Quasiharmonic analysis of protein energy landscapes from pressure-temperature molecular dynamics simulations

Rodgers, Jocelyn M.; Hemley, Russell J.; Ichiye, Toshiko

doi:10.1063/1.5003823

Title: Quasiharmonic analysis of protein energy landscapes from pressure-temperature molecular dynamics simulations

Journal Article · Wed Sep 27 00:00:00 EDT 2017 · Journal of Chemical Physics

DOI:https://doi.org/10.1063/1.5003823· OSTI ID:1535347

Rodgers, Jocelyn M. ^[1]; Hemley, Russell J. ^[2];

^[1]

Georgetown Univ., Washington, DC (United States)
George Washington Univ., Washington, DC (United States)

Positional fluctuations of an atom in a protein can be described as motion in an effective local energy minimum created by the surrounding protein atoms. The dependence of atomic fluctuations on both temperature (T) and pressure (P) has been used to probe the nature of these minima, which are generally described as harmonic in experiments such as x-ray crystallography and neutron scattering. Here, a quasiharmonic analysis method is presented in which the P-T dependence of atomic fluctuations is in terms of an intrinsic isobaric thermal expansivity αP and an intrinsic isothermal compressibility κT. The method is tested on previously reported mean-square displacements from P-T molecular dynamics simulations of lysozyme, which were interpreted to have a pressure-independent dynamical transition Tg near 200 K and a change in the pressure dependence near 480 MPa. Our quasiharmonic analysis of the same data shows that the P-T dependence can be described in terms of αP and κT where below Tg, the temperature dependence is frozen at the Tg value. In addition, the purported transition at 480 MPa is reinterpreted as a consequence of the pressure dependence of Tg and the quasiharmonic frequencies. The former also indicates that barrier heights between substates are pressure dependent in these data. Furthermore, the insights gained from this quasiharmonic analysis, which was of the energy landscape near the native state of a protein, suggest that similar analyses of other simulations may be useful in understanding such phenomena as pressure-induced protein unfolding.

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Research Organization:: Carnegie Inst. of Washington, Washington, DC (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: NA0002006; NA-0002006

OSTI ID:: 1535347

Alternate ID(s):: OSTI ID: 1395194

Journal Information:: Journal of Chemical Physics, Vol. 147, Issue 12; ISSN 0021-9606

Publisher:: American Institute of Physics (AIP)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 7 works

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References (26)

Constant pressure molecular dynamics for molecular systems Nosé, Shuichi; Klein, M. L. Molecular Physics, Vol. 50, Issue 5 https://doi.org/10.1080/00268978300102851	journal	December 1983
The energy landscape in non-biological and biological molecules Frauenfelder, Hans; Leeson, Daan Thorn Nature Structural Biology, Vol. 5, Issue 9 https://doi.org/10.1038/1784	journal	September 1998
Pressure-dependent Changes in the Solution Structure of Hen Egg-white Lysozyme Refaee, Mohamed; Tezuka, Tomoko; Akasaka, Kazuyuki Journal of Molecular Biology, Vol. 327, Issue 4 https://doi.org/10.1016/s0022-2836(03)00209-2	journal	April 2003
Evaluation and Reparametrization of the OPLS-AA Force Field for Proteins via Comparison with Accurate Quantum Chemical Calculations on Peptides ^† Kaminski, George A.; Friesner, Richard A.; Tirado-Rives, Julian The Journal of Physical Chemistry B, Vol. 105, Issue 28 https://doi.org/10.1021/jp003919d	journal	July 2001
Anisotropy and anharmonicity of atomic fluctuations in proteins: implications for x-ray analysis Ichiye, Toshiko; Karplus, Martin Biochemistry, Vol. 27, Issue 9 https://doi.org/10.1021/bi00409a054	journal	May 1988
GROMACS 3.0: a package for molecular simulation and trajectory analysis Lindahl, Erik; Hess, Berk; van der Spoel, David Journal of Molecular Modeling, Vol. 7, Issue 8 https://doi.org/10.1007/s008940100045	journal	August 2001
Pressure-induced amorphization of crystalline silica Hemley, R. J.; Jephcoat, A. P.; Mao, H. K. Nature, Vol. 334, Issue 6177 https://doi.org/10.1038/334052a0	journal	July 1988
Polymorphic transitions in single crystals: A new molecular dynamics method Parrinello, M.; Rahman, A. Journal of Applied Physics, Vol. 52, Issue 12 https://doi.org/10.1063/1.328693	journal	December 1981
Extreme biophysics: Enzymes under pressure Huang, Qi; Rodgers, Jocelyn M.; Hemley, Russell J. Journal of Computational Chemistry, Vol. 38, Issue 15 https://doi.org/10.1002/jcc.24737	journal	January 2017
Pressure-dependent transition in protein dynamics at about $4 kbar$ revealed by molecular dynamics simulation Meinhold, Lars; Smith, Jeremy C. Physical Review E, Vol. 72, Issue 6 https://doi.org/10.1103/physreve.72.061908	journal	December 2005
Vibrational thermodynamics of materials Fultz, Brent Progress in Materials Science, Vol. 55, Issue 4 https://doi.org/10.1016/j.pmatsci.2009.05.002	journal	May 2010
Structure of Pressure-Assisted Cold Denatured Lysozyme and Comparison with Lysozyme Folding Intermediates ^† Nash, David P.; Jonas, Jiri Biochemistry, Vol. 36, Issue 47 https://doi.org/10.1021/bi970881v	journal	November 1997
Physical aspects of protein dynamics Parak, Fritz G. Reports on Progress in Physics, Vol. 66, Issue 2 https://doi.org/10.1088/0034-4885/66/2/201	journal	December 2002
CHARMM: The biomolecular simulation program Brooks, B. R.; Brooks, C. L.; Mackerell, A. D. Journal of Computational Chemistry, Vol. 30, Issue 10 https://doi.org/10.1002/jcc.21287	journal	July 2009
The Protein Data Bank Berman, H. M. Nucleic Acids Research, Vol. 28, Issue 1 https://doi.org/10.1093/nar/28.1.235	journal	January 2000
Proteins, supercooled liquids, and glasses: A micro-review Frauenfelder, Hans Physica E: Low-dimensional Systems and Nanostructures, Vol. 42, Issue 3 https://doi.org/10.1016/j.physe.2009.08.005	journal	January 2010
Picosecond fluctuating protein energy landscape mapped by pressure temperature molecular dynamics simulation Meinhold, L.; Smith, J. C.; Kitao, A. Proceedings of the National Academy of Sciences, Vol. 104, Issue 44 https://doi.org/10.1073/pnas.0708199104	journal	October 2007
Dynamical transition of myoglobin revealed by inelastic neutron scattering Doster, Wolfgang; Cusack, Stephen; Petry, Winfried Nature, Vol. 337, Issue 6209 https://doi.org/10.1038/337754a0	journal	February 1989
Anisotropy and anharmonicity of atomic fluctuations in proteins: Analysis of a molecular dynamics simulation Ichiye, Toshiko; Karplus, Martin Proteins: Structure, Function, and Genetics, Vol. 2, Issue 3 https://doi.org/10.1002/prot.340020308	journal	January 1987
Protein Compressibility, Dynamics, and Pressure Kharakoz, Dmitri P. Biophysical Journal, Vol. 79, Issue 1 https://doi.org/10.1016/s0006-3495(00)76313-2	journal	July 2000
A unified formulation of the constant temperature molecular dynamics methods Nosé, Shuichi The Journal of Chemical Physics, Vol. 81, Issue 1 https://doi.org/10.1063/1.447334	journal	July 1984
Collective motions in proteins: A covariance analysis of atomic fluctuations in molecular dynamics and normal mode simulations Ichiye, Toshiko; Karplus, Martin Proteins: Structure, Function, and Genetics, Vol. 11, Issue 3 https://doi.org/10.1002/prot.340110305	journal	November 1991
Probing Conformational Fluctuation of Proteins by Pressure Perturbation Akasaka, Kazuyuki Chemical Reviews, Vol. 106, Issue 5 https://doi.org/10.1021/cr040440z	journal	May 2006
The ‘glass transition’ in protein dynamics: what it is, why it occurs, and how to exploit it Ringe, Dagmar; Petsko, Gregory A. Biophysical Chemistry, Vol. 105, Issue 2-3 https://doi.org/10.1016/s0301-4622(03)00096-6	journal	September 2003
Slaving: Solvent fluctuations dominate protein dynamics and functions Fenimore, P. W.; Frauenfelder, H.; McMahon, B. H. Proceedings of the National Academy of Sciences, Vol. 99, Issue 25 https://doi.org/10.1073/pnas.212637899	journal	November 2002
Theory of protein folding Onuchic, José Nelson; Wolynes, Peter G. Current Opinion in Structural Biology, Vol. 14, Issue 1 https://doi.org/10.1016/j.sbi.2004.01.009	journal	February 2004

Cited By (2)

Adaptations for pressure and temperature effects on loop motion in Escherichia coli and Moritella profunda dihydrofolate reductase Huang, Qi; Rodgers, Jocelyn M.; Hemley, Russell J. High Pressure Research, Vol. 39, Issue 2 https://doi.org/10.1080/08957959.2019.1584799	journal	March 2019
Effects of Pressure and Temperature on the Atomic Fluctuations of Dihydrofolate Reductase from a Psychropiezophile and a Mesophile Huang, Qi; Rodgers, Jocelyn; Hemley, Russell International Journal of Molecular Sciences, Vol. 20, Issue 6 https://doi.org/10.3390/ijms20061452	journal	March 2019

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