Theoretical study of the partial molar volume change associated with the pressure‐induced structural transition of ubiquitin

The partial molar volume (PMV) change associated with the pressure‐induced structural transition of ubiquitin is analyzed by the three‐dimensional reference interaction site model (3D‐RISM) theory of molecular solvation. The theory predicts that the PMV decreases upon the structural transition, which is consistent with the experimental observation. The volume decomposition analysis demonstrates that the PMV reduction is primarily caused by the decrease in the volume of structural voids in the protein, which is partially canceled by the volume expansion due to the hydration effects. It is found from further analysis that the PMV reduction is ascribed substantially to the penetration of water molecules into a specific part of the protein. Based on the thermodynamic relation, this result implies that the water penetration causes the pressure‐induced structural transition. It supports the water penetration model of pressure denaturation of proteins proposed earlier.

[1]  M. Paulaitis,et al.  Pressure denaturation of staphylococcal nuclease studied by neutron small-angle scattering and molecular simulation. , 2004, Biophysical journal.

[2]  G. Hummer,et al.  The pressure dependence of hydrophobic interactions is consistent with the observed pressure denaturation of proteins. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[3]  K Schulten,et al.  VMD: visual molecular dynamics. , 1996, Journal of molecular graphics.

[4]  B. Montgomery Pettitt,et al.  A dielectrically consistent interaction site theory for solvent—electrolyte mixtures , 1992 .

[5]  T. Chalikian,et al.  On volume changes accompanying conformational transitions of biopolymers. , 1998, Biopolymers.

[6]  Kazuyuki Akasaka,et al.  Pressure-dependent changes in the solution structure of hen egg-white lysozyme. , 2003, Journal of molecular biology.

[7]  Fumio Hirata,et al.  Potentials of mean force of simple ions in ambient aqueous solution. I. Three-dimensional reference interaction site model approach , 2000 .

[8]  C. Dobson,et al.  Protein unfolding, amyloid fibril formation and configurational energy landscapes under high pressure conditions. , 2006, Chemical Society reviews.

[9]  P. Kollman,et al.  How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? , 2000 .

[10]  Kazuyuki Akasaka,et al.  The solution structure of bovine pancreatic trypsin inhibitor at high pressure , 2003, Protein science : a publication of the Protein Society.

[11]  Yuichi Harano,et al.  Theoretical study for partial molar volume of amino acids and polypeptides by the three-dimensional reference interaction site model , 2001 .

[12]  Percy Williams Bridgman,et al.  THE COAGULATION OF ALBUMEN BY PRESSURE , 1914 .

[13]  Herbert Edelsbrunner,et al.  Measuring proteins and voids in proteins , 1995, Proceedings of the Twenty-Eighth Annual Hawaii International Conference on System Sciences.

[14]  T. Straatsma,et al.  THE MISSING TERM IN EFFECTIVE PAIR POTENTIALS , 1987 .

[15]  F. Millero.  Molal volumes of electrolytes , 1971 .

[16]  Yuichi Harano,et al.  Crucial importance of translational entropy of water in pressure denaturation of proteins. , 2006, The Journal of chemical physics.

[17]  B. Lee.  Partial molar volume from the hard-sphere mixture model , 1983 .

[18]  R. Mazo,et al.  On the Statistical Mechanical Theory of Solutions , 1958 .

[19]  F. Hirata,et al.  Theoretical study of volume changes accompanying xenon-lysozyme binding: implications for the molecular mechanism of pressure reversal of anesthesia. , 2006, The journal of physical chemistry. B.

[20]  W. Kauzmann.  Some factors in the interpretation of protein denaturation. , 1959, Advances in protein chemistry.

[21]  F. Hirata,et al.  Three-dimensional density profiles of water in contact with a solute of arbitrary shape: a RISM approach , 1998 .

[22]  C. Royer.  Revisiting volume changes in pressure-induced protein unfolding. , 2002, Biochimica et biophysica acta.

[23]  P. Masson,et al.  High pressure effects on biological macromolecules: from structural changes to alteration of cellular processes. , 2002, Biochimica et biophysica acta.

[24]  Benoît Roux,et al.  An Integral Equation To Describe the Solvation of Polar Molecules in Liquid Water , 1997 .

[25]  C. Balny.  What lies in the future of high-pressure bioscience? , 2006, Biochimica et biophysica acta.

[26]  Fumio Hirata,et al.  Partial molar volume of proteins studied by the three-dimensional reference interaction site model theory. , 2005, The journal of physical chemistry. B.

[27]  Fumio Hirata,et al.  Locating missing water molecules in protein cavities by the three‐dimensional reference interaction site model theory of molecular solvation , 2006, Proteins.

[28]  F. Hirata,et al.  Theoretical study of volume changes associated with the helix–coil transition of an alanine‐rich peptide in aqueous solution , 2005, Biopolymers.

[29]  Shigeyuki Yokoyama,et al.  NMR snapshots of a fluctuating protein structure: ubiquitin at 30 bar-3 kbar. , 2005, Journal of molecular biology.

[30]  G. Barbosa‐Cánovas,et al.  Food Processing by High Hydrostatic Pressure , 2002, Critical reviews in food science and nutrition.

[31]  J. Vanderkooi,et al.  Molecular probes: what is the range of their interaction with the environment? , 2004, Biophysical journal.

[32]  Jerson L. Silva,et al.  Pressure stability of proteins. , 1993, Annual review of physical chemistry.

[33]  Andriy Kovalenko,et al.  Three-dimensional Rism Theory for Molecular Liquids and Solid-Liquid Interfaces , 2004 .

[34]  Gerhard Hummer,et al.  Cooperative water filling of a nonpolar protein cavity observed by high-pressure crystallography and simulation. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Fumio Hirata,et al.  Theoretical study of the cosolvent effect on the partial molar volume change of staphylococcal nuclease associated with pressure denaturation. , 2007, The journal of physical chemistry. B.

[36]  H. Yamada,et al.  Two folded conformers of ubiquitin revealed by high-pressure NMR. , 2001, Biochemistry.

[37]  Masahiro Kinoshita,et al.  Theoretical study for partial molar volume of amino acids in aqueous solution: Implication of ideal fluctuation volume , 2000 .

[38]  Fumio Hirata,et al.  Solvation thermodynamics of protein studied by the 3D-RISM theory , 2004 .

[39]  B. Montgomery Pettitt,et al.  Integral equation predictions of liquid state structure for waterlike intermolecular potentials , 1982 .

[40]  F. Hirata,et al.  Theoretical study for volume changes associated with the helix-coil transition of peptides. , 2001, Biopolymers.

[41]  F. Hirata,et al.  Hydrophobic effects on partial molar volume. , 2005, The Journal of chemical physics.

[42]  Junmei Wang,et al.  How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? , 2000, J. Comput. Chem..