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The role of protein–solvent hydrogen bond dynamics in the structural relaxation of a protein in glycerol versus water

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Abstract

We used MD simulations to investigate the dependence of the dynamics of a soluble protein, RNase A, on temperature and solvent environment. Consistent with neutron scattering data, the simulations predict that the protein undergoes a dynamical transition in both glycerol and aqueous solutions that is absent in the dry protein. The temperature of the transition is higher, while the rate of increase with temperature of the amplitudes of motion on the 100 ps timescale is lower, in glycerol versus water. Analysis of the dynamics of hydrogen bonds revealed that the protein dynamical transition is connected to the relaxation of the protein–solvent hydrogen bond network, which, in turn, is associated with solvent translational diffusion. Thus, it appears that the role of solvent dynamics in affecting the protein dynamical transition is qualitatively similar in water and glycerol.

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References

  • Allen MP, Tildesley DJ (1989) Computer simulation of liquids. Clarendon, Oxford

    Google Scholar 

  • Andersen HC (1983) Rattle: a velocity version of the shake algorithm for molecular dynamics calculations. J Comp Phys 52:24–34

    Article  ADS  MATH  Google Scholar 

  • Beé M (1988) Quasielastic neutron scattering: principles and applications in solid state chemistry, biology, and materials science. Adam Hilger, Bristol

    Google Scholar 

  • Caliskan G, Kisliuk A, Sokolov AP (2002) Dynamic transition in lysozyme: role of a solvent. J Non-Cryst Solids 307:868–873

    Article  ADS  Google Scholar 

  • Caliskan G, Mechtani D, Roh JH, Kisliuk A, Sokolov AP, Azzam S, Cicerone MT, Lin-Gibson S, Peral I (2004) Protein and solvent dynamics: how strongly are they coupled? J Chem Phys 121:1978–1783

    Article  ADS  Google Scholar 

  • Chen S-H, Liu L, Fratini E, Baglioni P, Faraone A, Mamontov E (2006) Observation of fragile-to-strong dynamic crossover in protein hydration water. Proc Natl Acad Sci USA 103:9012–9016

    Article  ADS  Google Scholar 

  • Cornicchi E, Marconi M, Onori G, Paciaroni A (2006) Controlling the protein dynamical transition with sugar-based bioprotectant matrices: a neutron scattering study. Biophys J 91:289–297

    Article  Google Scholar 

  • Curtis JE, Dirama TE, Carri GA, Tobias DJ (2006) Inertial suppression of protein dynamics in a binary glycerol-trehalose glass. J Phys Chem B 110:22953–22956

    Article  Google Scholar 

  • Daniel RM, Dunn RV, Finney JL, Smith JC (2003) The role of dynamics in enzyme activity. Ann Rev Biophys Biomol Struct 32:69–92

    Article  Google Scholar 

  • Dioumaev AK, Lanyi JK (2007) Bacteriorhodopsin photocycle at cryogenic temperatures reveals distributed barriers of conformational substates. Proc Natl Acad Sci USA 104:9621–9626

    Article  ADS  Google Scholar 

  • Dirama TE, Carri GA, Sokolov AP (2005) Coupling between lysozyme and glycerol dynamics: microscopic insights from molecular dynamics simulations. J Chem Phys 122(24):244910

    Article  ADS  Google Scholar 

  • Doster W, Cusack S, Petry W (1989) Dynamical transition of myoglobin revealed by inelastic neutron scattering. Nature 337:754–756

    Article  ADS  Google Scholar 

  • Doster W, Cusack S, Petry W (1990) Dynamical instability of liquidlike motions in a globular protein observed by inelastic neutron scattering. Phys Rev Lett 65:1080–1083

    Article  ADS  Google Scholar 

  • Doster W, Settles M (1999) The dynamical transition in proteins: the role of hydrogen bonds. In: Bellissent-Funel M-C (ed) Hydration processes in biology: experimental and theoretical approaches, vol 305. IOS, Amsterdam, pp 177–191

    Google Scholar 

  • Doster W, Settles M (2005) Protein–water displacement distributions. Biochim Biophys Acta 1749:173–186

    Google Scholar 

  • Essmann U, Perera L, Berkowitz ML, Darden T, Pedersen LG (1995) A smooth particle mesh Ewald method. J Chem Phys 103:8577–8593

    Article  ADS  Google Scholar 

  • Fenimore PW, Frauenfelder H, McMahon B, Parak FG (2002) Slaving: solvent fluctuations dominate protein dynamics and function. Proc Natl Acad Sci USA 99:16047–16051

