Advertisement

European Biophysics Journal

, Volume 41, Issue 4, pp 361–367 | Cite as

Bio-protective effects of homologous disaccharides on biological macromolecules

  • S. MagazùEmail author
  • F. Migliardo
  • A. Benedetto
  • R. La Torre
  • L. Hennet
ORIGINAL PAPER

Abstract

In this contribution the effects of the homologous disaccharides trehalose and sucrose on both water and hydrated lysozyme dynamics are considered by determining the mean square displacement (MSD) from elastic incoherent neutron scattering (EINS) experiments. The self-distribution function (SDF) procedure is applied to the data collected, by use of IN13 and IN10 spectrometers (Institute Laue Langevin, France), on trehalose and sucrose aqueous mixtures (at a concentration corresponding to 19 water molecules per disaccharide molecule), and on dry and hydrated (H2O and D2O) lysozyme also in the presence of the disaccharides. As a result, above the glass transition temperature of water, the MSD of the water–trehalose system is lower than that of the water–sucrose system. This result suggests that the hydrogen-bond network of the water–trehalose system is stronger than that of the water–sucrose system. Furthermore, by taking into account instrumental resolution effects it was found that the system relaxation time of the water–trehalose system is longer than that of the water–sucrose system, and the system relaxation time of the protein in a hydrated environment in the presence of disaccharides increases sensitively. These results explain the higher bioprotectant effectiveness of trehalose. Finally, the partial MSDs of sucrose/water and trehalose/water have been evaluated. It clearly emerges from the analysis that these are almost equivalent in the low-Q domain (0–1.7 Å−1) but differ substantially in the high-Q range (1.7–4 Å−1). These findings reveal that the lower structural sensitivity of trehalose to thermal changes is connected with the local spatial scale.

Keywords

Bioprotection Biological molecules Homologous disaccharides Lysozyme Water Elastic incoherent neutron scattering 

Notes

Acknowledgments

The authors wish to acknowledge Le STUDIUM for strong support of this research. The Institut Laue-Langevin (ILL), Grenoble, France, is also acknowledged for beam time on the IN10 and IN13 spectrometers. A special acknowledgement is addressed to Dr C. Mondelli and Dr M.A. Gonzalez for precious discussions and guiding support during these experiments.

References

  1. Affouard F, Bordat P, Descamps M, Lerbret A, Magazù S, Migliardo F, Ramirez-Cuesta AJ, Telling MFT (2005) A combined neutron scattering and simulation study on bioprotectant systems. Chem Phys 317:258–266. doi: 10.1016/j.chemphys.2005.05.033 Google Scholar
  2. Becker T, Smith JC (2003) Energy resolution and dynamical heterogeneity effects on elastic incoherent neutron scattering from molecular systems. Phys Rev E 67:021904–021908. doi: 10.1103/PhysRevE.67.021904 CrossRefGoogle Scholar
  3. Becker T, Hayward JA, Finney JL, Daniel RM, Smith JC (2004) Neutron frequency windows and the protein dynamical transition. Biophys J 87:1436–1444. doi: 10.1529/biophysj.104.042226 PubMedCrossRefGoogle Scholar
  4. Bellavia G, Giuffrida S, Cottone G, Cupane A, Cordone L (2011) Protein thermal denaturation and matrix glass transition in different protein–trehalose–water systems. J Phys Chem B 115:6340–6346. doi: 10.1021/jp201378y PubMedCrossRefGoogle Scholar
  5. Branca C, Magazù S, Maisano G, Bennington SM, Fak B (2003) Vibrational studies on disaccharide/H2O systems by inelastic neutron scattering, Raman, and IR spectroscopy. J Phys Chem B 107:1444–1451. doi: 10.1021/jp026255b CrossRefGoogle Scholar
  6. 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 121:1978–1983. doi: 10.1063/1.1764491 PubMedCrossRefGoogle Scholar
  7. Careri G (1998) Cooperative charge fluctuations by migrating protons in globular proteins. Prog Biophys Mol Biol 70:223–249. doi: 10.1016/S0079-6107(98)00030-3 Google Scholar
  8. Chen SH, 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. doi: 10.1073/pnas.0602474103 PubMedCrossRefGoogle Scholar
  9. Ciliberti S, De Los Rios P, Piazza F (2006) Glasslike structure of globular proteins and the boson peak. Phys Rev Lett 96:198103–198104. doi: 10.1103/PhysRevLett.96.198103 PubMedCrossRefGoogle Scholar
  10. Di Fonzo S, Masciovecchio C, Bencivenga F, Gessini A, Fioretto D, Comez L, Morresi A, Gallina ME, De Giacomo O, Cesàro A (2011) Concentration–temperature dependencies of structural relaxation time in trehalose–water solutions by Brillouin inelastic UV scattering. J Phys Chem A 111:12577–12583. doi: 0.1021/jp075982 CrossRefGoogle Scholar
  11. Doster W (2007) The dynamical transition of proteins, concepts and misconceptions. Eur Biophys J 37:591–602. doi: 10.1007/s00249-008-0274-3 CrossRefGoogle Scholar
  12. Doster W, Cusak S, Petry W (1989) Dynamical transition of myoglobin revealed by inelastic neutron scattering. Nature 337:754–756. doi: 10.1038/337754a0 PubMedCrossRefGoogle Scholar
  13. Doster W, Busch S, Gasper AM, Appavou MS, Wuttke J, Scheer H (2010) Dynamical transition of protein-hydration water. Phys Rev Lett 104:098101–098104. doi: 10.1103/PhysRevLett.104.098101 PubMedCrossRefGoogle Scholar
  14. Gabel F, Bellissent-Funel MC (2007) C-phycocyanin hydration water dynamics in the presence of trehalose: an incoherent elastic neutron scattering study at different energy resolutions. Biophys J 92:4054–4063. doi: 10.1529/biophysj.105.061028 PubMedCrossRefGoogle Scholar
  15. Gregory RB (1995) Protein-solvent interactions. Dekker, New YorkGoogle Scholar
  16. Khodadadi S, Pawlus S, Roh JH, Garcia Sakai V, Mamontov E, Sokolov AP (2008) The origin of the dynamic transition in proteins. J Chem Phys 128:195106. doi: 10.1063/1.2927871 PubMedCrossRefGoogle Scholar
  17. Kneller GR, Calandrini V (2007) Estimating the influence of finite instrumental resolution on elastic neutron scattering intensities from proteins. J Chem Phys 126:125107–125108. doi: 10.1063/1.2711207 PubMedCrossRefGoogle Scholar
  18. Kneller GR, Hinsen K (2009) Quantitative model for the heterogeneity of atomic position fluctuations in proteins: a simulation study. J Chem Phys 131:045104–045106. doi: 10.1063/1.3170941 PubMedCrossRefGoogle Scholar
  19. Lee AL, Wand J (2001) Microscopic origins of entropy, heat capacity and the glass transition in proteins. Nature 411:501–504. doi: 10.1038/35078119 PubMedCrossRefGoogle Scholar
  20. Lelong G, Price DL, Brady JW, Saboungi ML (2007) Dynamics of trehalose molecules in confined solutions. J Chem Phys 127:065102–065106. doi: 10.1063/1.2753841 PubMedCrossRefGoogle Scholar
  21. Magazù S (1996) IQENS—dynamic light scattering complementarity on hydrogenous systems. Physica B 226:92–106. doi: 10.1016/0921-4526(96)00255-4 CrossRefGoogle Scholar
  22. Magazù S, Migliardo F, Telling MFT (2006) α, α-Trehalose-water solutions. VIII. Study of the diffusive dynamics of water by high-resolution quasi elastic neutron scattering. J Phys Chem B 110:1020–1025. doi: 10.1021/jp0536450 PubMedCrossRefGoogle Scholar
