Abstract
We study the dynamics of the first hydration shell of lysozyme to determine the role of hydration water that accompanies lysozyme thermal denaturation. We use nuclear magnetic resonance spectroscopy to investigate both the translational and rotational contributions. Data on proton self-diffusion and reorentational correlation time indicate that the kinetics of the lysozyme folding/unfolding process is controlled by the dynamics of the water molecules in the first hydration shell. When the hydration water dynamics change, because of the weakening of the hydrogen bond network, the three-dimensional structure of the lysozyme is lost and denaturation is triggered. Our data indicates that at temperatures above approximately 315 K, water behaves as a simple liquid and is no longer a good solvent.
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G. R. Bowman and V. S. Pande, Protein folded states are kinetic hubs, Proc. Natl. Acad. Sci. USA 107, 10890 (2010)
G. D. Rose, P. J. Fleming, J. R. Banavar, and A. Maritan, A backbone-based theory of protein folding, Proc. Natl. Acad. Sci. USA 103(45), 16623 (2006)
M. Karplus, Behind the folding funnel diagram, Nat. Chem. Biol. 7, 401 (2011)
P. Ball, Water as an active constituent in cell biology, Chem. Rev. 108, 74 (2008)
J. A. Rupley, P. H. Yang, and G. Tollin, Thermodynamic and related studies of water interacting with proteins in water in polymers, Vol. 127, edited by S. P. Rowland, ACS Symposium Series, 1980, p. 111
R. B. Gregory, Protein Solvent Interaction, New York: Marcel Dekker, 1995
L. Comez, S. Perticaroli, M. Paolantoni, P. Sassi, S. Corezzi, A. Morresi, and D. Fioretto, Concentration dependence of hydration water in a model peptide, Phys. Chem. Chem. Phys. 16, 12433 (2014)
J. A. Rupley and G. Careri, Protein hydration and function, Adv. Protein Chem. 41, 37 (1991)
V. Helms, Protein dynamics tightly connected to the dynamics of surrounding and internal water molecules, Chem Phys Chem 8, 23 (2007)
G. Schirò, M. Fomina, and A. Cupane, Communication: Protein dynamical transition vs. liquid-liquid phase transition in protein hydration water, J. Chem. Phys. 139, 121102 (2013)
K. L. Ngai, S. Capaccioli, and N. Shinyashiki, The protein glass transition and the role of the solvent, J Phys Chem B 112(12), 3826 (2008)
K. L. Ngai, S. Capaccioli, and A. Paciaroni, Nature of the water specific relaxation in hydrated proteins and aqueous mixtures, Chem. Phys. 424, 37 (2013)
S.-H. Chen, L. Liu, E. Fratini, P. Baglioni, A. Faraone, and E. Mamontov, Observation of fragile-to-strong dynamic crossover in protein hydration water, Proc. Natl. Acad. Sci. USA 103, 9012 (2006)
F. Mallamace, S.-H. Chen, M. Broccio, C. Corsaro, V. Crupi, et al., Role of the solvent in the dynamical transitions of proteins: The case of the lysozyme-water system, J. Chem. Phys. 127, 045104 (2007)
F. Mallamace, C. Branca, C. Corsaro, N. Leone, J. Spooren, et al., Dynamical crossover and breakdown of the Stokes–Einstein relation in confined water and in Methanol–Diluted bulk water, J. Phys. Chem. B 114(5), 1870 (2010)
Y. Zhang, M. Lagi, D. Liu, F. Mallamace, E. Fratini, et al., Observation of high-temperature dynamic crossover in protein hydration water and its relation to reversible denaturation of lysozyme, J. Chem. Phys. 130, 135101 (2009)
M. Lagi, X. Chu, C. Kim, F. Mallamace, P. Baglioni, et al., The low-temperature dynamic crossover phenomenon in protein hydration water: Simulations vs. experiments, J. Phys. Chem. B 112(6), 1571 (2008)
P. Kumar, Z. Yan, L. Xu, M. G. Mazza, S. V. Buldyrev, et al., Glass transition in biomolecules and the liquid-liquid critical point of water, Phys. Rev. Lett. 97, 177802 (2006)
S.-H. Chen, Y. Zhang, M. Lagi, S.-H. Chong, P. Baglioni, and F. Mallamace, Evidence of dynamic crossover phenomena in water and other glass-forming liquids: Experiments, MD simulations and theory, J. Phys.: Condens. Matter 21, 504102 (2009)
F. Mallamace, M. Broccio, C. Corsaro, A. Faraone, L. Liu, C.-Y. Mou, and S.-H. Chen, Dynamical properties of confined supercooled water: an NMR study, J. Phys.: Condens. Matter 18, S2285 (2006)
W. Doster, S. Cusak, and W. Petry, Dynamical transition of myoglobin revealed by inelastic neutron scattering, Nature 337, 754 (1989)
W. Doster, The dynamical transition of proteins, concepts and misconceptions, Eur. Biophys. J. 37, 591 (2008)
W. Doster, S. Busch, A. M. Gaspar, M.-S. Appavou, J. Wuttke, and H. Scheer, Dynamical transition of proteinhydration water, Phys. Rev. Lett. 104, 098101 (2010)
S. Khodadadi, S. Pawlus, and A. P. Sokolov, Influence of hydration on protein dynamics: Combining dielectric and neutron scattering spectroscopy data, J. Phys. Chem. B 112, 14273 (2008)
S. Khodadadi, S. Pawlus, J. H. Roh, V. Garcia-Sakai, E. Mamontov, and A. P. Sokolov, The origin of the dynamic transition in proteins, J. Chem. Phys. 128, 195106 (2008)
G. Schirò, F. Natali, and A. Cupane, Physical origin of anharmonic dynamics in proteins: New insights from resolution-dependent neutron scattering on homomeric polypeptides, Phys. Rev. Lett. 109, 128102 (2012)
F. Mallamace, P. Baglioni, C. Corsaro, S.-H. Chen, D. Mallamace, C. Vasi, and H. E. Stanley, The influence of water on protein properties, J. Chem. Phys. 141, 165104 (2014)
F. Mallamace, C. Corsaro, D.Mallamace, S. Vasi, C. Vasi, H. E. Stanley, and S.-H. Chen, Some thermodynamical aspects of protein hydration water, J. Chem. Phys. 142, 215103 (2015)
F. Mallamace, C. Corsaro, D. Mallamace, S. Vasi, C. Vasi, and H. E. Stanley, Thermodynamic properties of bulk and confined water, J. Chem. Phys. 141, 18C504 (2014)
F. Mallamace, C. Corsaro, D. Mallamace, S. Vasi, C. Vasi, and G. Dugo, The role of water in protein’s behavior: The two dynamical crossovers studied by NMR and FTIR techniques, Computational and Structural Biotechnology Journal 13, 33 (2015)
F. Mallamace, C. Corsaro, P. Baglioni, E. Fratini, and S.-H. Chen, The dynamical crossover phenomenon in bulk water, confined water and protein hydration water, J. Phys.: Condens. Matter 24, 064103 (2012)
F. Mallamace, S.-H. Chen, Y. Liu, L. Lobry, and N. Micali, Percolation and viscoelasticity of triblock copolymer micellar solutions, Physica A: Statistical Mechanics and its Applications 266, 123 (1999)
D. Russo, G. Hura, and T. Head-Gordon, Hydration dynamics near a model protein surface, Biophys. J. 86, 1852 (2004)
A. Ben-Naim, The role of hydrogen bonds in protein folding and protein association, J. Phys. Chem. 95, 1437 (1991)
V. Kocherbitov, J. Latynis, A. Misiunas, J. Barauskas, and G. Niaura, Hydration of lysozyme studied by raman rpectroscopy, J. Phys. Chem. B 117, 4981 (2013)
G. Zaccai, How soft is a protein? A protein dynamics force constant measured by neutron scattering, Science 288, 1604 (2000)
P. W. Fenimore, H. Frauenfelder, B. H. McMahon, and F. G. Parak, Slaving: solvent fluctuations dominate protein dynamics and functions, Proc. Natl. Acad. Sci. USA 99, 16047 (2002)
H. Frauenfelder, P. W. Fenimore, and R. D. Young, Protein dynamics and function: Insights from the energy landscape and solvent slaving, IUBMB Life 59, 506 (2007)
F. Mallamace, C. Corsaro, and H. E. Stanley, A singular thermodynamically consistent temperature at the origin of the anomalous behavior of liquid water, Sci. Rep. 2, 993 (2012)
F. Chiti and C. M. Dobson, Amyloid formation by globular proteins under native conditions, Nat. Chem. Biol. 5, 15 (2009)
D. J. Selkoe, Folding proteins in fatal ways, Nature 426, 900 (2003)
G. Salvetti, E. Tombari, L. Mikheeva, and G. P. Johari, The endothermic effects during denaturation of lysozyme by temperature modulated calorimetry and an intermediate reaction equilibrium, J. Phys. Chem. B 106, 6081 (2002)
F. Mallamace, C. Corsaro, D. Mallamace, P. Baglioni, H. E. Stanley, and S.-H. Chen, A possible role of water in the protein folding process, J. Phys. Chem. B 115, 14280 (2011)
D. Mallamace, C. Corsaro, C. Vasi, S. Vasi, G. Dugo, and F. Mallamace, The protein irreversible denaturation studied by means of the bending vibrational mode, Physica A: Statistical Mechanics and its Applications 412, 39 (2014)
F. Sterpone, G. Stirnemann, and D. Laage, Magnitude and molecular origin of water slowdown next to a protein, J. Am. Chem. Soc. 134, 4116 (2012)
C. Mattea, J. Qvist, and B. Halle, Dynamics at the proteinwater interface from 17O spin relaxation in deeply supercooled solutions, Biophys. J. 95, 2951 (2008)
E. Dubouè-Dijon, A. C. Fogarty, and D. Laage, Temperature dependence of hydrophobic hydration dynamics: From retardation to acceleration, J. Phys. Chem. B 118, 1574 (2014)
S. Pronk, E. Lindahl, and P. M. Kasson, Dynamic heterogeneity controls diffusion and viscosity near biological interfaces, Nature Communications 5, 3034 (2014)
A. C. Fogarty and Damien Laage, Water dynamics in protein hydration shells: The molecular origins of the dynamical perturbation, J. Phys. Chem. B 118, 7715 (2014)
W. S. Price, Pulsed-field gradient nuclear magnetic resonance as a tool for studying translational diffusion (Part II): Experimental aspects, Concepts Magn. Reson. 10, 197 (1998)
A. Abragam, The Principles of Nuclear Magnetism, Oxford, UK: Oxford, 1961
S. Perticaroli, L. Comez, P. Sassi, M. Paolantoni, S. Corezzi, S. Caponi, A. Morresi, and D. Fioretto, Hydration and aggregation of lysozyme by extended frequency range depolarized light scattering, Journal of Non-Crystalline Solids 407, 472 (2015)
B. Jana, S. Pal, and B. Bagchi, Hydration dynamics of protein molecules in aqueous solution: Unity among diversity, J. Chem. Sci. 124 (1), 317 (2012)
A. S. Parmar and M. Muschol, Hydration and hydrodynamic interactions of lysozyme: effects of chaotropic versus kosmotropic ions, Biophysical Journal 97, 590 (2009)
A. Bizzarri, S. Cannistraro, Molecular dynamics of water at the protein-solvent interface, J. Phys. Chem. B 106, 6617 (2002)
W. S. Price, H. Ide, and Y. Arata, Self-diffusion of supercooled water to 238 K using PGSE NMR diffusion measurements, J. Phys. Chem. A 103, 448 (1999)
J. H. Simpson and H. Y. Carr, Diffusion and Nuclear Spin Relaxation in Water, Phys. Rev. 111, 1201 (1958)
C. Corsaro and D. Mallamace, A nuclear magnetic resonance study of the reversible denaturation of hydrated lysozyme, Physica A: Statistical Mechanics and its Applications 390, 2904 (2011)
D. W. G. Smith and J. G. Powles, Proton spin-lattice relaxation in liquid water and liquid ammonia, Mol. Phys. 10, 451 (1966)
T. DeFries and J. Jonas, Pressure dependence of NMR proton spin-lattice relaxation times and shear viscosity in liquid water in the temperature range–15–10 °C, J. Chem. Phys. 66, 896 (1977)
E. Lang and H.-D. Lüdemann, Pressure and temperature dependence of the longitudinal proton relaxation times in supercooled water to–87°C and 2500 bar, J. Chem. Phys. 67, 718 (1977)
N. Bloembergen, E. M. Purcell, and R. V. Pound, Relaxation effects in nuclear magnetic resonance absorption, Phys. Rev. 73, 679 (1948)
B. Halle and M. Davidovic, Biomolecular hydration: From water dynamics to hydrodynamics, Proc. Natl. Acad. Sci. USA 100, 12135 (2003)
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Mallamace, F., Corsaro, C., Mallamace, D. et al. Dynamical changes in hydration water accompanying lysozyme thermal denaturation. Front. Phys. 10, 106104 (2015). https://doi.org/10.1007/s11467-015-0486-9
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DOI: https://doi.org/10.1007/s11467-015-0486-9