    Article  ADS  Google Scholar 

  • Fenimore PW, Frauenfelder H, McMahon B, Young RD (2004a) Bulk-solvent and hydration-shell fluctuations, similar to alpha- and beta-fluctuations in glasses, control protein motions and functions. Proc Natl Acad Sci USA 101:14408–14413

    Article  ADS  Google Scholar 

  • Fenimore PW, Frauenfelder H, McMahon BH, Young RD (2004b) Proteins are paradigms of stochastic complexity. Physica A 351:1–13

    Article  ADS  Google Scholar 

  • Finkelstein IJ, Massari AM, Fayer MD (2007) Viscosity-dependent protein dynamics. Biophys J 92:3652–3662

    Article  Google Scholar 

  • Frauenfelder H, Petsko GA, Tsernoglou D (1979) Temperature-dependent X-ray diffraction as a probe of protein structural dynamics. Nature 280:558–563

    Article  ADS  Google Scholar 

  • Frauenfelder H, Sligar SG, Wolynes PG (1991) The energy landscapes and motions of proteins. Science 254:1598–1603

    Article  ADS  Google Scholar 

  • Frauenfelder H, Fenimore PW, McMahon BH (2002) Hydration, slaving and protein function. Biophys Chem 98:35–48

    Article  Google Scholar 

  • Heberle J, Fitter J, Sass HJ, Büldt G (2000) Bacteriorhodopsin: the functional details of a molecular machine are being resolved. Biophys Chem 85:229–248

    Article  Google Scholar 

  • Knapp EE, Fischer SF, Parak F (1982) Protein dynamics from Mössbauer spectra: the temperature dependence. J Phys Chem 86:5042–5047

    Article  Google Scholar 

  • Kumar P, Yan Z, Xu L, Mazza MG, Buldryev SV, Chen S-H, Sastry S, Stanley HE (2006) Glass transition in biomolecules and the liquid–liquid critical point of water. Phys Rev Lett: 97(17):177802

    Article  ADS  Google Scholar 

  • Kurkal V, Daniel RM, Finney JL, Tehei M, Dunn RV, Smith JC (2005) Low frequency enzyme dynamics as a function of temperature and hydration: a neutron scattering study. Chem Phys 317:267–273

    Article  ADS  Google Scholar 

  • Lechner RE, Fitter J, Dencher NA, Hauss T (2006) Low-energy dynamics and biological function. Physica B 385–386:835–837

    Article  Google Scholar 

  • Lee AL, Wand AJ (2001) Microscopic origins of entropy, heat capacity and the glass transition in proteins. Nature 411:501–504

    Article  ADS  Google Scholar 

  • Luzar A, Chandler D (1996a) Effect of environment on hydrogen bond dynamics in liquid water. Phys Rev Lett 76:928–931

    Article  ADS  Google Scholar 

  • Luzar A, Chandler D (1996b) Hydrogen bond kinetics in liquid water. Nature 379:55–57

    Article  ADS  Google Scholar 

  • MacKerell Jr AD, Bashford D, Bellott M, Dunbrack Jr RL, Evanseck J, Field MJ, Fischer S, Gao J, Guo H, Ha S, Joseph-McCarthy D, Kuchnir L, Kuczera K, Lau FTK, Mattos C, Michnick S, Ngo T, Nguyen DT, Prodhom B, Reiher III WE, Roux B, Schlenkrich M, Smith JC, Stote R, Straub J, Watanabe M, Wiorkiewicz-Kuczera J, Yin D, Karplus M (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102:3586–3616

    Article  Google Scholar 

  • Martyna GJ, Tuckerman ME, Klein ML (1992) Nosé-Hoover chains: the canonical ensemble via continuous dynamics. J Chem Phys 97:2635–2643

    Article  ADS  Google Scholar 

  • Martyna GJ, Tobias DJ, Klein ML (1994) Constant pressure molecular dynamics simulations. J Chem Phys 101:4177–4189

    Article  ADS  Google Scholar 

  • Martyna GJ, Tuckerman ME, Tobias DJ, Klein ML (1996) Explicit reversible integrators for extended systems dynamics. Mol Phys 87:1117–1157

    Article  ADS  Google Scholar 

  • Paciaroni A, Cinelli S, Onori G (2002) Effect of the environment on the protein dynamical transition: a neutron scattering study. Biophys J 83:1157–1164

    Google Scholar 

  • Parak F (2003) Physical aspects of protein dynamics. Rep Prog Phys 66:103–129

    Article  ADS  Google Scholar 

  • Rasmussen BF, Stock AM, Ringe D, Petsko GA (1992) Crystalline ribonuclease A loses function below the dynamical transition at 220 K. Nature 357:423–424

