectrosc 84: 62–67. doi: 10.1016/j.saa.2011.08.064
    [9]  Rabbani A, Iskandar M, Ausio J (1999) Daunomycin-induced unfolding and aggregation of chromatin. J Biol Chem 274: 18401–18406. doi: 10.1074/jbc.274.26.18401
    [10]  Mir MA, Majee S, Das S, et al. (2003) Association of chromatin with anticancer antibiotics, mithramycin and chromomycin A3. Bioorg Med Chem 11: 2791–2801. doi: 10.1016/S0968-0896(03)00211-6
    [11]  Mir MA, Dasgupta D (2001) Association of the anticancer antibiotic chromomycin A(3) with the nucleosome: role of core histone tail domains in the binding process. Biochemistry 40: 11578–11585. doi: 10.1021/bi010731r
    [12]  Mir MA, Dasgupta D (2001) Interaction of antitumor drug, mithramycin, with chromatin. Biochem Biophys Res Commun 280: 68–74. doi: 10.1006/bbrc.2000.4075
    [13]  Hagmar P, Pierrou S, Nielsen P, et al. (1992) Ionic strength dependence of the binding of methylene blue to chromatin and calf thymus DNA. J Biomol Struct Dyn 9: 667–679. doi: 10.1080/07391102.1992.10507947
    [14]  Mir MA, Das S, Dasgupta D (2004) N-terminal tail domains of core histones in nucleosome block the access of anticancer drugs, mithramycin and daunomycin, to the nucleosomal DNA. Biophys Chem 109: 121–135. doi: 10.1016/j.bpc.2003.10.023
    [15]  Hurley LH (2002) DNA and its associated processes as targets forcancer therapy. Nat Rev Cancer 2: 188–200. doi: 10.1038/nrc749
    [16]  Veselkov AN, Davies DB (2002) Anticancer drug design, Sevastopol: Sevntu press, 259.
    [17]  Veselkov AN, Maleev VYa, Glibin EN, et al. (2003) Structure–activity relation for synthetic phenoxazone drugs.Evidence for a direct correlation between DNA binding and pro-apoptotic activity. Eur J Biochem 270: 4200–4207
    [18]  Andersson J, Lincoln P (2011) Stereoselectivity for DNA threading intercalation of short binuclear ruthenium complexes. J Phys Chem B 115: 14768–14775. doi: 10.1021/jp2062767
    [19]  Chaurasiya KR, Paramanathan T, McCauley MJ, et al. (2010) Biophysical characterization of DNA binding from single molecule force measurements. Phys Life Rev 7: 299–341.
    [20]  Nordell P, Lincoln P (2005) Mechanism of DNA threading intercalation of binuclear Ru complexes: uni- or bimolecular pathways depending on ligand structure and binding density. J Am Chem Soc 127: 9670–9671. doi: 10.1021/ja0521674
    [21]  Andersson J, Li M, Lincoln P (2010) AT-specific DNA binding of binuclear ruthenium complexes at the border of threading intercalation. Chemistry 16: 11037–11046.
    [22]  Wilhelmsson LM, Lincoln P, Nordґen B (2006) Slow DNA binding. In: Waring M, editor. Sequence-Specific DNA Binding Agents, The Royal Society of Chemistry, Cambridge, 69–95.
    [23]  Palchaudhuri R, Hergenrother PJ (2007) DNA as a target for anticancer compounds: methods to determine the mode of binding and the mechanism of action. Curr Opin Biotechnol 18: 497–503. doi: 10.1016/j.copbio.2007.09.006
    [24]  Barton TF, Cooney RP, Denny WA (1992) Surface-enhanced Raman spectroscopic study of amsacrine and amsacrine–DNA interactions. J Raman Spectrosc 23: 341–345.
    [25]  Rodger A, Blagbrough IS, Adlam G, et al. (1994) DNA binding of a spermine derivative: Spectroscopic study of anthracene-9-carbonyl-n1-spermine with poly[d(G-C)·(d(G-C))] and poly[d(A-T) · d(A-T)]. Biopolymers 34: 1583–1593. doi: 10.1002/bip.360341203
    [26]  Hackl EV, Galkin VL, Blagoi YP (2004) DNA interaction with biologically active divalent metal ions: binding constants calculation. Int J Biol Macromol 34: 303–308.
    [27]  Evstigneev MP, Mykhina YV, Davies DB (2005) Complexation of daunomycin with a DNA oligomer in the presence of an aromatic vitamin (B2) determined by NMR spectroscopy. Biophys Chem 118: 118–127. doi: 10.1016/j.bpc.2005.08.007
    [28]  Hackl EV, Blagoi YP (2005) The effect of temperature on DNA structural transitions under the action of Cu2+ and Ca2+ ions in aqueous solutions. Biopolymers 77: 315–324. doi: 10.1002/bip.20225
    [29]  Kruglova EB, Gladkovskaia NA, Maleev V (2005) The use of the spectrophotometric analysis for the calculation of the thermodynamic parameters in actinocin derivative-DNA systems. Biofizika 50: 253–264.
    [30]  Evstigneev MP, Baranovskii SF, Rybakova KA, et al. (2006) 1H NMR study of the complexation of the quinolone antibiotic norfloxacin with DNA. Mol Biol (Mosk) 40: 894–899.
    [31]  Evstigneev MP, Rybakova KA, Davies DB (2006) Complexation of norfloxacin with DNA in the presence of caffeine. Biophys Chem 121: 84–95. doi: 10.1016/j.bpc.2005.12.003
    [32]  Williams AK, Dasilva SC, Bhatta A, et al. (2012) Determination of the drug-DNA binding modes using fluorescence-based assays. Anal Biochem 422: 66–73. doi: 10.1016/j.ab.2011.12.041
    [33]  Anupama B, Sunita M, Shiva LD, et al. (2014) Synthesis, spectral characterization, DNA binding studies and antimicrobial activity of Co(II), Ni(II), Zn(II), Fe(III) and VO(IV) complexes with 4-aminoantipyrine Schiff base of ortho-vanillin. J Fluoresc 24: 1067–1076. doi: 10.1007/s10895-014-1386-z
    [34]  Zasedatelev AS, Gurskii GV, Vol'kenshtein MV (1971) Theory of one-dimensional adsorption. I. Adsorption of small molecules on a homopolymer. Molecular biology 5: 194–198.
    [35]  McGhee JD, von Hippel PH (1974) Theoretical aspects of DNA-protein interactions: co-operative and non-co-operative binding of large ligands to a one-dimensional homogeneous lattice. J Mol Biol 86: 469–489. doi: 10.1016/0022-2836(74)90031-X
    [36]  Schellman JA (1974) Cooperative Multisite Binding to DNA. Israel Journal of Chemistry 12: 219–238. doi: 10.1002/ijch.197400021
    [37]  Nechipurenko YD, Gursky GV (1986) Cooperative effects on binding of proteins to DNA. Biophys Chem 24: 195–209. doi: 10.1016/0301-4622(86)85025-6
    [38]  Lando DY, Teif VB (2000) Long-range interactions between ligands bound to a DNA molecule give rise to adsorption with the character of phase transition of the first kind. J Biomol Struct Dyn 17: 903–911. doi: 10.1080/07391102.2000.10506578
    [39]  Teif VB, Rippe K (2010) Statistical-mechanical lattice models for protein-DNA binding in chromatin. J Phys Condens Matter 22: 414105. doi: 10.1088/0953-8984/22/41/414105
    [40]  Breslauer KJ, Freire E, Straume M (1992) Calorimetry: a tool for DNA and ligand-DNA studies. Methods Enzymol 211: 533–567.
    [41]  Doyle ML (1997) Characterization of binding interactions by isothermal titration calorimetry. Curr Opin Biotechnol 8: 31–35. doi: 10.1016/S0958-1669(97)80154-1
    [42]  Jelesarov I, Bosshard HR (1999) Isothermal titration calorimetry and differential scanning calorimetry as complementary tools to investigate the energetics of biomolecular recognition. J Mol Recognit 12: 3–18.
    [43]  Haq I, Chowdhry BZ, Jenkins TC (2001)Calorimetric techniques in the study of high-order DNA-drug interactions. Methods Enzymol 340: 109–149.
    [44]  Thomson JA, Ladbury JE (2004) Isothermal titration calorimetry: a tutorial. In Ladbury JE, Doyle ML, editors. Biocalorimetry 2. Applications of Calorimetry in the Biological Sciences, Chichester: John Wiley & Sons, 35–58.
    [45]  Holdgate GA, Ward WH (2005) Measurements of binding thermodynamics in drug discovery. Drug Discov Today 10: 1543–1550.
    [46]  Freyer MW, Lewis EA (2008) Isothermal titration calorimetry: experimental design, data analysis, and probing macromolecule/ligand binding and kinetic interactions. Methods Cell Biol 84: 79–113. doi: 10.1016/S0091-679X(07)84004-0
    [47]  Bhadra K, Maiti M, Kumar GS (2008) Berberine–DNA complexation: New insights into the cooperative binding and energetic aspects. Biochimica et Biophysica Acta 1780: 1054–1061. doi: 10.1016/j.bbagen.2008.05.005
    [48]  Hossain M, Kumar GS (2009) DNA intercalation of methylene blue and quinacrine: new insights into base and sequence specificity from structural and thermodynamic studies with polynucleotides. Mol Biosyst 5: 1311–1322.
    [49]  Crane-Robinson C, Dragan AI, Read CM (2009) Defining the thermodynamics of protein/DNA complexes and their components using micro-calorimetry. Methods Mol Biol 543: 625–651. doi: 10.1007/978-1-60327-015-1_37
    [50]  Kabir A, Kumar GS (2013) Binding of the biogenic polyamines to deoxyribonucleic acids of varying base composition: base specificity and the associated energetics of the interaction. PLoS One 8: e70510. doi: 10.1371/journal.pone.0070510
    [51]  Kumar S, Spano MN, Arya DP (2014) Shape readout of AT-rich DNA by carbohydrates. Biopolymers 101: 720–732. doi: 10.1002/bip.22448
    [52]  Basu A, Kumar GS (2015) Thermodynamic characterization of proflavine–DNA binding through microcalorimetric studies. J Chem Thermodyn 87: 1–7. doi: 10.1016/j.jct.2015.03.009
    [53]  Basu A, Kumar GS (2015) Studies on the interaction of the food colorant tartrazine with double stranded deoxyribonucleic acid. J Biomol Struct Dyn 10: 1–8.
    [54]  Chaires JB (1997) Possible origin of differences between van't Hoff and calorimetric enthalpy estimates. Biophys Chem 64: 15–23.
    [55]  Chaires JB (2008) Calorimetry and thermodynamics in drug design. Annu Rev Biophys 37: 135–151.
    [56]  Janjua NK, Siddiqa A, Yaqub A, et al. (2009) Spectrophotometric analysis of flavonoid-DNA binding interactions at physiological conditions. Spectrochim Acta A Mol Biomol Spectrosc 74: 1135–1137. doi: 10.1016/j.saa.2009.09.022
    [57]  Temerk YM, Ibrahim MS, Kotb M (2009) Voltammetric and spectroscopic studies on binding of antitumor Morin, Morin-Cu complex and Morin-beta-cyclodextrin with DNA. Spectrochim Acta A Mol Biomol Spectrosc 71: 1830–1836. doi: 10.1016/j.saa.2008.07.001
    [58]  Baranovskii SF, Chernyshev DN, Buchel’nikov AS, et al. (2011) Thermodynamic analysis of complex formation of ethidium bromide with DNA in water solutions. Biophysics 56: 214–219. doi: 10.1134/S0006350911020023
    [59]   Chaires JB (1997) Energetics of drug-DNA interactions. Biopolymers 44: 201–215.
    [60]   Ren J, Jenkins TC, Chaires JB (2000) Energetics of DNA intercalation reactions. Biochemistry 39: 8439–8447. doi: 10.1021/bi000474a
    [61]  Davies DB, Veselkov AN (1996) Structural and thermodynamical analysis of molecular complexation by 1H NMR spectroscopy. Intercalation of ethidium bromide with the isomeric deoxytetranucleoside triphosphates 5’-d(GpCpGpC) and 5’-d(CpGpCpG) in aqueous solution. J Chem Soc Faraday Trans 92: 3545-3557. doi: 10.1039/ft9969203545
    [62]  Kostjukov VV, Pahomov VI, Andrejuk DD, et al. (2007) Investigation of the complexation of the anti-cancer drug novantrone with the hairpin structure of the deoxyheptanucleotide 5′-d(GpCpGpApApGpC). J Mol Struct 843: 78–86. doi: 10.1016/j.molstruc.2006.12.036
    [63]  Wartell RM, Benight AS (1985) Thermal denaturation of DNA molecules: A comparison of theory with experiment. Phys Rep 126: 67–107. doi: 10.1016/0370-1573(85)90060-2
    [64]  Rice SA, Doty P (1957) The Thermal Denaturation of Desoxyribose Nucleic Acid. J Am Chem Soc 79: 3937–3947. doi: 10.1021/ja01572a001
    [65]  Guedin A, Lacroix L, Mergny JL (2010) Thermal melting studies of ligand DNA interactions. Methods Mol Biol 613: 25–35. doi: 10.1007/978-1-60327-418-0_2
    [66]  Goldstein G, Stern KG (1950) Experiments on the sonic, thermal, and enzymic depolymerization of desoxyribosenucleic acid. J Struc Chem 5: 687–708.
    [67]  Thomas R (1954) Recherches sur la d'enaturation des acides desoxyribonucléiques. Biochimica et Biophysica Acta 14: 231–240. doi: 10.1016/0006-3002(54)90163-8
    [68]  Frank-Kamenetskii M (1965) Theory of the helix–coil transition for deoxyribonucleic acids with additional connections between the chains. Vysokomolekulyarnye Soedineniya 7: 354–361.
