The Effect of Complex Solvents on the Structure and Dynamics of Protein Solutions: the case of Lysozyme in Trehalose/Water Mixtures
Abstract
We present a Molecular Dynamics simulation study of the effect of trehalose concentration on the structure and dynamics of individual proteins immersed in trehalose/water mixtures. Hen Egg White Lysozyme is used in this study and trehalose concentrations of 0%, 10%, 20%, 30% and 100% by weight are explored. Surprisingly, we have found that changes in trehalose concentration do not change the global structural characteristics of the protein as measured by standard quantities like the mean square deviation, radius of gyration, solvent accessible surface area, inertia tensor and asphericity. Only in the limit of pure trehalose these metrics change significantly. Specifically, we found that the protein is compressed by 2% when immersed in pure trehalose. At the amino acid level there is noticeable rearrangement of the surface residues due to the change in polarity of the surrounding environment with the addition of trehalose. From a dynamic perspective, our computation of the Incoherent Intermediate Scattering Function shows that the protein slows down with increasing trehalose concentration; however, this slowdown is not monotonic. Finally, we also report in-depth results for the hydration layer around the protein including its structure, hydrogen- bonding characteristics and dynamic behavior at different length scales.
- Authors:
-
- ORNL
- University of Akron
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1185330
- Grant/Contract Number:
- DE-AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- European Physical Journal B (EPJ B), The - Condensed Matter
- Additional Journal Information:
- Journal Name: European Physical Journal B (EPJ B), The - Condensed Matter; Journal Volume: 36; Journal Issue: 14
- Country of Publication:
- United States
- Language:
- English
Citation Formats
Ghattyvenkatakrishna, Pavan K, and Carri, Gustavo A. The Effect of Complex Solvents on the Structure and Dynamics of Protein Solutions: the case of Lysozyme in Trehalose/Water Mixtures. United States: N. p., 2013.
Web. doi:10.1140/epje/i2013-13014-3.
Ghattyvenkatakrishna, Pavan K, & Carri, Gustavo A. The Effect of Complex Solvents on the Structure and Dynamics of Protein Solutions: the case of Lysozyme in Trehalose/Water Mixtures. United States. https://doi.org/10.1140/epje/i2013-13014-3
Ghattyvenkatakrishna, Pavan K, and Carri, Gustavo A. Tue .
"The Effect of Complex Solvents on the Structure and Dynamics of Protein Solutions: the case of Lysozyme in Trehalose/Water Mixtures". United States. https://doi.org/10.1140/epje/i2013-13014-3. https://www.osti.gov/servlets/purl/1185330.
@article{osti_1185330,
title = {The Effect of Complex Solvents on the Structure and Dynamics of Protein Solutions: the case of Lysozyme in Trehalose/Water Mixtures},
author = {Ghattyvenkatakrishna, Pavan K and Carri, Gustavo A.},
abstractNote = {We present a Molecular Dynamics simulation study of the effect of trehalose concentration on the structure and dynamics of individual proteins immersed in trehalose/water mixtures. Hen Egg White Lysozyme is used in this study and trehalose concentrations of 0%, 10%, 20%, 30% and 100% by weight are explored. Surprisingly, we have found that changes in trehalose concentration do not change the global structural characteristics of the protein as measured by standard quantities like the mean square deviation, radius of gyration, solvent accessible surface area, inertia tensor and asphericity. Only in the limit of pure trehalose these metrics change significantly. Specifically, we found that the protein is compressed by 2% when immersed in pure trehalose. At the amino acid level there is noticeable rearrangement of the surface residues due to the change in polarity of the surrounding environment with the addition of trehalose. From a dynamic perspective, our computation of the Incoherent Intermediate Scattering Function shows that the protein slows down with increasing trehalose concentration; however, this slowdown is not monotonic. Finally, we also report in-depth results for the hydration layer around the protein including its structure, hydrogen- bonding characteristics and dynamic behavior at different length scales.},
doi = {10.1140/epje/i2013-13014-3},
journal = {European Physical Journal B (EPJ B), The - Condensed Matter},
number = 14,
volume = 36,
place = {United States},
year = {Tue Jan 01 00:00:00 EST 2013},
month = {Tue Jan 01 00:00:00 EST 2013}
}
Web of Science
Works referenced in this record:
Anhydrobiosis in Tardigrades and Nematodes
journal, October 1974
- Crowe, John H.; Madin, K. A.
- Transactions of the American Microscopical Society, Vol. 93, Issue 4
The role of Vitrification in Anhydrobiosis
journal, October 1998
- Crowe, John H.; Carpenter, John F.; Crowe, Lois M.
- Annual Review of Physiology, Vol. 60, Issue 1
The Trehalose Myth Revisited: Introduction to a Symposium on Stabilization of Cells in the Dry State
journal, September 2001
- Crowe, John H.; Crowe, Lois M.; Oliver, Ann E.
- Cryobiology, Vol. 43, Issue 2
An infrared spectroscopic study of the interactions of carbohydrates with dried proteins
journal, May 1989
- Carpenter, John F.; Crowe, John H.
- Biochemistry, Vol. 28, Issue 9
Separation of Freezing- and Drying-Induced Denaturation of Lyophilized Proteins Using Stress-Specific Stabilization
journal, June 1993
- Carpenter, J. F.; Prestrelski, S. J.; Arakawa, T.
- Archives of Biochemistry and Biophysics, Vol. 303, Issue 2
Stabilization of phosphofructokinase with sugars during freeze-drying: characterization of enhanced protection in the presence of divalent cations
journal, January 1987
- Carpenter, John F.; Crowe, Lois M.; Crowe, John H.
- Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 923, Issue 1
Preservation of functional integrity during long term storage of a biological membrane
journal, December 1984
- Mouradian, Robert; Womersley, Christopher; Crowe, Lois M.
- Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 778, Issue 3
Anomalous cryoprotective effectiveness of trehalose: Raman scattering evidences
journal, July 1999
- Branca, C.; Magazù, S.; Maisano, G.
- The Journal of Chemical Physics, Vol. 111, Issue 1
Formation of Spanning Water Networks on Protein Surfaces via 2D Percolation Transition
journal, February 2005
- Oleinikova, Alla; Smolin, Nikolai; Brovchenko, Ivan
- The Journal of Physical Chemistry B, Vol. 109, Issue 5
Water and proteins. II. The location and dynamics of water in protein systems and its relation to their stability and properties
journal, January 1983
- Edsall, J.
- Advances in Biophysics, Vol. 16
Elastic incoherent neutron scattering studies on glass forming hydrogen-bonded systems
journal, March 2004
- Migliardo, F.; Magazù, S.; Mondelli, C.
- Journal of Molecular Liquids, Vol. 110, Issue 1-3
Effect of the Environment on the Protein Dynamical Transition: A Neutron Scattering Study
journal, August 2002
- Paciaroni, Alessandro; Cinelli, Stefania; Onori, Giuseppe
- Biophysical Journal, Vol. 83, Issue 2
Protein and solvent dynamics: How strongly are they coupled?
journal, July 2004
- Caliskan, G.; Mechtani, D.; Roh, J. H.
- The Journal of Chemical Physics, Vol. 121, Issue 4
Inertial Suppression of Protein Dynamics in a Binary Glycerol−Trehalose Glass
journal, November 2006
- Curtis, Joseph E.; Dirama, Taner E.; Carri, Gustavo A.
- The Journal of Physical Chemistry B, Vol. 110, Issue 46
Slaving: Solvent fluctuations dominate protein dynamics and functions
journal, November 2002
- Fenimore, P. W.; Frauenfelder, H.; McMahon, B. H.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 25
Coupling between lysozyme and trehalose dynamics: Microscopic insights from molecular-dynamics simulations
journal, January 2006
- Dirama, Taner E.; Curtis, Joseph E.; Carri, Gustavo A.
- The Journal of Chemical Physics, Vol. 124, Issue 3
Role of Protein-Water Hydrogen Bond Dynamics in the Protein Dynamical Transition
journal, March 2002
- Tarek, M.; Tobias, D. J.
- Physical Review Letters, Vol. 88, Issue 13
Protein dynamics on the picosecond timescale as affected by the environment: a quasielastic neutron scattering study
journal, August 2003
- Paciaroni, A.; Orecchini, A.; Cinelli, S.
- Chemical Physics, Vol. 292, Issue 2-3
Fast and Slow Dynamics of Hydrogen Bonds in Liquid Water
journal, March 1999
- Starr, Francis W.; Nielsen, Johannes K.; Stanley, H. Eugene
- Physical Review Letters, Vol. 82, Issue 11
Molecular dynamics simulation of hydration in myoglobin
journal, May 1995
- Gu, Wei; Schoenborn, Benno P.
- Proteins: Structure, Function, and Genetics, Vol. 22, Issue 1
Effect of Environment on Hydrogen Bond Dynamics in Liquid Water
journal, February 1996
- Luzar, Alenka; Chandler, David
- Physical Review Letters, Vol. 76, Issue 6
Hydrogen-bond kinetics in liquid water
journal, January 1996
- Luzar, Alenka; Chandler, David
- Nature, Vol. 379, Issue 6560
Protein hydration elucidated by molecular dynamics simulation.
journal, October 1993
- Steinbach, P. J.; Brooks, B. R.
- Proceedings of the National Academy of Sciences, Vol. 90, Issue 19
VMD: Visual molecular dynamics
journal, February 1996
- Humphrey, William; Dalke, Andrew; Schulten, Klaus
- Journal of Molecular Graphics, Vol. 14, Issue 1
Molecular dynamics simulation evidence of anomalous diffusion of protein hydration water
journal, April 1996
- Bizzarri, Anna Rita; Cannistraro, Salvatore
- Physical Review E, Vol. 53, Issue 4
Solvent structure at a hydrophobic protein surface
journal, March 1997
- Kovacs, Helena; Mark, Alan E.; van Gunsteren, Wilfred F.
- Proteins: Structure, Function, and Genetics, Vol. 27, Issue 3
Molecular Dynamics of Water at the Protein−Solvent Interface
journal, July 2002
- Bizzarri, Anna Rita; Cannistraro, Salvatore
- The Journal of Physical Chemistry B, Vol. 106, Issue 26
Structure and dynamics of the water around myoglobin
journal, February 1995
- Phillips, George N.; Montgomery Pettitt, B.
- Protein Science, Vol. 4, Issue 2
Conformational changes of lysozyme in water-ethanol mixtures
journal, December 1997
- Bonincontro, A.; De Francesco, A.; Matzeu, M.
- Colloids and Surfaces B: Biointerfaces, Vol. 10, Issue 2
Correlations among Hydrogen Bonds in Liquid Water
journal, August 2004
- Raiteri, Paolo; Laio, Alessandro; Parrinello, Michele
- Physical Review Letters, Vol. 93, Issue 8
Ice Nanocrystals in Glycerol−Water Mixtures
journal, September 2005
- Hayashi, Yoshihito; Puzenko, Alexander; Feldman, Yuri
- The Journal of Physical Chemistry B, Vol. 109, Issue 35
Molecular Dynamics Study of Hydration in Ethanol−Water Mixtures Using a Polarizable Force Field †
journal, April 2005
- Noskov, Sergei Yu.; Lamoureux, Guillaume; Roux, Benoît
- The Journal of Physical Chemistry B, Vol. 109, Issue 14
Hydrogen Bonding and the Cryoprotective Properties of Glycerol/Water Mixtures
journal, July 2006
- Dashnau, Jennifer L.; Nucci, Nathaniel V.; Sharp, Kim A.
- The Journal of Physical Chemistry B, Vol. 110, Issue 27
Computational Approaches to Investigate How Biological Macromolecules Can Be Protected in Extreme Conditions
journal, January 2007
- Dashnau, J. L.; Vanderkooi, J. M.
- Journal of Food Science, Vol. 72, Issue 1
Spectroscopy and dynamics of mixtures of water with acetone, acetonitrile, and methanol
journal, December 2000
- Venables, Dean S.; Schmuttenmaer, Charles A.
- The Journal of Chemical Physics, Vol. 113, Issue 24
Relaxation Dynamics in Glycerol−Water Mixtures: I. Glycerol-Rich Mixtures
journal, March 2005
- Puzenko, Alexander; Hayashi, Yoshihito; Ryabov, Yaroslav E.
- The Journal of Physical Chemistry B, Vol. 109, Issue 12
Dielectric properties of glycerol/water mixtures at temperatures between 10 and 50°C
journal, April 2006
- Behrends, R.; Fuchs, K.; Kaatze, U.
- The Journal of Chemical Physics, Vol. 124, Issue 14
Picosecond Internal Dynamics of Lysozyme as Affected by Thermal Unfolding in Nonaqueous Environment
journal, January 2004
- De Francesco, A.; Marconi, M.; Cinelli, S.
- Biophysical Journal, Vol. 86, Issue 1
Development and testing of a general amber force field
journal, January 2004
- Wang, Junmei; Wolf, Romain M.; Caldwell, James W.
- Journal of Computational Chemistry, Vol. 25, Issue 9
Solvent dependence of dynamic transitions in protein solutions
journal, August 2000
- Reat, V.; Dunn, R.; Ferrand, M.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 18
The role of protein–solvent hydrogen bond dynamics in the structural relaxation of a protein in glycerol versus water
journal, April 2008
- Tarek, Mounir; Tobias, Douglas J.
- European Biophysics Journal, Vol. 37, Issue 5
Thermodynamic and kinetic examination of protein stabilization by glycerol
journal, August 1981
- Gekko, Kunihiko; Timasheff, Serge N.
- Biochemistry, Vol. 20, Issue 16
Mechanism of protein stabilization by glycerol: preferential hydration in glycerol-water mixtures
journal, August 1981
- Gekko, Kunihiko; Timasheff, Serge N.
- Biochemistry, Vol. 20, Issue 16
Crystallization of Ice in Aqueous Solutions of Glycerol and Dimethyl Sulfoxide 2: Ice Crystal Growth Kinetics
journal, September 1998
- Hey, J. M.; MacFarlane, D. R.
- Cryobiology, Vol. 37, Issue 2
Crystallization of Ice in Aqueous Solutions of Glycerol and Dimethyl Sulfoxide. 1. A Comparison of Mechanisms
journal, April 1996
- Hey, J. M.; Macfarlane, D. R.
- Cryobiology, Vol. 33, Issue 2
Molecular‐dynamics simulation of aqueous mixtures: Methanol, acetone, and ammonia
journal, October 1990
- Ferrario, Mauro; Haughney, Michael; McDonald, Ian R.
- The Journal of Chemical Physics, Vol. 93, Issue 7
The Dynamics of Protein Hydration Water: A Quantitative Comparison of Molecular Dynamics Simulations and Neutron-scattering Experiments
journal, December 2000
- Tarek, Mounir; Tobias, Douglas J.
- Biophysical Journal, Vol. 79, Issue 6
Percolation transition of hydration water in biosystems
journal, November 2006
- Oleinikova, Alla; Brovchenko, Ivan
- Molecular Physics, Vol. 104, Issue 22-24
Comparison of simple potential functions for simulating liquid water
journal, July 1983
- Jorgensen, William L.; Chandrasekhar, Jayaraman; Madura, Jeffry D.
- The Journal of Chemical Physics, Vol. 79, Issue 2
The influence of a protein on water dynamics in its vicinity investigated by molecular dynamics simulation
journal, July 1996
- Abseher, Roger; Schreiber, Hellfried; Steinhauser, Othmar
- Proteins: Structure, Function, and Genetics, Vol. 25, Issue 3
Viscosity-Dependent Protein Dynamics
journal, May 2007
- Finkelstein, Ilya J.; Massari, Aaron M.; Fayer, M. D.
- Biophysical Journal, Vol. 92, Issue 10
How a Vicinal Layer of Solvent Modulates the Dynamics of Proteins
journal, January 2008
- Atilgan, Canan; Aykut, Ayse Ozlem; Atilgan, Ali Rana
- Biophysical Journal, Vol. 94, Issue 1
How Do Trehalose, Maltose, and Sucrose Influence Some Structural and Dynamical Properties of Lysozyme? Insight from Molecular Dynamics Simulations
journal, August 2007
- Lerbret, A.; Bordat, P.; Affouard, F.
- The Journal of Physical Chemistry B, Vol. 111, Issue 31
Coupling between lysozyme and glycerol dynamics: Microscopic insights from molecular-dynamics simulations
journal, June 2005
- Dirama, Taner E.; Carri, Gustavo A.; Sokolov, Alexei P.
- The Journal of Chemical Physics, Vol. 122, Issue 24
Trehalose-protein interaction in aqueous solution
journal, February 2004
- Lins, Roberto D.; Pereira, Cristina S.; Hünenberger, Philippe H.
- Proteins: Structure, Function, and Bioinformatics, Vol. 55, Issue 1
Protein Thermal Denaturation and Matrix Glass Transition in Different Protein−Trehalose−Water Systems
journal, May 2011
- Bellavia, Giuseppe; Giuffrida, Sergio; Cottone, Grazia
- The Journal of Physical Chemistry B, Vol. 115, Issue 19
Calorimetric study of myoglobin embedded in trehalose-water matrixes
journal, March 2009
- Bellavia, G.; Cordone, L.; Cupane, A.
- Journal of Thermal Analysis and Calorimetry, Vol. 95, Issue 3
Trehalose As a “Chemical Chaperone”
book, January 2007
- Crowe, John H.
- Advances in Experimental Medicine and Biology, Vol. Molecular Aspects of the Stress Response: Chaperones, Membranes and Networks
Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures
journal, July 2002
- Kandror, O.; DeLeon, A.; Goldberg, A. L.
- Proceedings of the National Academy of Sciences, Vol. 99, Issue 15
How Strongly Does Trehalose Interact with Lysozyme in the Solid State? Insights from Molecular Dynamics Simulation and Inelastic Neutron Scattering
journal, August 2012
- Lerbret, Adrien; Affouard, Frédéric; Hédoux, Alain
- The Journal of Physical Chemistry B, Vol. 116, Issue 36
High-Resolution Structure (1.33 Å) of a HEW Lysozyme Tetragonal Crystal Grown in the APCF Apparatus. Data and Structural Comparison with a Crystal Grown under Microgravity from SpaceHab-01 Mission
journal, May 1996
- Vaney, M. C.; Maignan, S.; Riès-Kautt, M.
- Acta Crystallographica Section D Biological Crystallography, Vol. 52, Issue 3
Enhanced Trehalose Production Improves Growth of Escherichia coli under Osmotic Stress†
journal, July 2005
- Purvis, J. E.; Yomano, L. P.; Ingram, L. O.
- Applied and Environmental Microbiology, Vol. 71, Issue 7
Comparison of multiple Amber force fields and development of improved protein backbone parameters
journal, November 2006
- Hornak, Viktor; Abel, Robert; Okur, Asim
- Proteins: Structure, Function, and Bioinformatics, Vol. 65, Issue 3
Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems
journal, June 1993
- Darden, Tom; York, Darrin; Pedersen, Lee
- The Journal of Chemical Physics, Vol. 98, Issue 12
Molecular dynamics with coupling to an external bath
journal, October 1984
- Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F.
- The Journal of Chemical Physics, Vol. 81, Issue 8
An analysis of the accuracy of Langevin and molecular dynamics algorithms
journal, December 1988
- Pastor, Richard W.; Brooks, Bernard R.; Szabo, Attila
- Molecular Physics, Vol. 65, Issue 6
Relaxation dynamics of biopolymers seeded with unfolded lysozyme transients in vacuo. The role of primary sequence in protein folding
journal, January 2000
- Arteca, Gustavo A.; Paulino, M.; Reimann, C. T.
- Physical Chemistry Chemical Physics, Vol. 2, Issue 22
Knowledge-based protein secondary structure assignment
journal, December 1995
- Frishman, Dmitrij; Argos, Patrick
- Proteins: Structure, Function, and Genetics, Vol. 23, Issue 4
Dielectric study of the antiplasticization of trehalose by glycerol
journal, September 2006
- Anopchenko, A.; Psurek, T.; VanderHart, D.
- Physical Review E, Vol. 74, Issue 3
Amplitudes and Frequencies of Protein Dynamics: Analysis of Discrepancies between Neutron Scattering and Molecular Dynamics Simulations
journal, October 2000
- Tarek, Mounir; Martyna, Glenn J.; Tobias, Douglas J.
- Journal of the American Chemical Society, Vol. 122, Issue 42
Onsets of Anharmonicity in Protein Dynamics
journal, July 2005
- Roh, J. H.; Novikov, V. N.; Gregory, R. B.
- Physical Review Letters, Vol. 95, Issue 3
Influence of Hydration on the Dynamics of Lysozyme
journal, October 2006
- Roh, J. H.; Curtis, J. E.; Azzam, S.
- Biophysical Journal, Vol. 91, Issue 7
Protein normal-mode dynamics: Trypsin inhibitor, crambin, ribonuclease and lysozyme
journal, February 1985
- Levitt, Michael; Sander, Christian; Stern, Peter S.
- Journal of Molecular Biology, Vol. 181, Issue 3
Domain communication in the dynamical structure of human immunodeficiency virus 1 protease.
journal, November 1990
- Harte, W. E.; Swaminathan, S.; Mansuri, M. M.
- Proceedings of the National Academy of Sciences, Vol. 87, Issue 22
Investigation of domain structure in proteins via molecular dynamics simulation: application to HIV-1 protease dimer
journal, March 1991
- Swaminathan, S.; Harte, W. E.; Beveridge, David L.
- Journal of the American Chemical Society, Vol. 113, Issue 7
Relating Molecular Flexibility to Function: A Case Study of Tubulin
journal, August 2002
- Keskin, Ozlem; Durell, Stewart R.; Bahar, Ivet
- Biophysical Journal, Vol. 83, Issue 2
Cis/trans isomerization in HIV-1 capsid protein catalyzed by cyclophilin A: Insights from computational and theoretical studies
journal, May 2004
- Agarwal, Pratul K.
- Proteins: Structure, Function, and Bioinformatics, Vol. 56, Issue 3
Dielectric Relaxation of Biological Water †
journal, December 1997
- Nandi, Nilashis; Bagchi, Biman
- The Journal of Physical Chemistry B, Vol. 101, Issue 50
Dielectric relaxation spectra of water adsorbed on lysozyme
journal, October 1972
- Harvey, S. C.; Hoekstra, P.
- The Journal of Physical Chemistry, Vol. 76, Issue 21
Works referencing / citing this record:
Temperature-induced recovery of a bioactive enzyme using polyglycerol dendrimers: correlation between bound water and protein interaction
journal, February 2018
- Ooya, Tooru; Ogawa, Takaya; Takeuchi, Toshifumi
- Journal of Biomaterials Science, Polymer Edition, Vol. 29, Issue 6
Temperature-induced recovery of a bioactive enzyme using polyglycerol dendrimers: correlation between bound water and protein interaction
text, January 2018
- Ooya, Tooru; Ogawa, Takaya; Takeuchi, Toshifumi
- Taylor & Francis
Temperature-induced recovery of a bioactive enzyme using polyglycerol dendrimers: correlation between bound water and protein interaction
text, January 2018
- Ooya, Tooru; Ogawa, Takaya; Takeuchi, Toshifumi
- Taylor & Francis