    Article  ADS  Google Scholar 

  • Russo D, Hura GL, Copley JRD (2007) Effects of hydration water on protein methyl group dynamics in solution. Phys Rev E 75:040902

    Article  ADS  Google Scholar 

  • Ryckaert J-P, Ciccotti G, Berendsen HJC (1977) Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comp Phys 23:327–341

    Article  ADS  Google Scholar 

  • Smith J, Kuczera K, Karplus M (1990) Dynamics of myoglobin: comparison of simulation results with neutron scattering spectra. Proc Natl Acad Sci USA 90:9135–9139

    Google Scholar 

  • Swenson J, Jansson H, Bergman R (2006) Relaxation processes in supercooled confined water and implications for protein dynamics. Phys Rev Lett 96:247802

    Article  ADS  Google Scholar 

  • Tarek M, Tobias DJ (1999) Environmental dependence of the dynamics of protein hydration water. J Am Chem Soc 121:9740–9741

    Article  Google Scholar 

  • Tarek M, Tobias DJ (2000) The dynamics of protein hydration water: a quantitative comparison of molecular dynamics simulations and incoherent neutron scattering experiments. Biophys J 79:3244–3257

    Article  Google Scholar 

  • Tarek M, Martyna GJ, Tobias DJ (2000) Amplitudes and frequencies of protein dynamics: an analysis of discrepancies between neutron scattering and molecular dynamics simulations. J Am Chem Soc 102:10450–10451

    Article  Google Scholar 

  • Tarek M, Tobias DJ (2002) Role of protein–water hydrogen bond dynamics in the protein dynamical transition. Phys Rev Lett 88:138101

    Article  ADS  Google Scholar 

  • Tournier AL, Xu J, Smith JC (2003) Translational water dynamics drives the protein glass transition. Biophys J 85:1871–1875

    Google Scholar 

  • Tsai AM, Neumann DA, Bell LN (2000) Molecular dynamics of solid-state lysozyme as affected by glycerol and water: a neutron scattering study. Biophys J 79:2728–2732

    Google Scholar 

  • Tuckerman ME, Yarne DA, Samuelson SO, Hughes AL, Martyna GJ (2000) Exploiting multiple levels of parallelism in molecular dynamics based calculations via modern techniques and software paradigms. Comp Phys Comm 128:333

    Article  ADS  MATH  Google Scholar 

  • Wlodawer A, Svensson LA, Sjolin L, Gilliland G (1988) Structure of phosphate free ribonuclease A refined at 1.26 Å resolution. Biochemistry 27:2705–2717

    Article  Google Scholar 

  • Wood K, Frölich A, Paciaroni A, Moulin M, Härtlein M, Zaccaï G, Tobias DJ, Weik M (2008) Coincidence of dynamical transitions in a soluble protein and its hydration-water: direct measurements by neutron scattering and MD simulations. J Am Chem Soc 130:4586–4587

    Article  Google Scholar 

  • Wuttke J, Petry W, Coddens G, Fujara F (1995) Fast dynamics of glass-forming glycerol. Phys Rev E 52:4026–4034

    Article  ADS  Google Scholar 

  • Zanotti J-M, Bellissent-Funel MC, Chen SH (2005) Experimental evidence of a liquid–liquid transition in interfacial water. Europhys Lett 71:91–97

    Article  ADS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants CHE–0417158 and CHE-0750175 from the National Science Foundation.

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Authors and Affiliations

  1. Equipe de dynamique des assemblages membranaires, Unité mixte de recherche CNRS/UHP 7565, Université Henri Poincaré, BP 239, 54506, Vandoeuvre-lès-Nancy cedex, France

    Mounir Tarek

  2. Department of Chemistry, University of California, Irvine, CA, 92697-2025, USA

    Douglas J. Tobias

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  1. Mounir Tarek
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  2. Douglas J. Tobias
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Correspondence to Douglas J. Tobias.

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Advanced neutron scattering and complementary techniques to study biological systems. Contributions from the meetings, "Neutrons in Biology", STFC Rutherford Appleton Laboratory, Didcot, UK, 11–13 July and "Proteins At Work 2007", Perugia, Italy, 28–30 May 2007.

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Tarek, M., Tobias, D.J. The role of protein–solvent hydrogen bond dynamics in the structural relaxation of a protein in glycerol versus water. Eur Biophys J 37, 701–709 (2008). https://doi.org/10.1007/s00249-008-0324-x

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  • DOI: https://doi.org/10.1007/s00249-008-0324-x

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