    [69]  Frank-Kamenetskii M (1968) Consideration of helix-coil transition in homopolymers by the most probable distribution method. Mol Biol 2: 408–419.
    [70]  Stewart CR (1968) Broadening by acridine orange of the thermal transition of DNA. Biopolymers 6: 1737–1743. doi: 10.1002/bip.1968.360061208
    [71]  Lazurkin YS, Frank-Kamenetskii MD, Trifonov EN (1970) Melting of DNA: its study and application as a research method. Biopolymers 9: 1253–1306. doi: 10.1002/bip.1970.360091102
    [72]  Barcelo F, Capo D, Portugal J (2002) Thermodynamic characterization of the multivalent binding of chartreusin to DNA. Nucleic Acids Res 30: 4567–4573. doi: 10.1093/nar/gkf558
    [73]  Zhong W, Yu JS, Liang Y (2003) Chlorobenzylidine-herring sperm DNA interaction: binding mode and thermodynamic studies. Spectrochim Acta A Mol Biomol Spectrosc 59: 1281–1288. doi: 10.1016/S1386-1425(02)00301-3
    [74]  Vardevanyan PO, Antonyan AP, Hambardzumyan LA, et al. (2013) Thermodynamic analysis of DNA complexes with methylene blue, ethidium bromide and Hoechst 33258. Biopolym. Cell 29: 515–520. doi: 10.7124/bc.000843
    [75]  Hajian R, Guan Huat T (2013) Spectrophotometric Studies on the Thermodynamics of the ds-DNA Interaction with Irinotecan for a Better Understanding of Anticancer Drug-DNA Interactions. J Spectrosc 2013: 1–8.
    [76]  Cooper A, Johnson CM (1994) Introduction to microcalorimetry and biomolecular energetics. Methods Mol Biol 22: 109–24.
    [77]  Rosgen J, Hinz HJ (1999) Theory and practice of DSC mesuarements on proteins. In: Kemp RB, editor. Handbook of Thermal Analysis and Calorimetry, Vol.4, From Macromolecules to Man, Amsterdam: Elsevier, 63–108.
    [78]  Bruylants G, Wouters J, Michaux C (2005) Differential scanning calorimetry in life science: thermodynamics, stability, molecular recognition and application in drug design. Curr Med Chem 12: 2011–2020. doi: 10.2174/0929867054546564
    [79]  Spink CH (2008) Differential scanning calorimetry. Methods Cell Biol 84: 115–141. doi: 10.1016/S0091-679X(07)84005-2
    [80]  Bereznyak EG, Gladkovskaya NA, Khrebtova AS, et al. (2009) Peculiarities of DNA-proflavine binding under different concentration ratios. Biophysics 54: 574–580. doi: 10.1134/S0006350909050030
    [81]  Garbett N (2011) The Use of Calorimetry to Study Ligand–DNA Interactions. In: Aldrich-Wright J, editor. Metallointercalators, Vienna: Springer, 299–324.
    [82]  Ising E (1925) Beitrag zur Theorie des Ferromagnetismus. Zeitschrift für Physik 31: 253–258. doi: 10.1007/BF02980577
    [83]  Poland DC, Scheraga HA (1970) The theory of helix coil transition, New York: Academic Press.
    [84]  Peyrard M, Bishop AR (1989) Statistical mechanics of a nonlinear model for DNA denaturation. Phys Rev Lett 62: 2755–2758. doi: 10.1103/PhysRevLett.62.2755
    [85]  Dauxois T, Peyrard M, Bishop AR (1993) Entropy-driven DNA denaturation. Physical Review E 47: R44–R47. doi: 10.1103/PhysRevE.47.R44
    [86]  Dauxois T, Peyrard M, Bishop AR (1993) Dynamics and thermodynamics of a nonlinear model for DNA denaturation. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 47: 684–695.
    [87]  Grosberg AIU, Khokhlov AR (1994) Statistical physics of macromolecules, New York: AIP Press.
    [88]  Frank-Kamenetskii MD, Prakash S (2014) Fluctuations in the DNA double helix: A critical review. Phys Life Rev 11: 153–170. doi: 10.1016/j.plrev.2014.01.005
    [89]  Cantor CR, Schimmel PR (1980) Biophysical chemistry. 3. The behavior of biological macromolecules, San Francisco, Freeman.
    [90]  Zimm BH, Bragg JK (1959) Theory of the Phase Transition between Helix and Random Coil in Polypeptide Chains. J Chem Phys 31: 526–535. doi: 10.1063/1.1730390
    [91]  Crothers DM (1971) Statistical thermodynamics of nucleic acid melting transitions with coupled binding equilibria. Biopolymers 10: 2147–2160. doi: 10.1002/bip.360101110
    [92]  McGhee JD (1976) Theoretical calculations of the helix-coil transition of DNA in the presence of large, cooperatively binding ligands. Biopolymers 15: 1345–1375. doi: 10.1002/bip.1976.360150710
    [93]   Akhrem AA, Fridman AS, Lando D (1985) Theory of helix-coil transition of the heterogeneous DNA-heteroqeneous ligands complexes. Biopolym Cell 1: 171–179. doi: 10.7124/bc.00017E
    [94]  Lando D (1994) A theoretical consideration of the influence of selective binding of small ligands on DNA helix-coil transition. J Biomol Struct Dyn 12: 343–354. doi: 10.1080/07391102.1994.10508744
    [95]   Akhrem AA, Lando D (1979) Influence of ligands characteristic of selective binding to a certain type of base pairs on DNA helix-coil transition I. Model. Theory. Mol Biol (Mosk) 13: 1098–1109.
    [96]  Akhrem AA, Lando D, Shpakovskii AG, et al. (1990) The effect of long-range interactions between adsorbed ligands on the DNA helix-coil transition. Mol Biol (Mosk) 24: 649–656.
    [97]  Lando D, Ivanova MA, Akhrem AA (1980) Effect of changes in the stoichiometry of DNA-ligand complexes during heat denaturation of DNA on helix-coil transition parameters. Mol Biol (Mosk) 14: 1281–1288.
    [98]  Karapetian AT, Mehrabian NM, Terzikian GA, et al. (1996) Theoretical treatment of melting of complexes of DNA with ligands having several types of binding sites on helical and single-stranded DNA. J Biomol Struct Dyn 14: 275–283. doi: 10.1080/07391102.1996.10508118
    [99]  Plum GE, Bloomfield VA (1990) Structural and electrostatic effects on binding of trivalent cations to double-stranded and single-stranded poly[d (AT)]. Biopolymers 29: 13–27. doi: 10.1002/bip.360290105
    [100]   Spink CH, Chaires JB (1997) Thermodynamics of the Binding of a Cationic Lipid to DNA. J Am Chem Soc 119: 10920–10928. doi: 10.1021/ja964324s
    [101]   Leng F, Chaires JB, Waring MJ (2003) Energetics of echinomycin binding to DNA. Nucleic Acids Res 31: 6191–6197. doi: 10.1093/nar/gkg826
    [102]   Pasic L, Sepcic K, Turk T, et al. (2001) Characterization of parazoanthoxanthin A binding to a series of natural and synthetic host DNA duplexes. Arch Biochem Biophys 393: 132–142. doi: 10.1006/abbi.2001.2469
    [103]   Portugal J, Cashman DJ, Trent JO, et al. (2005) A new bisintercalating anthracycline with picomolar DNA binding affinity. J Med Chem 48: 8209–8219. doi: 10.1021/jm050902g
    [104]   Liu Y-J, Wei X, Mei W-J, et al. (2007) Synthesis, characterization and DNA binding studies of ruthenium(II) complexes: [Ru(bpy)2(dtmi)]2+ and [Ru(bpy)2(dtni)]2+. Transit Metal Chem 32: 762–768. doi: 10.1007/s11243-007-0246-y
    [105]   Peng B, Chen X, Du KJ, et al. (2009) Synthesis, characterization and DNA-binding studies of ruthenium(II) mixed-ligand complexes containing dipyrido[1,2,5]oxadiazolo[3,4-b]quinoxaline. Spectrochim Acta A Mol Biomol Spectrosc 74: 896–901. doi: 10.1016/j.saa.2009.08.031
    [106]   Barcelo F, Portugal J (2004) Elsamicin A binding to DNA. A comparative thermodynamic characterization. FEBS Lett 576: 68–72.
    [107]   Barcelo F, Scotta C, Ortiz-Lombardia M, et al. (2007) Entropically-driven binding of mithramycin in the minor groove of C/G-rich DNA sequences. Nucleic Acids Res 35: 2215–2226. doi: 10.1093/nar/gkm037
    [108]   Marky LA, Blumenfeld KS, Breslauer KJ (1983) Calorimetric and spectroscopic investigation of drug-DNA interactions. I. The binding of netropsin to poly d(AT). Nucleic Acids Res 11: 2857–2870.
    [109]   Remeta DP, Mudd CP, Berger RL, et al (1993) Thermodynamic characterization of daunomycin-DNA interactions: comparison of complete binding profiles for a series of DNA host duplexes. Biochemistry 32: 5064–5073. doi: 10.1021/bi00070a014
    [110]   Brandts JF, Lin LN (1990) Study of strong to ultratight protein interactions using differential scanning calorimetry. Biochemistry 29: 69276940.
    [111]   Barone G, Catanzano F, Del Vecchio P, et al. (1995) Differential scanning calorimetry as a tool to study protein-ligand interactions. Pure Appl Chem 67: 1867–1872.
    [112]   Dassie SA, Celej MS, Fidelio GD (2005) Protein Unfolding Coupled to Ligand Binding: Differential Scanning Calorimetry Simulation Approach. J Chem Educ 82: 85. doi: 10.1021/ed082p85
    [113]   Celej MS, Dassie SA, Gonzalez M, et al. (2006) Differential scanning calorimetry as a tool to estimate binding parameters in multiligand binding proteins. Anal Biochem 350: 277–284. doi: 10.1016/j.ab.2005.12.029
    [114]   Esposito D, Del Vecchio P, Barone G (2001) A thermodynamic study of herring protamine-DNA complex by differential scanning calorimetry. Phys Chem Chem Phys 3: 5320–5325. doi: 10.1039/b107218h
    [115]   Dukhopelnikov EV, Bereznyak EG, Khrebtova AS, et al. (2013) Determination of ligand to DNA binding parameters from two-dimensional DSC curves. J Therm Anal Calorim 111: 1817–1827. doi: 10.1007/s10973-012-2561-6
    [116]   Straume M, Freire E (1992) Two-dimensional differential scanning calorimetry: Simultaneous resolution of intrinsic protein structural energetics and ligand binding interactions by global linkage analysis. Anal Biochem 203: 259–268. doi: 10.1016/0003-2697(92)90311-T
    [117]   Freire E (1994) Statistical thermodynamic analysis of differential scanning calorimetry data: structural deconvolution of heat capacity function of proteins. Methods Enzymol 240: 502–530. doi: 10.1016/S0076-6879(94)40062-8
    [118]   Freire E (1995) Differential scanning calorimetry. Methods Mol Biol 40: 191–218.
    [119]   Marky LA, Breslauer KJ (1987) Calculating thermodynamic data for transitions of any molecularity from equilibrium melting curves. Biopolymers 26: 1601–1620. doi: 10.1002/bip.360260911
    [120]   Sturtevant JM (1987) Biochemical Applications of Differential Scanning Calorimetry. Annu Rev Phys Chem 38: 463–488. doi: 10.1146/annurev.pc.38.100187.002335
    [121]   Kawai Y (1999) Thermal transition profiles of bacteriophage T4 and its DNA. J Gen Appl Microbiol 45: 135–138. doi: 10.2323/jgam.45.135
    [122]   Tostesen E, Sandve GK, Liu F, et al. (2009) Segmentation of DNA sequences into twostate regions and melting fork regions. J Phys Condens Matter 21: 034109. doi: 10.1088/0953-8984/21/3/034109
    [123]   Duguid JG, Bloomfield VA, Benevides JM, et al. (1996) DNA melting investigated by differential scanning calorimetry and Raman spectroscopy. Biophys J 71: 3350–3360.
    [124]   Movileanu L, Benevides JM, Thomas GJ (2002) Determination of base and backbone contributions to the thermodynamics of premelting and melting transitions in B DNA. Nucleic Acids Res 30: 3767–3777. doi: 10.1093/nar/gkf471
    [125]   Dukhopelnikov EV (2014) Modeling of heat absorption curves for ligand-competitor-DNA triple system. Biophysical Bulletin 31: 49–58.