  23. Magazù S, Maisano G, Migliardo F, Galli G, Benedetto A, Morineau D, Affouard F, Descamps M (2008) Characterization of molecular motions in biomolecular systems by elastic incoherent neutron scattering. J Chem Phys 129:155103–155108. doi: 10.1063/1.2989804 PubMedCrossRefGoogle Scholar
  24. Magazù S, Maisano G, Migliardo F, Benedetto A (2009) Biomolecular motion characterization by a self-distribution-function procedure in elastic incoherent neutron scattering. Phys Rev E 79:041915–041919. doi: 10.1103/PhysRevE.79.041915 CrossRefGoogle Scholar
  25. Magazù S, Maisano G, Migliardo F, Benedetto A (2010a) Motion characterization by self-distribution function procedure. Biochim et Biophys Acta 1804:49–55. doi: 10.1016/j.bbapap.2009.09.017 Google Scholar
  26. Magazù S, Migliardo F, Affouard F, Descamps M, Telling TF (2010b) Study of the relaxational and vibrational dynamics of bioprotectant glass-forming mixtures by neutron scattering and molecular dynamics simulation. J Chem Phys 132:184512–184519. doi: 10.1063/1.3407428 CrossRefGoogle Scholar
  27. Magazù S, Migliardo F, Benedetto A (2010c) Mean square displacements from elastic incoherent neutron scattering evaluated by spectrometers working with different energy resolution on dry and hydrated (H2O and D2O) lysozyme. J Phys Chem B 114:9268–9274. doi: 10.1021/jp102436y PubMedCrossRefGoogle Scholar
  28. Magazù S, Migliardo F, Benedetto A (2011a) Puzzle of protein dynamical transition. J Phys Chem B 115:7736–7743. doi: 10.1021/jp111421m PubMedCrossRefGoogle Scholar
  29. Magazù S, Migliardo F, Benedetto A, Mondelli C, Gonzalez M (2011b) Thermal behaviour of hydrated lysozyme in the presence of sucrose and trehalose by EINS. J Non Cryst Sol 357:664–670. doi: 10.1016/j.jnoncrysol.2010.06.075 Google Scholar
  30. Magazù S, Migliardo F, Benedetto A (2011c) Elastic incoherent neutron scattering operating by varying instrumental energy resolution: principle, simulations and experiments of the resolution elastic neutron scattering (RENS). Rev Sci Instr 82:105115-1–105115-11Google Scholar
  31. Meinhold L, Clement D, Tehei M, Daniel R, Finney JL, Smith JC (2008) Protein dynamics and stability: the distribution of atomic fluctuations in thermophilic and mesophilic dihydrofolate reductase derived using elastic incoherent neutron scattering. Biophys J 92:4812–4818. doi: 10.1529/biophysj.107.121418 CrossRefGoogle Scholar
  32. Piazza F, De Los Rios P, Sanejouand YH (2005) Slow energy relaxation of macromolecules and nanoclusters in solution. Phys Rev Lett 94:145502–145504. doi: 10.1103/PhysRevLett.94.145502 PubMedCrossRefGoogle Scholar
  33. 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. doi: 10.1038/357423a0 PubMedCrossRefGoogle Scholar
  34. Smith LJ, Price DL, Chowdhuri Z, Brady JW, Saboungi ML (2004) Molecular dynamics of glucose in solution: a quasielastic neutron scattering study. J Chem Phys 120:3527. doi: 10.1063/1.1648302 PubMedCrossRefGoogle Scholar
  35. Sokolov AP, Roh JH, Mamontov E, Garcia Sakai V (2008) Role of hydration water in dynamics of biological macromolecules. Chem Phys 345:212–218. doi: 10.1016/j.chemphys.2007.07.013 CrossRefGoogle Scholar
  36. Talon C, Smith LJ, Brady JW, Lewis BA, Copley JRD, Price DL, Saboungi ML (2004) Dynamics of water molecules in glucose solutions. J Phys Chem B 108:5120–5126. doi: 10.1021/jp035161e CrossRefGoogle Scholar
  37. Tokuhisa A, Joti Y, Nakagawa H, Kitao A, Kataoka M (2007) Non-Gaussian behavior of elastic incoherent neutron scattering profiles of proteins studied by molecular dynamics simulation. Phys Rev E 75:041912–041918. doi: 10.1103/PhysRevE.75.041912 CrossRefGoogle Scholar
  38. Van Hove L (1954) Correlations in space and time and born approximation scattering in systems of interacting particles. Phys Rev 95:249–262. doi: 10.1103/PhysRev.95.249 CrossRefGoogle Scholar
  39. Zaccai G (2000) How soft is a protein? A protein dynamics force constant measured by neutron scattering. Science 288:1604–1607. doi: 10.1126/science.288.5471.1604 PubMedCrossRefGoogle Scholar

Copyright information

© European Biophysical Societies' Association 2011

Authors and Affiliations

  • S. Magazù
    • 1
    Email author
  • F. Migliardo
    • 1
  • A. Benedetto
    • 1
  • R. La Torre
    • 2
  • L. Hennet
    • 3
  1. 1.Department of PhysicsUniversity of MessinaS. Agata, MessinaItaly
  2. 2.Department of Matter Physics and Electronic EngineeringUniversity of MessinaS. Agata, MessinaItaly
  3. 3.CEMHTI and University of OrléansOrléans Cedex 02France

Personalised recommendations