Nucleic acid hydration: a volumetric perspective

Physics of Life Reviews

Volumn 4, Issue 2, 2007, Pages 91-115

  Chalikian, Tigran V ^a   Macgregor Jr , Robert B ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Conformational transitions; DNA hydration; Drug binding; Kinetics; Thermodynamics; Volumetric measurements

Indexed keywords

EID: 34250747531     PISSN: 15710645     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plrev.2006.11.001     Document Type: Review

References (134)

1. Tinoco I. Nucleic acid structures, energetics, and dynamics. J Phys Chem 100 (1996) 13311-13322
2. Makhatadze G.I., and Privalov P.L. Energetics of protein structure. Adv Protein Chem 47 (1995) 307-425
3. Muller N. Search for a realistic view of hydrophobic effects. Acc Chem Res 23 (1990) 23-28
4. Halle B. Protein hydration dynamics in solution: a critical survey. Philos Trans Royal Soc London: Series B - Biol Sci 359 (2004) 1207-1223
5. Pal S.K., Peon J., Bagchi B., and Zewail A.H. Biological water: Femtosecond dynamics of macromolecular hydration. J Phys Chem B 106 (2002) 12376-12395
6. Bagchi B. Water dynamics in the hydration layer around proteins and micelles. Chem Rev 105 (2005) 3197-3219
7. Chalikian T.V. Structural thermodynamics of hydration. J Phys Chem B 105 (2001) 12566-12578
8. Drew H.R., and Dickerson R.E. Structure of a B-DNA dodecamer. 3. Geometry of hydration. J Mol Biol 151 (1981) 535-556
9. Denisov V.P., Carlstrom G., Venu K., and Halle B. Kinetics of DNA hydration. J Mol Biol 268 (1997) 118-136
10. Egli M., Tereshko V., Teplova M., Minasov G., Joachimiak A., Sanishvili R., Weeks C.M., Miller R., Maier M.A., An H., Dan C.P., and Manoharan M. X-ray crystallographic analysis of the hydration of A- and B-form DNA at atomic resolution. Biopolymers 48 (1998) 234-252
11. Parsegian V.A., Rand R.P., and Rau D.C. Macromolecules and water: probing with osmotic stress. Methods Enzymol 259 (1995) 43-94
12. Svergun D.I., Richard S., Koch M.H.J., Sayers Z., Kuprin S., and Zaccai G. Protein hydration in solution: experimental observation by X-ray and neutron scattering. Proc Natl Acad Sci USA 95 (1998) 2267-2272
13. Savage H., and Wlodawer A. Determination of water-structure around biomolecules using X-ray and neutron-diffraction methods. Methods Enzymol 127 (1986) 162-183
14. Perkins S.J. X-ray and neutron scattering analyses of hydration shells: a molecular interpretation based on sequence predictions and modeling fits. Biophys Chem 93 (2001) 129-139
15. Belton P.S. Nuclear magnetic resonance studies of the hydration of proteins and DNA. Cell Mol Life Sci 57 (2000) 993-998
16. Chalikian T.V., and Breslauer K.J. Thermodynamic analysis of biomolecules: a volumetric approach. Curr Opin Struct Biol 8 (1998) 657-664
17. Chalikian T.V., and Breslauer K.J. Volumetric properties of nucleic acids. Biopolymers 48 (1998) 264-280
18. Chalikian T.V. Volumetric properties of proteins. Annu Rev Biophys Biomol Struct 32 (2003) 207-235
19. Chalikian T.V., Sarvazyan A.P., and Breslauer K.J. Hydration and partial compressibility of biological compounds. Biophys Chem 51 (1994) 89-107
20. Elcock A.H., and Mccammon J.A. Sequence-dependent hydration of DNA-theoretical results. J Am Chem Soc 117 (1995) 10161-10162
21. Feig M., and Pettitt B.M. A molecular simulation picture of DNA hydration around A- and B-DNA. Biopolymers 48 (1998) 199-209
22. Feig M., and Pettitt B.M. Modeling high-resolution hydration patterns in correlation with DNA sequence and conformation. J Mol Biol 286 (1999) 1075-1095
23. Makarov V., Pettitt B.M., and Feig M. Solvation and hydration of proteins and nucleic acids: a theoretical view of simulation and experiment. Acc Chem Res 35 (2002) 376-384
24. Imai T., Kovalenko A., and Hirata F. Partial molar volume of proteins studied by the three-dimensional reference interaction site model theory. J Phys Chem B 109 (2005) 6658-6665
25. Imai T., and Hirata F. Hydrophobic effects on partial molar volume. J Chem Phys 122 (2005) 094509
26. Lockwood D.M., and Rossky P.J. Evaluation of functional group contributions to excess volumetric properties of solvated molecules. J Phys Chem B 103 (1999) 1982-1990
27. Lockwood D.M., Rossky P.J., and Levy R.M. Functional group contributions to partial molar compressibilities of alcohols in water. J Phys Chem B 104 (2000) 4210-4217
28. Matubayasi N., and Levy R.M. Thermodynamics of the hydration shell. 2. Excess volume and compressibility of a hydrophobic solute. J Phys Chem 100 (1996) 2681-2688
29. Macgregor Jr. R.B. Effect of hydrostatic pressure on nucleic acids. Biopolymers 48 (1998) 253-263
30. Macgregor Jr. R.B. The interactions of nucleic acids at elevated hydrostatic pressure. Biochim Biophys Acta 1595 (2002) 266-276
31. Barciszewski J., Jurczak J., Porowski S., Specht T., and Erdmann V.A. The role of water structure in conformational changes of nucleic acids in ambient and high-pressure conditions. Eur J Biochem 260 (1999) 293-307
32. Pal S.K., Zhao L.A., and Zewail A.H. Water at DNA surfaces: ultrafast dynamics in minor groove recognition. Proc Natl Acad Sci USA 100 (2003) 8113-8118
33. Chalikian T.V., Plum G.E., Sarvazyan A.P., and Breslauer K.J. Influence of drug binding on DNA hydration: acoustic and densimetric characterizations of netropsin binding to the poly(dAdT)poly(dAdT) and poly(dA)poly(dT) duplexes and the poly(dT)poly(dA)poly(dT) triplex at 25 °C. Biochemistry 33 (2004) 8629-8640
34. Filfil R., and Chalikian T.V. The thermodynamics of protein-protein recognition as characterized by a combination of volumetric and calorimetric techniques: the binding of turkey ovomucoid third domain to α-chymotrypsin. J Mol Biol 326 (2003) 1271-1288
35. Phan A.T., Leroy J.L., and Gueron M. Determination of the residence time of water molecules hydrating B′-DNA and B-DNA by one-dimensional zero-enhancement nuclear Overhauser effect spectroscopy. J Mol Biol 286 (1999) 505-519
36. Scheraga H.A. Interactions in aqueous-solution. Acc Chem Res 12 (1979) 7-14
37. Cho C.H., Singh S., and Robinson G.W. An explanation of the density maximum in water. Phys Rev Lett 76 (1996) 1651-1654
38. Robinson G.W., Urquidi J., Singh S., and Cho C.H. Protein denaturation described by a two-state structural model of liquid water. Cell Mol Biol 47 (2001) 757-765
39. Hagler A.T., Scheraga H.A., and Nemethy G. Current status of the water-structure problem; application to proteins. Ann NY Acad Sci 204 (1973) 51-78
40. Shimizu S. Estimating hydration changes upon biomolecular reactions from osmotic stress, high pressure, and preferential hydration experiments. Proc Natl Acad Sci USA 101 (2004) 1195-1199
41. Dill K.A., Truskett T.M., Vlachy V., and Hribar-Lee B. Modeling water, the hydrophobic effect, and ion solvation. Annu Rev Biophys Biomol Struct 34 (2005) 173-199
42. Høiland H. Partial molar volumes of biochemical model compounds in aqueous solution. In: Hinz H.-J. (Ed). Thermodynamic data for biochemistry and biotechnology (1986), Springer, Berlin 17-44
43. Høiland H. Partial molar compressibilities of organic solutes in water. In: Hinz H.-J. (Ed). Thermodynamic data for biochemistry and biotechnology (1986), Springer, Berlin 129-147
44. Sarvazyan A.P. Ultrasonic velocimetry of biological compounds. Annu Rev Biophys Biophys Chem 20 (1991) 321-342
45. Kratky O., Leopold H., and Stabinger H. The determination of the partial specific volume of proteins by the mechanical oscillator technique. Methods Enzymol 27 (1973) 98-110
46. Lin L.N., Brandts J.F., Brandts J.M., and Plotnikov V. Determination of the volumetric properties of proteins and other solutes using pressure perturbation calorimetry. Anal Biochem 302 (2002) 144-160
47. Owen B.B., and Simons H.L. Standard partial molal compressibilities by ultrasonics. 1. Sodium chloride and potassium chloride at 25 °C. J Phys Chem 61 (1957) 479-482
48. Sarvazyan A.P. Development of methods of precise ultrasonic measurements in small volumes of liquids. Ultrasonics 20 (1982) 151-154
49. Sarvazyan A.P., and Chalikian T.V. Theoretical analysis of an ultrasonic interferometer for precise measurements at high pressures. Ultrasonics 29 (1991) 119-124
50. Eggers F., and Funck Th. Ultrasonic measurements with milliliter liquid samples in 0.5-100 MHz range. Rev Sci Instrum 44 (1973) 969-977
51. Eggers F., and Kaatze U. Broad-band ultrasonic measurement techniques for liquids. Meas Sci Technol 7 (1996) 1-19
52. Zamyatnin A.A. Amino acid, peptide, and protein volume in solution. Annu Rev Biophys Bioeng 13 (1984) 145-165
53. Edward J.T., and Farrell P.G. Relation between van der Waals and partial molal volumes of organic molecules in water. Can J Chem 53 (1975) 2965-2970
54. Kharakoz D.P. Volumetric properties of proteins and their analogs in diluted water solutions. 1. Partial volumes of amino acids at 15-55 °C. Biophys Chem 34 (1989) 115-125
55. Kharakoz D.P. Partial molar volumes of molecules of arbitrary shape and the effect of hydrogen bonding with water. J Solution Chem 21 (1992) 569-595
56. Bano M., and Marek J. How thick is the layer of thermal volume surrounding the protein?. Biophys Chem 120 (2006) 44-54
57. Imai T., Harano Y., Kovalenko A., and Hirata F. Theoretical study for volume changes associated with the helix-coil transition of peptides. Biopolymers 59 (2001) 512-519
58. Chalikian T.V., Totrov M., Abagyan R., and Breslauer K.J. The hydration of globular proteins as derived from volume and compressibility measurements: cross correlating thermodynamic and structural data. J Mol Biol 260 (1996) 588-603
59. 2O. J Am Chem Soc 121 (1999) 1156-1163
60. Imai T., Takahiro T., Kovalenko A., Hirata F., Kato M., and Taniguchi Y. Theoretical study of volume changes associated with the helix-coil transition of an alanine-rich peptide in aqueous solution. Biopolymers 79 (2005) 97-105
61. Richards F.M. Areas, volumes, packing, and protein structure. Annu Rev Biophys Bioeng 6 (1977) 151-176
62. Richards F.M. Calculation of molecular volumes and areas for structures of known geometry. Methods Enzymol 115 (1985) 440-464
63. Connolly M.L. Solvent-accessible surfaces of proteins and nucleic acids. Science 221 (1983) 709-713
64. Taulier N., and Chalikian T.V. Compressibility of protein transitions. Biochim Biophys Acta 1595 (2002) 48-70
65. Cooper A. Thermodynamic fluctuations in protein molecules. Proc Natl Acad Sci USA 73 (1976) 2740-2741
66. Cooper A. Protein fluctuations and the thermodynamic uncertainty principle. Prog Biophys Mol Biol 44 (1984) 181-214
67. Eggers F. Ultrasonic velocity and attenuation measurements in liquids with resonators, extending the MHz frequency range. Acustica 76 (1992) 231-240
68. Taulier N., and Chalikian T.V. Hydrophobic hydration in cyclodextrin complexation. J Phys Chem B 110 (2006) 12222-12224
69. Harano Y., Imai T., Kovalenko A., Kinoshita M., and Hirata F. Theoretical study for partial molar volume of amino acids and polypeptides by the three-dimensional reference interaction site model. J Chem Phys 114 (2001) 9506-9511
70. Høiland H., and Holvik H. Partial molal volumes and compressibilities of carbohydrates in water. J Solution Chem 7 (1978) 587-596
71. Galema S.A., and Høiland H. Stereochemical aspects of hydration of carbohydrates in aqueous solutions. 3. Density and ultrasound measurements. J Phys Chem 95 (1991) 5321-5326
72. Buckin V.A. Hydration of nucleic bases in dilute aqueous solutions. Apparent molar adiabatic and isothermal compressibilities, apparent molar volumes and their temperature slopes at 25 °C. Biophys Chem 29 (1988) 283-292
73. Lee A., and Chalikian T.V. Volumetric characterization of the hydration properties of heterocyclic bases and nucleosides. Biophys Chem 92 (2001) 209-227
74. Buckin V.A., Kankiya B.I., and Kazaryan R.L. Hydration of nucleosides in dilute aqueous solutions. Ultrasonic velocity and density measurements. Biophys Chem 34 (1989) 211-223
75. Chalikian T.V. Ultrasonic and densimetric characterizations of the hydration properties of polar groups in monosaccharides. J Phys Chem B 102 (1998) 6921-6926
76. Durshchlag H. Specific volumes of biological macromolecules and some other molecules of biological interest. In: Hinz H.-J. (Ed). Thermodynamic data for biochemistry and biotechnology (1986), Springer, Berlin 45-128
77. Dashnau J.L., Sharp K.A., and Vanderkooi J.M. Carbohydrate intramolecular hydrogen bonding cooperativity and its effect on water structure. J Phys Chem B 109 (2005) 24152-24159
78. Chalikian T.V., Sarvazyan A.P., Plum G.E., and Breslauer K.J. Influence of base composition, base sequence, and duplex structure on DNA hydration: apparent molar volumes and apparent molar adiabatic compressibilities of synthetic and natural DNA duplexes at 25 °C. Biochemistry 33 (1994) 2394-2401
79. Chalikian T.V., Volker J., Srinivasan A.R., Olson W.K., and Breslauer K.J. The hydration of nucleic acid duplexes as assessed by a combination of volumetric and structural techniques. Biopolymers 50 (1999) 459-471
80. Manning G.S. Molecular theory of polyelectrolyte solutions with applications to electrostatic properties of polynucleotides. Q Rev Biophys 11 (1978) 179-246
81. Strauss U.P., Helfgott C., and Pink H. Interactions of polyelectrolytes with simple electrolytes. 2. Donnan equilibria obtained with DNA in solutions of 1-1 electrolytes. J Phys Chem 71 (1967) 2550-2556
82. Record M.T., Anderson C.F., and Lohman T.M. Thermodynamic analysis of ion effects on binding and conformational equilibria of proteins and nucleic acids. Roles of ion association or release, screening, and ion effects on water activity. Q Rev Biophys 11 (1978) 103-178
83. Bond J.P., Anderson C.F., and Record M.T. Conformational transitions of duplex and triplex nucleic acid helices. Thermodynamic analysis of effects of salt concentration on stability using preferential interaction coefficients. Biophys J 67 (1994) 825-836
84. Bloomfield V.A., Crothers D.M., and Tinoco Jr. I. Nucleic acids: Structures, properties, and functions (2000), University Science Books, Sausalito, CA
85. Saenger W., Hunter W.N., and Kennard O. DNA conformation is determined by economics in the hydration of phosphate groups. Nature 324 (1986) 385-388
86. Westhof E. Water: an integral part of nucleic acid structure. Annu Rev Biophys Biophys Chem 17 (1988) 125-144
87. Mikulecky P.J., and Feig A.L. Heat capacity changes associated with nucleic acid folding. Biopolymers 82 (2006) 38-58
88. Tikhomirova A., and Chalikian T.V. Probing hydration of monovalent cations condensed around polymeric nucleic acids. J Mol Biol 341 (2004) 551-563
89. Anderson C.F., and Record M.T. The relationship between the Poisson-Boltzmann model and the condensation hypothesis. An analysis based on the low salt form of the Donnan coefficient. Biophys Chem 11 (1980) 353-360
90. Anderson C.F., and Record M.T. Polyelectrolyte theories and their applications to DNA. Annu Rev Phys Chem 33 (1982) 191-222
91. 12 duplexes. J Mol Biol 305 (2001) 1057-1072
92. Kankia B.I. Interaction of alkaline-earth metal ions with calf thymus DNA. Volume and compressibility effects in diluted aqueous solutions. Biophys Chem 84 (2000) 227-237
93. 2+ binding to synthetic polynucleotides with regularly alternating purine-pyrimidine sequences. Nucl Acids Res 28 (2000) 911-916
94. Kankia B.I. Inner-sphere complexes of divalent cations with single-stranded poly(rA) and poly(rU). Biopolymers 74 (2004) 232-239
95. Wu J.Q., and Macgregor Jr. R.B. Pressure dependence of the melting temperature of dAdT polymers. Biochemistry 32 (1993) 12531-12537
96. Wu J.Q., and Macgregor Jr. R.B. Pressure dependence of the helix-coil transition temperature of poly[d(G-C)]. Biopolymers 35 (1995) 369-376
97. Najaf-Zadeh R., Wu J.Q., and Macgregor Jr. R.B. Effect of cations on the volume of the helix-coil transition of poly[d(A-T)]. Biochim Biophys Acta 1262 (1995) 52-58
98. Nordmeier E. Effects of pressure on the helix coil transition of calf thymus DNA. J Phys Chem 96 (1992) 1494-1501
99. Chalikian T.V., Volker J., Plum G.E., and Breslauer K.J. A more unified picture for the thermodynamics of nucleic acid duplex melting: a characterization by calorimetric and volumetric techniques. Proc Natl Acad Sci USA 96 (1999) 7853-7858
100. Rayan G., and Macgregor R.B. Comparison of the heat- and pressure-induced helix-coil transition of two DNA copolymers. J Phys Chem B 109 (2005) 15558-15565
101. Spink C.H., and Chaires J.B. Effects of hydration, ion release, and excluded volume on the melting of triplex and duplex DNA. Biochemistry 38 (1999) 496-508
102. Reid C., and Rand R.P. Probing protein hydration and conformational states in solution. Biophys J 72 (1997) 1022-1030
103. Filfil R., and Chalikian T.V. Volumetric and spectroscopic characterizations of glucose-hexokinase association. FEBS Lett 554 (2003) 351-356
104. Harries D., Rau D.C., and Parsegian V.A. Solutes probe hydration in specific association of cyclodextrin and adamantane. J Am Chem Soc 12 (2005) 2184-2190
105. Dubins D.N., Lee A., Macgregor Jr. R.B., and Chalikian T.V. On the stability of double stranded nucleic acids. J Am Chem Soc 123 (2001) 9254-9259
106. Privalov P.L. Cold denaturation of proteins. Crit Rev Biochem Mol Biol 25 (1990) 281-305
107. Mikulecky P.J., and Feig A.L. Heat capacity changes associated with DNA duplex formation: salt- and sequence-dependent effects. Biochemistry 45 (2006) 604-616
108. P. J Am Chem Soc 126 (2004) 16387-16394
109. Owczarzy R., You Y., Moreira B.G., Manthey J.A., Huang L., Behlke M.A., and Walder J.A. Effects of sodium ions on DNA duplex oligomers: improved predictions of melting temperatures. Biochemistry 43 (2004) 3537-3554
110. Macgregor Jr. R.B. Chain length and oligonucleotide stability at high pressure. Biopolymers 38 (1996) 321-327
111. Lin M.C., and Macgregor Jr. R.B. Activation volume of DNA duplex formation. Biochemistry 36 (1997) 6539-6544
112. Lin M.C., and Macgregor Jr. R.B. The activation volume of a DNA helix-coil transition. Biochemistry 35 (1996) 11846-11851
113. Lin M.C., and Macgregor Jr. R.B. Pressure-jump relaxation kinetics of a DNA triplex helix-coil equilibrium. Biopolymers 42 (1997) 129-132
114. Dubins D.N., and Macgregor Jr. R.B. Volumetric properties of the formation of double stranded DNA: a nearest-neighbor analysis. Biopolymers 73 (2004) 242-257
115. Lin M.C., Eid P., Wong P.T., and Macgregor Jr. R.B. High pressure Fourier transform infrared spectroscopy of poly(dA)poly(dT), poly(dA) and poly(dT). Biophys Chem 76 (1999) 87-94
116. Cantor C.R., Warshaw M.M., and Shapiro H. Oligonucleotide interactions. 3. Circular dichroism studies of conformation of deoxyoligonucleotides. Biopolymers 9 (1970) 1059-1077
117. Kallansrud G., and Ward B. A comparison of measured and calculated single- and double-stranded oligodeoxynucleotide extinction coefficients. Anal Biochem 236 (1996) 134-138
118. Henderson J.T., Benight A.S., and Hanlon S. A semi-micromethod for the determination of the extinction coefficients of duplex and single-stranded DNA. Anal Biochem 201 (1992) 17-29
119. Cavaluzzi M.J., and Borer P.N. Revised UV extinction coefficients for nucleoside-5′-monophosphates and unpaired DNA and RNA. Nucl Acids Res 32 (2004) e13
120. Breslauer K.J., Frank R., Blocker H., and Marky L.A. Predicting DNA duplex stability from the base sequence. Proc Natl Acad Sci USA 83 (1986) 3746-3750
121. SantaLucia Jr. J., and Hicks D. The thermodynamics of DNA structural motifs. Annu Rev Biophys Biomol Struct 33 (2004) 415-440
122. Vologodskii A.V., Amirikyan B.R., Lyubchenko Y.L., and Frank-Kamenetskii M.D. Allowance for heterogeneous stacking in the DNA helix-coil transition theory. J Biomol Struct Dyn 2 (1984) 131-148
123. Marky L.A., and Macgregor Jr. R.B. Hydration of dAdT polymers: role of water in the thermodynamics of ethidium and propidium intercalation. Biochemistry 29 (1990) 4805-4811
124. Marky L.A., Kupke D.W., and Kankia B.I. Volume changes accompanying interaction of ligands with nucleic acids. Methods Enzymol 340 (2001) 149-165
125. Tang G.Q., Tanaka N., and Kunugi S. Salt effects on fluorescence spectral shifts of DNA-bound Hoechst 33258 and reaction volumes of the minor groove binding. Bull Chem Soc Jpn 72 (1999) 1129-1137
126. Tang G.Q., Tanaka N., and Kunugi S. Effects of pressure on the DNA minor groove binding of Hoechst 33258. Bull Chem Soc Jpn 71 (1998) 1725-1730
127. Han F., and Chalikian T.V. Hydration changes accompanying nucleic acid intercalation reactions: volumetric characterizations. J Am Chem Soc 125 (2003) 7219-7229
128. 2: volumetric, calorimetric, and spectroscopic characterizations. Biochemistry 44 (2005) 9785-9794
129. Shi X.S., and Macgregor R.B. Temperature dependence of the volumetric parameters of drug binding to poly[d(A-T)]poly[d(A-T)] and poly(dA)poly(dT). Biophys J 90 (2006) 1729-1738
130. Breslauer K.J., Remeta D.P., Chou W.Y., Ferrante R., Curry J., Zaunczkowski D., Snyder J.G., and Marky L.A. Enthalpy-entropy compensations in drug-DNA binding studies. Proc Natl Acad Sci USA 84 (1987) 8922-8926
131. Chan S.S., Breslauer K.J., Hogan M.E., Kessler D.J., Austin R.H., Ojemann J., Passner J.M., and Wiles N.C. Physical studies of DNA premelting equilibria in duplexes with and without homo dAdT tracts: correlations with DNA bending. Biochemistry 29 (1990) 6161-6171
132. Herrera J.E., and Chaires J.B. A premelting conformational transition in poly(dA)poly(dT) coupled to daunomycin binding. Biochemistry 28 (1989) 1993-2000
133. Arnott S., Chandrasekaran R., Hall I.H., and Puigjaner L.C. Heteronomous DNA. Nucl Acids Res 11 (1983) 4141-4155
134. Alexeev D.G., Lipanov A.A., and Skuratovskii I.Y. Poly(dA)poly(dT) is a B-type double helix with a distinctively narrow minor groove. Nature 325 (1987) 821-823