Conformational changes of ubiquitin under high pressure conditions: A pressure simulated tempering molecular dynamics study

Molecular dynamics simulations for the system of ubiquitin were performed with pressure simulated tempering to study pressure‐induced conformational changes of ubiquitin. The pressure dependence of ubiquitin was analyzed in a wide range of pressure from atmospheric pressure (0.1 MPa) to 1.0 GPa. The fluctuation of the distance between amino‐acid residues and the distribution of a largely fluctuating distance were calculated. The large fluctuation of the L8‐E34 distance induced by pressure means that the conformation of ubiquitin changes under high pressure conditions. There were more water molecules near the largely fluctuating region at high pressure than at low pressure. The pressure dependence of interaction energies among ubiquitin and water was also calculated to investigate the role of water for the pressure‐induced conformational changes of ubiquitin. The protein–water interaction is important when the conformation of ubiquitin changes at high pressure. © 2017 Wiley Periodicals, Inc.

[1]  Ryan Day,et al.  Water penetration in the low and high pressure native states of ubiquitin , 2008, Proteins.

[2]  K. Lindorff-Larsen,et al.  Atomic-level description of ubiquitin folding , 2013, Proceedings of the National Academy of Sciences.

[3]  S. Grzesiek,et al.  Key stabilizing elements of protein structure identified through pressure and temperature perturbation of its hydrogen bond network. , 2012, Nature chemistry.

[4]  Yuko Okamoto,et al.  Monte Carlo simulations in generalized isobaric-isothermal ensembles. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

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

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

[8]  Y. Engelborghs,et al.  Molecular mechanisms of pressure induced conformational changes in BPTI , 1996, Proteins.

[9]  A Joshua Wand,et al.  Mapping the hydration dynamics of ubiquitin. , 2011, Journal of the American Chemical Society.

[10]  B. Brooks,et al.  Constant pressure molecular dynamics simulation: The Langevin piston method , 1995 .

[11]  N. Metropolis,et al.  Equation of State Calculations by Fast Computing Machines , 1953, Resonance.

[12]  Kazuyuki Akasaka,et al.  Close identity of a pressure-stabilized intermediate with a kinetic intermediate in protein folding , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[13]  C A Royer,et al.  Pressure provides new insights into protein folding, dynamics and structure. , 2001, Trends in biochemical sciences.

[14]  Hoover,et al.  Canonical dynamics: Equilibrium phase-space distributions. , 1985, Physical review. A, General physics.

[15]  Hisashi Okumura,et al.  Temperature and pressure denaturation of chignolin: Folding and unfolding simulation by multibaric‐multithermal molecular dynamics method , 2012, Proteins.

[16]  G. Parisi,et al.  Simulated tempering: a new Monte Carlo scheme , 1992, hep-lat/9205018.

[17]  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.

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

[19]  Michael R. Shirts,et al.  Statistically optimal analysis of samples from multiple equilibrium states. , 2008, The Journal of chemical physics.

[20]  W. Delano.  The PyMOL Molecular Graphics System , 2002 .

[21]  Yuji Sugita,et al.  Dynamic correlation between pressure-induced protein structural transition and water penetration. , 2010, The journal of physical chemistry. B.

[22]  Yuko Okamoto,et al.  Replica-exchange Monte Carlo method for the isobaric isothermal ensemble , 2001 .

[23]  K. Hukushima,et al.  Exchange Monte Carlo Method and Application to Spin Glass Simulations , 1995, cond-mat/9512035.

[24]  A. Garcia,et al.  Reversible temperature and pressure denaturation of a protein fragment: a replica exchange molecular dynamics simulation study. , 2004, Physical review letters.

[25]  W. L. Jorgensen,et al.  Comparison of simple potential functions for simulating liquid water , 1983 .

[26]  H. Okumura,et al.  Monte Carlo simulations in multibaric–multithermal ensemble , 2004 .

[27]  Yuko Okamoto,et al.  Molecular dynamics simulations in the multibaric–multithermal ensemble , 2004 .

[28]  Y. Okamoto,et al.  Molecular dynamics, Langevin, and hybrid Monte Carlo simulations in multicanonical ensemble , 1996, physics/9710018.

[29]  Takashi Imai,et al.  Understanding high pressure stability of helical conformation of oligopeptides and helix bundle protein high pressure FT-IR and RISM theoretical studies. , 2006, Biochimica et biophysica acta.

[30]  A. Lyubartsev,et al.  New approach to Monte Carlo calculation of the free energy: Method of expanded ensembles , 1992 .

[31]  S. Nosé.  A unified formulation of the constant temperature molecular dynamics methods , 1984 .

[32]  Yuko Okamoto,et al.  Generalized-Ensemble Algorithms for the Isobaric–Isothermal Ensemble , 2010, 1004.2076.

[33]  Berg,et al.  Multicanonical ensemble: A new approach to simulate first-order phase transitions. , 1992, Physical review letters.

[34]  Yuko Okamoto,et al.  Replica-Exchange Monte Carlo Method for Ar Fluid , 2000 .

[35]  Alexander D. MacKerell,et al.  All-atom empirical potential for molecular modeling and dynamics studies of proteins. , 1998, The journal of physical chemistry. B.

[36]  Laxmikant V. Kalé,et al.  Scalable molecular dynamics with NAMD , 2005, J. Comput. Chem..

[37]  R. Swendsen,et al.  THE weighted histogram analysis method for free‐energy calculations on biomolecules. I. The method , 1992 .

[38]  A. Garcia,et al.  Simulations of the pressure and temperature unfolding of an α-helical peptide , 2005 .

[39]  Fumio Hirata,et al.  Theoretical study of the partial molar volume change associated with the pressure‐induced structural transition of ubiquitin , 2007, Protein science : a publication of the Protein Society.

[40]  Minoru Kato,et al.  Differences in the structural stability and cooperativity between monomeric variants of natural and de novo Cro proteins revealed by high-pressure Fourier transform infrared spectroscopy. , 2012, Biochemistry.

[41]  Alexander D. MacKerell,et al.  Extending the treatment of backbone energetics in protein force fields: Limitations of gas‐phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations , 2004, J. Comput. Chem..

[42]  C. Bugg,et al.  Structure of ubiquitin refined at 1.8 A resolution. , 1987, Journal of molecular biology.

[43]  S. Takada,et al.  On the Hamiltonian replica exchange method for efficient sampling of biomolecular systems: Application to protein structure prediction , 2002 .

[44]  David J Wilton,et al.  Pressure‐induced changes in the solution structure of the GB1 domain of protein G , 2007, Proteins.

[45]  Kenji Sugase,et al.  Solution structure of the Q41N variant of ubiquitin as a model for the alternatively folded N2 state of ubiquitin. , 2013, Biochemistry.

[46]  A Mitsutake,et al.  Generalized-ensemble algorithms for molecular simulations of biopolymers. , 2000, Biopolymers.

[47]  Jose A. Caro,et al.  Cavities determine the pressure unfolding of proteins , 2012, Proceedings of the National Academy of Sciences.

[48]  Yuko Okamoto,et al.  From multidimensional replica-exchange method to multidimensional multicanonical algorithm and simulated tempering. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

[50]  Matt Probert,et al.  Langevin dynamics in constant pressure extended systems. , 2004, The Journal of chemical physics.

[51]  R. Levy,et al.  Molecular dynamics simulation of solvated protein at high pressure. , 1992, Biochemistry.

[52]  Kazuyuki Akasaka,et al.  Simulation of Hydrated BPTI at High Pressure: Changes in Hydrogen Bonding and Its Relation with NMR Experiments , 2001 .

[53]  Ayori Mitsutake,et al.  Simulated-tempering replica-exchange method for the multidimensional version. , 2009, The Journal of chemical physics.

[54]  A. Kidera,et al.  Multicanonical Ensemble Generated by Molecular Dynamics Simulation for Enhanced Conformational Sampling of Peptides , 1997 .

[55]  Alan M. Ferrenberg,et al.  Optimized Monte Carlo data analysis. , 1989, Physical Review Letters.

[56]  Yuko Okamoto,et al.  Multibaric–Multithermal Molecular Dynamics Simulation of Alanine Dipeptide in Explicit Water , 2007 .

[57]  T. Darden,et al.  A smooth particle mesh Ewald method , 1995 .

[58]  Ryan Day,et al.  Pressure effects on the ensemble dynamics of ubiquitin inspected with molecular dynamics simulations and isotropic reorientational eigenmode dynamics. , 2008, Biophysical journal.

[59]  Yuko Okamoto,et al.  Replica-Exchange Molecular Dynamics Simulations for Various Constant Temperature Algorithms , 2010 .

[60]  Y. Sugita,et al.  Replica-exchange molecular dynamics method for protein folding , 1999 .

[61]  Yuko Okamoto,et al.  Multibaric–multithermal ensemble molecular dynamics simulations , 2006, J. Comput. Chem..

[62]  B. Berg,et al.  Multicanonical algorithms for first order phase transitions , 1991 .

[63]  T. Darden,et al.  Particle mesh Ewald: An N⋅log(N) method for Ewald sums in large systems , 1993 .

[64]  Y. Sugita,et al.  Multidimensional replica-exchange method for free-energy calculations , 2000, cond-mat/0009120.

[65]  Yoshiharu Mori,et al.  Pressure-Induced Helical Structure of a Peptide Studied by Simulated Tempering Molecular Dynamics Simulations. , 2013, The journal of physical chemistry letters.

[66]  Yuko Okamoto,et al.  Temperature and pressure dependence of alanine dipeptide studied by multibaric-multithermal molecular dynamics simulations. , 2008, The journal of physical chemistry. B.

[67]  U H Hansmann,et al.  New Monte Carlo algorithms for protein folding. , 1999, Current opinion in structural biology.

[68]  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.

[69]  Yuko Okamoto,et al.  Multidimensional generalized-ensemble algorithms for complex systems. , 2009, The Journal of chemical physics.

[70]  Vincent J Hilser,et al.  Coupled motion in proteins revealed by pressure perturbation. , 2012, Journal of the American Chemical Society.