    [126] 1. Finley A, Copeland RA (2014) Small molecule control of chromatin remodeling. Chem Biol 21: 1196-1210. doi: 10.1016/j.chembiol.2014.07.024
    [127] 2. Prinjha R, Tarakhovsky A (2013) Chromatin targeting drugs in cancer and immunity. Genes Dev 27: 1731-1738. doi: 10.1101/gad.221895.113
    [128] 3. Rabbani A, Finn RM, Ausio J (2005) The anthracycline antibiotics: antitumor drugs that alter chromatin structure. Bioessays 27: 50-56. doi: 10.1002/bies.20160
    [129] 4. Majumder P, Pradhan SK, Devi PG, et al. (2007) Chromatin as a target for the DNA-binding anticancer drugs. Subcell Biochem 41: 145-189. doi: 10.1007/1-4020-5466-1_8
    [130] 5. Banerjee A, Majumder P, Sanyal S, et al. (2014) The DNA intercalators ethidium bromide and propidium iodide also bind to core histones. FEBS Open Bio 4: 251-259. doi: 10.1016/j.fob.2014.02.006
    [131] 6. Hajihassan Z, Rabbani-Chadegani A (2009) Studies on the binding affinity of anticancer drug mitoxantrone to chromatin, DNA and histone proteins. J Biomed Sci 16: 31. doi: 10.1186/1423-0127-16-31
    [132] 7. Rabbani-Chadegani A, Chamani E, Hajihassan Z (2009) The effect of vinca alkaloid anticancer drug, vinorelbine, on chromatin and histone proteins in solution. Eur J Pharmacol 613: 34-38. doi: 10.1016/j.ejphar.2009.04.040
    [133] 8. Rabbani-Chadegani A, Keyvani-Ghamsari S, Zarkar N (2011) Spectroscopic studies of dactinomycin and vinorelbine binding to deoxyribonucleic acid and chromatin. Spectrochim Acta A Mol Biomol Spectrosc 84: 62-67. doi: 10.1016/j.saa.2011.08.064
    [134] 9. Rabbani A, Iskandar M, Ausio J (1999) Daunomycin-induced unfolding and aggregation of chromatin. J Biol Chem 274: 18401-18406. doi: 10.1074/jbc.274.26.18401
    [135] 10. Mir MA, Majee S, Das S, et al. (2003) Association of chromatin with anticancer antibiotics, mithramycin and chromomycin A3. Bioorg Med Chem 11: 2791-2801. doi: 10.1016/S0968-0896(03)00211-6
    [136] 11. Mir MA, Dasgupta D (2001) Association of the anticancer antibiotic chromomycin A(3) with the nucleosome: role of core histone tail domains in the binding process. Biochemistry 40: 11578-11585. doi: 10.1021/bi010731r
    [137] 12. Mir MA, Dasgupta D (2001) Interaction of antitumor drug, mithramycin, with chromatin. Biochem Biophys Res Commun 280: 68-74. doi: 10.1006/bbrc.2000.4075
    [138] 13. Hagmar P, Pierrou S, Nielsen P, et al. (1992) Ionic strength dependence of the binding of methylene blue to chromatin and calf thymus DNA. J Biomol Struct Dyn 9: 667-679. doi: 10.1080/07391102.1992.10507947
    [139] 14. Mir MA, Das S, Dasgupta D (2004) N-terminal tail domains of core histones in nucleosome block the access of anticancer drugs, mithramycin and daunomycin, to the nucleosomal DNA. Biophys Chem 109: 121-135. doi: 10.1016/j.bpc.2003.10.023
    [140] 15. Hurley LH (2002) DNA and its associated processes as targets forcancer therapy. Nat Rev Cancer 2: 188-200. doi: 10.1038/nrc749
    [141] 17. Veselkov AN, Maleev VYa, Glibin EN, et al. (2003) Structure-activity relation for synthetic phenoxazone drugs.Evidence for a direct correlation between DNA binding and pro-apoptotic activity. Eur J Biochem 270: 4200-4207
    [142] 18. Andersson J, Lincoln P (2011) Stereoselectivity for DNA threading intercalation of short binuclear ruthenium complexes. J Phys Chem B 115: 14768-14775. doi: 10.1021/jp2062767
    [143] 19. Chaurasiya KR, Paramanathan T, McCauley MJ, et al. (2010) Biophysical characterization of DNA binding from single molecule force measurements. Phys Life Rev 7: 299-341.
    [144] 20. Nordell P, Lincoln P (2005) Mechanism of DNA threading intercalation of binuclear Ru complexes: uni- or bimolecular pathways depending on ligand structure and binding density. J Am Chem Soc 127: 9670-9671. doi: 10.1021/ja0521674
    [145] 21. Andersson J, Li M, Lincoln P (2010) AT-specific DNA binding of binuclear ruthenium complexes at the border of threading intercalation. Chemistry 16: 11037-11046.
    [146] 22. Wilhelmsson LM, Lincoln P, Nordґen B (2006) Slow DNA binding. In: Waring M, editor. Sequence-Specific DNA Binding Agents, The Royal Society of Chemistry, Cambridge, 69-95.
    [147] 23. Palchaudhuri R, Hergenrother PJ (2007) DNA as a target for anticancer compounds: methods to determine the mode of binding and the mechanism of action. Curr Opin Biotechnol 18: 497-503. doi: 10.1016/j.copbio.2007.09.006
    [148] 24. Barton TF, Cooney RP, Denny WA (1992) Surface-enhanced Raman spectroscopic study of amsacrine and amsacrine-DNA interactions. J Raman Spectrosc 23: 341-345.
    [149] 25. Rodger A, Blagbrough IS, Adlam G, et al. (1994) DNA binding of a spermine derivative: Spectroscopic study of anthracene-9-carbonyl-n1-spermine with poly[d(G-C)·(d(G-C))] and poly[d(A-T) · d(A-T)]. Biopolymers 34: 1583-1593. doi: 10.1002/bip.360341203
    [150] 26. Hackl EV, Galkin VL, Blagoi YP (2004) DNA interaction with biologically active divalent metal ions: binding constants calculation. Int J Biol Macromol 34: 303-308.
    [151] 27. Evstigneev MP, Mykhina YV, Davies DB (2005) Complexation of daunomycin with a DNA oligomer in the presence of an aromatic vitamin (B2) determined by NMR spectroscopy. Biophys Chem 118: 118-127. doi: 10.1016/j.bpc.2005.08.007
    [152] 28. Hackl EV, Blagoi YP (2005) The effect of temperature on DNA structural transitions under the action of Cu2+ and Ca2+ ions in aqueous solutions. Biopolymers 77: 315-324. doi: 10.1002/bip.20225
    [153] 29. Kruglova EB, Gladkovskaia NA, Maleev V (2005) The use of the spectrophotometric analysis for the calculation of the thermodynamic parameters in actinocin derivative-DNA systems. Biofizika 50: 253-264.
    [154] 30. Evstigneev MP, Baranovskii SF, Rybakova KA, et al. (2006) 1H NMR study of the complexation of the quinolone antibiotic norfloxacin with DNA. Mol Biol (Mosk) 40: 894-899.
    [155] 31. Evstigneev MP, Rybakova KA, Davies DB (2006) Complexation of norfloxacin with DNA in the presence of caffeine. Biophys Chem 121: 84-95. doi: 10.1016/j.bpc.2005.12.003
    [156] 32. Williams AK, Dasilva SC, Bhatta A, et al. (2012) Determination of the drug-DNA binding modes using fluorescence-based assays. Anal Biochem 422: 66-73. doi: 10.1016/j.ab.2011.12.041
    [157] 33. Anupama B, Sunita M, Shiva LD, et al. (2014) Synthesis, spectral characterization, DNA binding studies and antimicrobial activity of Co(II), Ni(II), Zn(II), Fe(III) and VO(IV) complexes with 4-aminoantipyrine Schiff base of ortho-vanillin. J Fluoresc 24: 1067-1076. doi: 10.1007/s10895-014-1386-z
    [158] 34. Zasedatelev AS, Gurskii GV, Vol'kenshtein MV (1971) Theory of one-dimensional adsorption. I. Adsorption of small molecules on a homopolymer. Molecular biology 5: 194-198.
    [159] 35. McGhee JD, von Hippel PH (1974) Theoretical aspects of DNA-protein interactions: co-operative and non-co-operative binding of large ligands to a one-dimensional homogeneous lattice. J Mol Biol 86: 469-489. doi: 10.1016/0022-2836(74)90031-X
    [160] 36. Schellman JA (1974) Cooperative Multisite Binding to DNA. Israel Journal of Chemistry 12: 219-238. doi: 10.1002/ijch.197400021
    [161] 37. Nechipurenko YD, Gursky GV (1986) Cooperative effects on binding of proteins to DNA. Biophys Chem 24: 195-209. doi: 10.1016/0301-4622(86)85025-6
    [162] 38. Lando DY, Teif VB (2000) Long-range interactions between ligands bound to a DNA molecule give rise to adsorption with the character of phase transition of the first kind. J Biomol Struct Dyn 17: 903-911. doi: 10.1080/07391102.2000.10506578
    [163] 39. Teif VB, Rippe K (2010) Statistical-mechanical lattice models for protein-DNA binding in chromatin. J Phys Condens Matter 22: 414105. doi: 10.1088/0953-8984/22/41/414105
    [164] 40. Breslauer KJ, Freire E, Straume M (1992) Calorimetry: a tool for DNA and ligand-DNA studies. Methods Enzymol 211: 533-567.
    [165] 41. Doyle ML (1997) Characterization of binding interactions by isothermal titration calorimetry. Curr Opin Biotechnol 8: 31-35. doi: 10.1016/S0958-1669(97)80154-1
    [166] 42. Jelesarov I, Bosshard HR (1999) Isothermal titration calorimetry and differential scanning calorimetry as complementary tools to investigate the energetics of biomolecular recognition. J Mol Recognit 12: 3-18. doi: 10.1002/(SICI)1099-1352(199901/02)12:1<3::AID-JMR441>3.0.CO;2-6
    [167] 43. Haq I, Chowdhry BZ, Jenkins TC (2001)Calorimetric techniques in the study of high-order DNA-drug interactions. Methods Enzymol 340: 109-149.
    [168] 44. Thomson JA, Ladbury JE (2004) Isothermal titration calorimetry: a tutorial. In Ladbury JE, Doyle ML, editors. Biocalorimetry 2. Applications of Calorimetry in the Biological Sciences, Chichester: John Wiley & Sons, 35-58.
    [169] 45. Holdgate GA, Ward WH (2005) Measurements of binding thermodynamics in drug discovery. Drug Discov Today 10: 1543-1550.
    [170] 46. Freyer MW, Lewis EA (2008) Isothermal titration calorimetry: experimental design, data analysis, and probing macromolecule/ligand binding and kinetic interactions. Methods Cell Biol 84: 79-113. doi: 10.1016/S0091-679X(07)84004-0
    [171] 47. Bhadra K, Maiti M, Kumar GS (2008) Berberine-DNA complexation: New insights into the cooperative binding and energetic aspects. Biochimica et Biophysica Acta 1780: 1054-1061. doi: 10.1016/j.bbagen.2008.05.005
    [172] 48. Hossain M, Kumar GS (2009) DNA intercalation of methylene blue and quinacrine: new insights into base and sequence specificity from structural and thermodynamic studies with polynucleotides. Mol Biosyst 5: 1311-1322.
    [173] 49. Crane-Robinson C, Dragan AI, Read CM (2009) Defining the thermodynamics of protein/DNA complexes and their components using micro-calorimetry. Methods Mol Biol 543: 625-651. doi: 10.1007/978-1-60327-015-1_37
    [174] 50. Kabir A, Kumar GS (2013) Binding of the biogenic polyamines to deoxyribonucleic acids of varying base composition: base specificity and the associated energetics of the interaction. PLoS One 8: e70510. doi: 10.1371/journal.pone.0070510
    [175] 51. Kumar S, Spano MN, Arya DP (2014) Shape readout of AT-rich DNA by carbohydrates. Biopolymers 101: 720-732. doi: 10.1002/bip.22448
    [176] 52. Basu A, Kumar GS (2015) Thermodynamic characterization of proflavine-DNA binding through microcalorimetric studies. J Chem Thermodyn 87: 1-7. doi: 10.1016/j.jct.2015.03.009
    [177] 53. Basu A, Kumar GS (2015) Studies on the interaction of the food colorant tartrazine with double stranded deoxyribonucleic acid. J Biomol Struct Dyn 10: 1-8.
    [178] 54. Chaires JB (1997) Possible origin of differences between van't Hoff and calorimetric enthalpy estimates. Biophys Chem 64: 15-23.
    [179] 55. Chaires JB (2008) Calorimetry and thermodynamics in drug design. Annu Rev Biophys 37: 135-151.
    [180] 56. Janjua NK, Siddiqa A, Yaqub A, et al. (2009) Spectrophotometric analysis of flavonoid-DNA binding interactions at physiological conditions. Spectrochim Acta A Mol Biomol Spectrosc 74: 1135-1137. doi: 10.1016/j.saa.2009.09.022
    [181] 57. Temerk YM, Ibrahim MS, Kotb M (2009) Voltammetric and spectroscopic studies on binding of antitumor Morin, Morin-Cu complex and Morin-beta-cyclodextrin with DNA. Spectrochim Acta A Mol Biomol Spectrosc 71: 1830-1836. doi: 10.1016/j.saa.2008.07.001
    [182] 58. Baranovskii SF, Chernyshev DN, Buchel’nikov AS, et al. (2011) Thermodynamic analysis of complex formation of ethidium bromide with DNA in water solutions. Biophysics 56: 214-219. doi: 10.1134/S0006350911020023
    [183] 59. Chaires JB (1997) Energetics of drug-DNA interactions. Biopolymers 44: 201-215.
    [184] 60. Ren J, Jenkins TC, Chaires JB (2000) Energetics of DNA intercalation reactions. Biochemistry 39: 8439-8447.
    [185] 61. Davies DB, Veselkov AN (1996) Structural and thermodynamical analysis of molecular complexation by 1H NMR spectroscopy. Intercalation of ethidium bromide with the isomeric deoxytetranucleoside triphosphates 5’-d(GpCpGpC) and 5’-d(CpGpCpG) in aqueous solution. J Chem Soc Faraday Trans 92: 3545-3557.
    [186] 62. Kostjukov VV, Pahomov VI, Andrejuk DD, et al. (2007) Investigation of the complexation of the anti-cancer drug novantrone with the hairpin structure of the deoxyheptanucleotide 5′-d(GpCpGpApApGpC). J Mol Struct 843: 78-86. doi: 10.1016/j.molstruc.2006.12.036
    [187] 63. Wartell RM, Benight AS (1985) Thermal denaturation of DNA molecules: A comparison of theory with experiment. Phys Rep 126: 67-107. doi: 10.1016/0370-1573(85)90060-2
    [188] 64. Rice SA, Doty P (1957) The Thermal Denaturation of Desoxyribose Nucleic Acid. J Am Chem Soc 79: 3937-3947. doi: 10.1021/ja01572a001
    [189] 65. Guedin A, Lacroix L, Mergny JL (2010) Thermal melting studies of ligand DNA interactions. Methods Mol Biol 613: 25-35. doi: 10.1007/978-1-60327-418-0_2
    [190] 66. Goldstein G, Stern KG (1950) Experiments on the sonic, thermal, and enzymic depolymerization of desoxyribosenucleic acid. J Struc Chem 5: 687-708.
    [191] 67. Thomas R (1954) Recherches sur la d'enaturation des acides desoxyribonucléiques. Biochimica et Biophysica Acta 14: 231-240. doi: 10.1016/0006-3002(54)90163-8
    [192] 68. Frank-Kamenetskii M (1965) Theory of the helix-coil transition for deoxyribonucleic acids with additional connections between the chains. Vysokomolekulyarnye Soedineniya 7: 354-361.
    [193] 69. Frank-Kamenetskii M (1968) Consideration of helix-coil transition in homopolymers by the most probable distribution method. Mol Biol 2: 408-419.
    [194] 70. Stewart CR (1968) Broadening by acridine orange of the thermal transition of DNA. Biopolymers 6: 1737-1743. doi: 10.1002/bip.1968.360061208
    [195] 71. Lazurkin YS, Frank-Kamenetskii MD, Trifonov EN (1970) Melting of DNA: its study and application as a research method. Biopolymers 9: 1253-1306. doi: 10.1002/bip.1970.360091102
    [196] 72. Barcelo F, Capo D, Portugal J (2002) Thermodynamic characterization of the multivalent binding of chartreusin to DNA. Nucleic Acids Res 30: 4567-4573. doi: 10.1093/nar/gkf558
    [197] 73. Zhong W, Yu JS, Liang Y (2003) Chlorobenzylidine-herring sperm DNA interaction: binding mode and thermodynamic studies. Spectrochim Acta A Mol Biomol Spectrosc 59: 1281-1288. doi: 10.1016/S1386-1425(02)00301-3
    [198] 74. Vardevanyan PO, Antonyan AP, Hambardzumyan LA, et al. (2013) Thermodynamic analysis of DNA complexes with methylene blue, ethidium bromide and Hoechst 33258. Biopolym. Cell 29: 515-520.
    [199] 75. Hajian R, Guan Huat T (2013) Spectrophotometric Studies on the Thermodynamics of the ds-DNA Interaction with Irinotecan for a Better Understanding of Anticancer Drug-DNA Interactions. J Spectrosc 2013: 1-8.
    [200] 76. Cooper A, Johnson CM (1994) Introduction to microcalorimetry and biomolecular energetics. Methods Mol Biol 22: 109-24.
    [201] 77. Rosgen J, Hinz HJ (1999) Theory and practice of DSC mesuarements on proteins. In: Kemp RB, editor. Handbook of Thermal Analysis and Calorimetry, Vol.4, From Macromolecules to Man, Amsterdam: Elsevier, 63-108.
    [202] 78. Bruylants G, Wouters J, Michaux C (2005) Differential scanning calorimetry in life science: thermodynamics, stability, molecular recognition and application in drug design. Curr Med Chem 12: 2011-. doi: 10.2174/0929867054546564
    [203] 79. Spink CH (2008) Differential scanning calorimetry. Methods Cell Biol 84: 115-141. doi: 10.1016/S0091-679X(07)84005-2
    [204] 80. Bereznyak EG, Gladkovskaya NA, Khrebtova AS, et al. (2009) Peculiarities of DNA-proflavine binding under different concentration ratios. Biophysics 54: 574-580. doi: 10.1134/S0006350909050030
    [205] 81. Garbett N (2011) The Use of Calorimetry to Study Ligand-DNA Interactions. In: Aldrich-Wright J, editor. Metallointercalators, Vienna: Springer, 299-324.
    [206] 82. Ising E (1925) Beitrag zur Theorie des Ferromagnetismus. Zeitschrift für Physik 31: 253-258. doi: 10.1007/BF02980577
    [207] 83. Poland DC, Scheraga HA (1970) The theory of helix coil transition, New York: Academic Press.
    [208] 84. Peyrard M, Bishop AR (1989) Statistical mechanics of a nonlinear model for DNA denaturation. Phys Rev Lett 62: 2755-2758.
    [209] 85. Dauxois T, Peyrard M, Bishop AR (1993) Entropy-driven DNA denaturation. Physical Review E 47: R44-R47.
    [210] 86. Dauxois T, Peyrard M, Bishop AR (1993) Dynamics and thermodynamics of a nonlinear model for DNA denaturation. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 47: 684-695.
    [211] 87. Grosberg AIU, Khokhlov AR (1994) Statistical physics of macromolecules, New York: AIP Press.
    [212] 88. Frank-Kamenetskii MD, Prakash S (2014) Fluctuations in the DNA double helix: A critical review. Phys Life Rev 11: 153-170.
    [213] 89. Cantor CR, Schimmel PR (1980) Biophysical chemistry. 3. The behavior of biological macromolecules, San Francisco, Freeman.
    [214] 90. Zimm BH, Bragg JK (1959) Theory of the Phase Transition between Helix and Random Coil in Polypeptide Chains. J Chem Phys 31: 526-535.
    [215] 91. Crothers DM (1971) Statistical thermodynamics of nucleic acid melting transitions with coupled binding equilibria. Biopolymers 10: 2147-2160.
    [216] 92. McGhee JD (1976) Theoretical calculations of the helix-coil transition of DNA in the presence of large, cooperatively binding ligands. Biopolymers 15: 1345-1375.
    [217] 93. Akhrem AA, Fridman AS, Lando D (1985) Theory of helix-coil transition of the heterogeneous DNA-heteroqeneous ligands complexes. Biopolym Cell 1: 171-179.
    [218] 94. Lando D (1994) A theoretical consideration of the influence of selective binding of small ligands on DNA helix-coil transition. J Biomol Struct Dyn 12: 343-354. doi: 10.1080/07391102.1994.10508744
    [219] 95. Akhrem AA, Lando D (1979) Influence of ligands characteristic of selective binding to a certain type of base pairs on DNA helix-coil transition I. Model. Theory. Mol Biol (Mosk) 13: 1098-1109.
    [220] 96. Akhrem AA, Lando D, Shpakovskii AG, et al. (1990) The effect of long-range interactions between adsorbed ligands on the DNA helix-coil transition. Mol Biol (Mosk) 24: 649-656.
    [221] 97. Lando D, Ivanova MA, Akhrem AA (1980) Effect of changes in the stoichiometry of DNA-ligand complexes during heat denaturation of DNA on helix-coil transition parameters. Mol Biol (Mosk) 14: 1281-1288.
    [222] 98. Karapetian AT, Mehrabian NM, Terzikian GA, et al. (1996) Theoretical treatment of melting of complexes of DNA with ligands having several types of binding sites on helical and single-stranded DNA. J Biomol Struct Dyn 14: 275-283. doi: 10.1080/07391102.1996.10508118
    [223] 99. Plum GE, Bloomfield VA (1990) Structural and electrostatic effects on binding of trivalent cations to double-stranded and single-stranded poly[d (AT)]. Biopolymers 29: 13-27. doi: 10.1002/bip.360290105
    [224] 100. Spink CH, Chaires JB (1997) Thermodynamics of the Binding of a Cationic Lipid to DNA. J Am Chem Soc 119: 10920-10928. doi: 10.1021/ja964324s
    [225] 101. Leng F, Chaires JB, Waring MJ (2003) Energetics of echinomycin binding to DNA. Nucleic Acids Res 31: 6191-6197. doi: 10.1093/nar/gkg826
    [226] 102. Pasic L, Sepcic K, Turk T, et al. (2001) Characterization of parazoanthoxanthin A binding to a series of natural and synthetic host DNA duplexes. Arch Biochem Biophys 393: 132-142. doi: 10.1006/abbi.2001.2469
    [227] 103. Portugal J, Cashman DJ, Trent JO, et al. (2005) A new bisintercalating anthracycline with picomolar DNA binding affinity. J Med Chem 48: 8209-8219. doi: 10.1021/jm050902g
    [228] 104. Liu Y-J, Wei X, Mei W-J, et al. (2007) Synthesis, characterization and DNA binding studies of ruthenium(II) complexes: [Ru(bpy)2(dtmi)]2+ and [Ru(bpy)2(dtni)]2+. Transit Metal Chem 32: 762-768. doi: 10.1007/s11243-007-0246-y
    [229] 105. Peng B, Chen X, Du KJ, et al. (2009) Synthesis, characterization and DNA-binding studies of ruthenium(II) mixed-ligand complexes containing dipyrido[1,2,5]oxadiazolo[3,4-b]quinoxaline. Spectrochim Acta A Mol Biomol Spectrosc 74: 896-901. doi: 10.1016/j.saa.2009.08.031
    [230] 106. Barcelo F, Portugal J (2004) Elsamicin A binding to DNA. A comparative thermodynamic characterization. FEBS Lett 576: 68-72.
    [231] 107. Barcelo F, Scotta C, Ortiz-Lombardia M, et al. (2007) Entropically-driven binding of mithramycin in the minor groove of C/G-rich DNA sequences. Nucleic Acids Res 35: 2215-2226. doi: 10.1093/nar/gkm037
    [232] 108. Marky LA, Blumenfeld KS, Breslauer KJ (1983) Calorimetric and spectroscopic investigation of drug-DNA interactions. I. The binding of netropsin to poly d(AT). Nucleic Acids Res 11: 2857-2870.
    [233] 109. Remeta DP, Mudd CP, Berger RL, et al (1993) Thermodynamic characterization of daunomycin-DNA interactions: comparison of complete binding profiles for a series of DNA host duplexes. Biochemistry 32: 5064-5073. doi: 10.1021/bi00070a014
    [234] 110. Brandts JF, Lin LN (1990) Study of strong to ultratight protein interactions using differential scanning calorimetry. Biochemistry 29: 6927-6940.
    [235] 111. Barone G, Catanzano F, Del Vecchio P, et al. (1995) Differential scanning calorimetry as a tool to study protein-ligand interactions. Pure Appl Chem 67: 1867-1872.
    [236] 112. Dassie SA, Celej MS, Fidelio GD (2005) Protein Unfolding Coupled to Ligand Binding: Differential Scanning Calorimetry Simulation Approach. J Chem Educ 82: 85. doi: 10.1021/ed082p85
    [237] 113. Celej MS, Dassie SA, Gonzalez M, et al. (2006) Differential scanning calorimetry as a tool to estimate binding parameters in multiligand binding proteins. Anal Biochem 350: 277-284. doi: 10.1016/j.ab.2005.12.029
    [238] 114. Esposito D, Del Vecchio P, Barone G (2001) A thermodynamic study of herring protamine-DNA complex by differential scanning calorimetry. Phys Chem Chem Phys 3: 5320-5325. doi: 10.1039/b107218h
    [239] 115. Dukhopelnikov EV, Bereznyak EG, Khrebtova AS, et al. (2013) Determination of ligand to DNA binding parameters from two-dimensional DSC curves. J Therm Anal Calorim 111: 1817-1827. doi: 10.1007/s10973-012-2561-6
    [240] 116. Straume M, Freire E (1992) Two-dimensional differential scanning calorimetry: Simultaneous resolution of intrinsic protein structural energetics and ligand binding interactions by global linkage analysis. Anal Biochem 203: 259-268. doi: 10.1016/0003-2697(92)90311-T
    [241] 117. Freire E (1994) Statistical thermodynamic analysis of differential scanning calorimetry data: structural deconvolution of heat capacity function of proteins. Methods Enzymol 240: 502-530. doi: 10.1016/S0076-6879(94)40062-8
    [242] 118. Freire E (1995) Differential scanning calorimetry. Methods Mol Biol 40: 191-218.
    [243] 119. Marky LA, Breslauer KJ (1987) Calculating thermodynamic data for transitions of any molecularity from equilibrium melting curves. Biopolymers 26: 1601-1620. doi: 10.1002/bip.360260911
    [244] 120. Sturtevant JM (1987) Biochemical Applications of Differential Scanning Calorimetry. Annu Rev Phys Chem 38: 463-488. doi: 10.1146/annurev.pc.38.100187.002335
    [245] 121. Kawai Y (1999) Thermal transition profiles of bacteriophage T4 and its DNA. J Gen Appl Microbiol 45: 135-138. doi: 10.2323/jgam.45.135
    [246] 122. Tostesen E, Sandve GK, Liu F, et al. (2009) Segmentation of DNA sequences into twostate regions and melting fork regions. J Phys Condens Matter 21: 034109. doi: 10.1088/0953-8984/21/3/034109
    [247] 123. Duguid JG, Bloomfield VA, Benevides JM, et al. (1996) DNA melting investigated by differential scanning calorimetry and Raman spectroscopy. Biophys J 71: 3350-3360.
    [248] 124. Movileanu L, Benevides JM, Thomas GJ (2002) Determination of base and backbone contributions to the thermodynamics of premelting and melting transitions in B DNA. Nucleic Acids Res 30: 3767-3777. doi: 10.1093/nar/gkf471
    [249] 125. Dukhopelnikov EV (2014) Modeling of heat absorption curves for ligand-competitor-DNA triple system. Biophysical Bulletin 31: 49-58.
  • Reader Comments
  • © 2015 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(6987) PDF downloads(1477) Cited by(8)

Article outline

Figures and Tables

Figures(1)

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog