Please wait a minute...
Frontiers of Physics

ISSN 2095-0462

ISSN 2095-0470(Online)

CN 11-5994/O4

Postal Subscription Code 80-965

2018 Impact Factor: 2.483

Front. Phys.    2015, Vol. 10 Issue (5) : 106104    https://doi.org/10.1007/s11467-015-0486-9
RESEARCH ARTICLE
Dynamical changes in hydration water accompanying lysozyme thermal denaturation
Francesco Mallamace1,2,3,*(),Carmelo Corsaro1,2,Domenico Mallamace4,Nicola Cicero4,Sebastiano Vasi2,Giacomo Dugo4,H. Eugene Stanley3
1. CNR-IPCF Messina, Istituto per i Processi Chimico-Fisici, Viale F. Stagno D’Alcontres 37, 98158 Messina, Italy
2. Dipartimento di Fisica e Scienze della Terra, Università di Messina, Viale F. Stagno D’Alcontres 31, 98166 Messina, Italy
3. Center for Polymer Studies and Department of Physics, Boston University, Boston, MA 02215, USA
4. Dipartimento di Scienze dell’Ambiente, della Sicurezza, del Territorio, degli Alimenti, e della Salute, Università di Messina Viale F. Stagno d’Alcontres 31, 98166 Messina, Italy
 Download: PDF(292 KB)  
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
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.

Keywords lysozyme unfolding      hydration water      NMR      correlation time      solvent dynamics     
Corresponding Author(s): Francesco Mallamace   
Issue Date: 26 October 2015
 Cite this article:   
Francesco Mallamace,Carmelo Corsaro,Domenico Mallamace, et al. Dynamical changes in hydration water accompanying lysozyme thermal denaturation[J]. Front. Phys. , 2015, 10(5): 106104.
 URL:  
https://academic.hep.com.cn/fop/EN/10.1007/s11467-015-0486-9
https://academic.hep.com.cn/fop/EN/Y2015/V10/I5/106104
1 G. R. Bowman and V. S. Pande, Protein folded states are kinetic hubs, Proc. Natl. Acad. Sci. USA 107, 10890 (2010)
https://doi.org/10.1073/pnas.1003962107
2 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)
https://doi.org/10.1073/pnas.0606843103
3 M. Karplus, Behind the folding funnel diagram, Nat. Chem. Biol. 7, 401 (2011)
https://doi.org/10.1038/nchembio.565
4 P. Ball, Water as an active constituent in cell biology, Chem. Rev. 108, 74 (2008)
https://doi.org/10.1021/cr068037a
5 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
6 R. B. Gregory, Protein Solvent Interaction, New York: Marcel Dekker, 1995
7 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)
https://doi.org/10.1039/c4cp00840e
8 J. A. Rupley and G. Careri, Protein hydration and function, Adv. Protein Chem. 41, 37 (1991)
https://doi.org/10.1016/S0065-3233(08)60197-7
9 V. Helms, Protein dynamics tightly connected to the dynamics of surrounding and internal water molecules, ChemPhysChem 8, 23 (2007)
https://doi.org/10.1002/cphc.200600298
10 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)
https://doi.org/10.1063/1.4822250
11 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)
https://doi.org/10.1021/jp710462e
12 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)
https://doi.org/10.1016/j.chemphys.2013.05.018
13 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)
https://doi.org/10.1073/pnas.0602474103
14 F. Mallamace, S.-H. Chen, M. Broccio, C. Corsaro, V. Crupi, , Role of the solvent in the dynamical transitions of proteins: The case of the lysozyme-water system, J. Chem. Phys. 127, 045104 (2007)
https://doi.org/10.1063/1.2757171
15 F. Mallamace, C. Branca, C. Corsaro, N. Leone, J. Spooren, , 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)
https://doi.org/10.1021/jp910038j
16 Y. Zhang, M. Lagi, D. Liu, F. Mallamace, E. Fratini, , Observation of high-temperature dynamic crossover in protein hydration water and its relation to reversible denaturation of lysozyme, J. Chem. Phys. 130, 135101 (2009)
https://doi.org/10.1063/1.3081137
17 M. Lagi, X. Chu, C. Kim, F. Mallamace, P. Baglioni, , The low-temperature dynamic crossover phenomenon in protein hydration water: Simulations vs. experiments, J. Phys. Chem. B 112(6), 1571 (2008)
https://doi.org/10.1021/jp710714j
18 P. Kumar, Z. Yan, L. Xu, M. G. Mazza, S. V. Buldyrev, , Glass transition in biomolecules and the liquid-liquid critical point of water, Phys. Rev. Lett. 97, 177802 (2006)
https://doi.org/10.1103/PhysRevLett.97.177802
19 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)
https://doi.org/10.1088/0953-8984/21/50/504102
20 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)
https://doi.org/10.1088/0953-8984/18/36/S04
21 W. Doster, S. Cusak, and W. Petry, Dynamical transition of myoglobin revealed by inelastic neutron scattering, Nature 337, 754 (1989)
https://doi.org/10.1038/337754a0
22 W. Doster, The dynamical transition of proteins, concepts and misconceptions, Eur. Biophys. J. 37, 591 (2008)
https://doi.org/10.1007/s00249-008-0274-3
23 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)
https://doi.org/10.1103/PhysRevLett.104.098101
24 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)
https://doi.org/10.1021/jp8059807
25 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)
https://doi.org/10.1063/1.2927871
26 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)
https://doi.org/10.1103/PhysRevLett.109.128102
27 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)
https://doi.org/10.1063/1.4900500
28 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)
https://doi.org/10.1063/1.4921897
29 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)
30 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)
https://doi.org/10.1016/j.csbj.2014.11.007
31 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)
https://doi.org/10.1088/0953-8984/24/6/064103
32 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)
33 D. Russo, G. Hura, and T. Head-Gordon, Hydration dynamics near a model protein surface, Biophys. J. 86, 1852 (2004)
https://doi.org/10.1016/S0006-3495(04)74252-6
34 A. Ben-Naim, The role of hydrogen bonds in protein folding and protein association, J. Phys. Chem. 95, 1437 (1991)
https://doi.org/10.1021/j100156a074
35 V. Kocherbitov, J. Latynis, A. Misiūnas, J. Barauskas, and G. Niaura, Hydration of lysozyme studied by raman rpectroscopy, J. Phys. Chem. B 117, 4981 (2013)
https://doi.org/10.1021/jp4017954
36 G. Zaccai, How soft is a protein? A protein dynamics force constant measured by neutron scattering, Science 288, 1604 (2000)
https://doi.org/10.1126/science.288.5471.1604
37 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)
https://doi.org/10.1073/pnas.212637899
38 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)
https://doi.org/10.1080/15216540701194113
39 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)
https://doi.org/10.1038/srep00993
40 F. Chiti and C. M. Dobson, Amyloid formation by globular proteins under native conditions, Nat. Chem. Biol. 5, 15 (2009)
https://doi.org/10.1038/nchembio.131
41 D. J. Selkoe, Folding proteins in fatal ways, Nature 426, 900 (2003)
https://doi.org/10.1038/nature02264
42 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)
https://doi.org/10.1021/jp025587d
43 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)
https://doi.org/10.1021/jp205285t
44 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)
45 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)
https://doi.org/10.1021/ja3007897
46 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)
https://doi.org/10.1529/biophysj.108.135194
47 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)
https://doi.org/10.1021/jp408603n
48 S. Pronk, E. Lindahl, and P. M. Kasson, Dynamic heterogeneity controls diffusion and viscosity near biological interfaces, Nature Communications 5, 3034 (2014)
https://doi.org/10.1038/ncomms4034
49 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)
https://doi.org/10.1021/jp409805p
50 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)
https://doi.org/10.1002/(SICI)1099-0534(1998)10:4<197::AID-CMR1>3.0.CO;2-S
51 A. Abragam, The Principles of Nuclear Magnetism, Oxford, UK: Oxford, 1961
52 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)
https://doi.org/10.1016/j.jnoncrysol.2014.07.017
53 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)
https://doi.org/10.1007/s12039-012-0231-7
54 A. S. Parmar and M. Muschol, Hydration and hydrodynamic interactions of lysozyme: effects of chaotropic versus kosmotropic ions, Biophysical Journal 97, 590 (2009)
https://doi.org/10.1016/j.bpj.2009.04.045
55 A. Bizzarri, S. Cannistraro, Molecular dynamics of water at the protein-solvent interface, J. Phys. Chem. B 106, 6617 (2002)
https://doi.org/10.1021/jp020100m
56 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)
https://doi.org/10.1021/jp9839044
57 J. H. Simpson and H. Y. Carr, Diffusion and Nuclear Spin Relaxation in Water, Phys. Rev. 111, 1201 (1958)
https://doi.org/10.1103/PhysRev.111.1201
58 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)
59 D. W. G. Smith and J. G. Powles, Proton spin-lattice relaxation in liquid water and liquid ammonia, Mol. Phys. 10, 451 (1966)
https://doi.org/10.1080/00268976600100571
60 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)
https://doi.org/10.1063/1.433995
61 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)
https://doi.org/10.1063/1.434878
62 N. Bloembergen, E. M. Purcell, and R. V. Pound, Relaxation effects in nuclear magnetic resonance absorption, Phys. Rev. 73, 679 (1948)
https://doi.org/10.1103/PhysRev.73.679
63 B. Halle and M. Davidovic, Biomolecular hydration: From water dynamics to hydrodynamics, Proc. Natl. Acad. Sci. USA 100, 12135 (2003)
https://doi.org/10.1073/pnas.2033320100
64 http://webbook.nist.gov/chemistry/fluid/
[1] Domenico Mallamace, Sebastiano Vasi, Mauro Missori, Francesco Mallamace, Carmelo Corsaro. NMR investigation of degradation processes of ancient and modern paper at different hydration levels[J]. Front. Phys. , 2018, 13(1): 138202-.
[2] Carmelo Corsaro, Francesco Mallamace, Sebastiano Vasi, Sow-Hsin Chen, H. Eugene Stanley, Domenico Mallamace. Contrasting microscopic interactions determine the properties of water/methanol solutions[J]. Front. Phys. , 2018, 13(1): 138201-.
[3] Margherita De Marzio, Gaia Camisasca, Mauro Rovere, Paola Gallo. Fragile to strong crossover and Widom line in supercooled water: A comparative study[J]. Front. Phys. , 2018, 13(1): 136103-.
[4] Francesco Mallamace,Carmelo Corsaro,Domenico Mallamace,Cirino Vasi,Nicola Cicero,H. Eugene Stanley. Water and lysozyme: Some results from the bending and stretching vibrational modes[J]. Front. Phys. , 2015, 10(5): 106105-.
[5] Chun Li, Zheng-Lin Jia, Dong-Cheng Mei. Effects of correlation time between noises on the noise enhanced stability phenomenon in an asymmetric bistable system[J]. Front. Phys. , 2015, 10(1): 100501-.
[6] A. M. Mounce, S. Oh, W. P. Halperin. Nuclear magnetic resonance studies of vortices in high temperature superconductors[J]. Front. Phys. , 2011, 6(4): 450-462.
[7] Xin-hua PENG (彭新华), Dieter SUTER, . Spin qubits for quantum simulations [J]. Front. Phys. , 2010, 5(1): 1-25.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed