Advertisement

Chinese Journal of Polymer Science

, Volume 37, Issue 11, pp 1083–1091 | Cite as

Combining Neutron Scattering, Deuteration Technique, and Molecular Dynamics Simulations to Study Dynamics of Protein and Its Surface Water Molecules

  • Li-Rong Zheng
  • Liang HongEmail author
Feature Article
  • 22 Downloads

Abstract

Protein internal dynamics is essential for its function. Exploring the internal dynamics of protein molecules as well as its connection to protein structure and function is a central topic in biophysics. However, the atomic motions in protein molecules exhibit a great degree of complexities. These complexities arise from the complex chemical composition and superposition of different types of atomic motions on the similar time scales, and render it challenging to explicitly understand the microscopic mechanism governing protein motions, functions, and their connections. Here, we demonstrate that, by using neutron scattering, molecular dynamics simulation, and deuteration technique, one can address this challenge to a large extent.

Keywords

Neutron scattering Deuteration techniques Molecular dynamics simulations Protein Hydration water Dynamics 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (Nos. 11504231 and 31630002), and the Innovation Program of Shanghai Municipal Education Commission. The authors acknowledge the Center for High Performance Computing at Shanghai Jiao Tong University for computing resources, and the student innovation center at Shanghai Jiao Tong University.

References

  1. 1.
    Johs, A.; Harwood, I. M.; Parks, J. M.; Nauss, R. E.; Smith, J. C.; Liang, L.; Miller, S. M. Structural characterization of intramolecular Hg2+ transfer between flexibly linked domains of mercuric ion reductase. J. Mol. Biol. 2011, 413, 639–656.CrossRefPubMedGoogle Scholar
  2. 2.
    Martin, G. S. The hunting of the Src. Nat. Rev. Mol. Cell. Biol. 2001, 2, 47–47.CrossRefGoogle Scholar
  3. 3.
    Banks, R. D.; Blake, C. C.; Evans, P. R.; Haser, R.; Rice, D. W.; Hardy, G. W.; Merrett, M.; Phillips, A. W. Sequence, structure and activity of phosphoglycerate kinase: A possible hinge-bending enzyme. Nature 1979, 279, 773–777.CrossRefPubMedGoogle Scholar
  4. 4.
    Rupley, J. A.; Careri, G. Protein hydration and function. In Advances in protein chemistry. Elsevier, 1991, Vol. 41, p. 37–172CrossRefPubMedGoogle Scholar
  5. 5.
    Bellissent-Funel, M. C.; Hassanali, A.; Havenith, M.; Henchman, R.; Pohl, P.; Sterpone, F.; van der Spoel, D.; Xu, Y.; Garcia, A. E. Water determines the structure and dynamics of proteins. Chem. Rev. 2016, 116, 7673–7679.CrossRefPubMedGoogle Scholar
  6. 6.
    Hans, F.; Guo, C.; Joel, B.; Fenimore, P. W.; Helén, J.; Mcmahon, B. H.; Stroe, I. R.; Jan, S.; Young, R. D. A unified model of protein dynamics. Proc. Natl. Acad. Sci. 2009, 106, 5129–5134.CrossRefGoogle Scholar
  7. 7.
    Biman, B. Water dynamics in the hydration layer around proteins and micelles. Chem. Rev. 2005, 105, 3197–3219.CrossRefGoogle Scholar
  8. 8.
    Ball, P. Water and life: Seeking the solution. Nature 2005, 436, 1084–1085.CrossRefPubMedGoogle Scholar
  9. 9.
    Pocker, Y. Water in enzyme reactions: Biophysical aspects of hydration-dehydration processes. Cell. Mol. Life Sci. 2000, 57, 1008–1017.CrossRefPubMedGoogle Scholar
  10. 10.
    Jian, P.; Todd, S.; Ning, Z.; Catterall, W. A. The crystal structure of a voltage-gated sodium channel. Nature 2011, 475, 353–358.CrossRefGoogle Scholar
  11. 11.
    Pawlus, S.; Khodadadi, S.; Sokolov, A. P. Conductivity in hydrated proteins: No signs of the fragile-to-strong crossover. Phys. Rev. Lett. 2008, 100, 2197–2204.CrossRefGoogle Scholar
  12. 12.
    Otting, G.; Liepinsh, E.; Wuthrich, K. Protein hydration in aqueous solution. Science 1991, 254, 974–980.CrossRefPubMedGoogle Scholar
  13. 13.
    Valeria, C. N.; Martina, H. New insights into the role of water in biological function: Studying solvated biomolecules using terahertz absorption spectroscopy in conjunction with molecular dynamics simulations. J. Am. Chem. Soc. 2014, 136, 12800–12807.CrossRefGoogle Scholar
  14. 14.
    Yang, J.; Wang, Y.; Wang, L.; Zhong, D. Mapping hydration dynamics around a β-barrel protein. J. Am. Chem. Soc. 2017, 139, 4399–4408.CrossRefPubMedGoogle Scholar
  15. 15.
    Chen, C.; Stevens, B.; Kaur, J.; Cabral, D.; Liu, H.; Wang, Y.; Zhang, H.; Rosenblum, G.; Smilansky, Z.; Goldman, Y. E. Single-molecule fluorescence measurements of ribosomal translocation dynamics. Mol. Cell 2011, 42, 367–377.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Hong, L.; Jain, N.; Cheng, X.; Bernal, A.; Tyagi, M.; Smith, J. C. Determination of functional collective motions in a protein at atomic resolution using coherent neutron scattering. Sci. Adv. 2016, 2, e1600886.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Hong, L.; Sharp, M. A.; Poblete, S.; Biehl, R.; Zamponi, M.; Szekely, N.; Appavou, M. S.; Winkler, R. G.; Nauss, R. E.; Johs, A.; Parks, J. M.; Yi, Z.; Cheng, X.; Liang, L.; Ohl, M.; Miller, S. M.; Richter, D.; Gompper, G.; Smith, J. C. Structure and dynamics of a compact state of a multidomain protein, the mercuric ion reductase. Biophys. J. 2014, 107, 393–400.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Hong, L.; Smolin, N.; Lindner, B.; Sokolov, A. P.; Smith, J. C. Three classes of motion in the dynamic neutron-scattering susceptibility of a globular protein. Phys. Rev. Lett. 2011, 107, 148102.CrossRefPubMedGoogle Scholar
  19. 19.
    Hong, L.; Smolin, N.; Smith, J. C. de Gennes narrowing describes the relative motion of protein domains. Phys. Rev. Lett. 2014, 112, 158102.CrossRefPubMedGoogle Scholar
  20. 20.
    Liu, Z.; Huang, J.; Tyagi, M.; O'Neill, H.; Zhang, Q.; Mamontov, E.; Jain, N.; Wang, Y.; Zhang, J.; Smith, J. C.; Hong, L. Dynamical transition of collective motions in dry proteins. Phys. Rev. Lett. 2017, 119, 048101.CrossRefPubMedGoogle Scholar
  21. 21.
    Nickels, J. D.; O'Neill, H.; Hong, L.; Tyagi, M.; Ehlers, G.; Weiss, K. L.; Zhang, Q.; Yi, Z.; Mamontov, E.; Smith, J. C.; Sokolov, A. P. Dynamics of protein and its hydration water: Neutron scattering studies on fully deuterated GFP. Biophys. J. 2012, 103, 1566–1575.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Tan, P.; Liang, Y.; Xu, Q.; Mamontov, E.; Li, J.; Xing, X.; Hong, L. Gradual crossover from subdiffusion to normal diffusion: A many-body effect in protein surface water. Phys. Rev. Lett. 2018, 120, 248101.CrossRefPubMedGoogle Scholar
  23. 23.
    Hong, L.; Cheng, X.; Glass, D. C.; Smith, J. C. Surface hydration amplifies single-well protein atom diffusion propagating into the macromolecular core. Phys. Rev. Lett. 2012, 108, 238102.CrossRefPubMedGoogle Scholar
  24. 24.
    Hong, L.; Glass, D. C.; Nickels, J. D.; Perticaroli, S.; Yi, Z.; Tyagi, M.; O'Neill, H.; Zhang, Q.; Sokolov, A. P.; Smith, J. C. Elastic and conformational softness of a globular protein. Phys. Rev. Lett. 2013, 110, 028104.CrossRefPubMedGoogle Scholar
  25. 25.
    Liu, Z.; Yang, C.; Huang, J.; Ciampalini, G.; Li, J.; García Sakai, V.; Tyagi, M.; O'Neill, H.; Zhang, Q.; Capaccioli, S.; Ngai, K. L.; Hong, L. Direct experimental characterization of contributions from self-motion of hydrogen and from interatomic motion of heavy atoms to protein anharmonicity. J. Phys. Chem. B 2018, 122, 9956–9961.CrossRefPubMedGoogle Scholar
  26. 26.
    Liu, Z.; Lemmonds, S.; Huang, J.; Tyagi, M.; Hong, L.; Jain, N. Entropic contribution to enhanced thermal stability in the thermostable P450 CYP119. Proc. Natl. Acad. Sci. 2018, 115, E10049–E10058.CrossRefPubMedGoogle Scholar
  27. 27.
    Buchenau, U.; Wischnewski, A.; Richter, D.; Frick, B. Is the fast process at the glass transition mainly due to long wavelength excitations? Phys. Rev. Lett. 1996, 77, 4035–4038.CrossRefGoogle Scholar
  28. 28.
    Nickels, J. D.; Perticaroli, S.; O'Neill, H.; Zhang, Q.; Ehlers, G.; Sokolov, A. P. Coherent neutron scattering and collective dynamics in the protein, GFP. Biophys. J. 2013, 105, 2182–2187.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Carpenter, J. M.; Pelizzari, C. A. Inelastic neutron scattering from amorphous solids. I. Calculation of the scattering law for model structures. Phys. Rev. B 1975, 12, 2391.Google Scholar
  30. 30.
    Suhre, K.; Sanejouand, Y. H. ElNémo: A normal mode web server for protein movement analysis and the generation of templates for molecular replacement. Nucleic Acids Res. 2004, 32, W610–W614.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Khodadadi, S.; Pawlus, S.; Sokolov, A. P. Influence of hydration on protein dynamics: Combining dielectric and neutron scattering spectroscopy data. J. Phys. Chem. B 2008, 112, 14273–14280.CrossRefPubMedGoogle Scholar
  32. 32.
    Modig, K.; Liepinsh, E.; Otting, G.; Halle, B. Dynamics of protein and peptide hydration. J. Am. Chem. Soc. 2004, 126, 102–114.CrossRefPubMedGoogle Scholar
  33. 33.
    Ebbinghaus, S.; Kim, S. J.; Heyden, M.; Yu, X.; Heugen, U.; Gruebele, M.; Leitner, D. M.; Havenith, M. An extended dynamical hydration shell around proteins. Proc. Natl. Acad. Sci. 2007, 104, 20749–20752.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    King, J. T.; Kubarych, K. J. Site-specific coupling of hydration water and protein flexibility studied in solution with ultrafast 2D-IR spectroscopy. J. Am. Chem. Soc. 2012, 134, 18705–18712.CrossRefPubMedGoogle Scholar
  35. 35.
    Vitkup, D.; Ringe, D.; Petsko, G. A.; Karplus, M. Solvent mobility and the protein ‘glass’ transition. Nat. Struct. Biol. 2000, 7, 34–38.CrossRefPubMedGoogle Scholar
  36. 36.
    Roh, J. H.; Curtis, J. E.; Azzam, S.; Novikov, V. N.; Peral, I.; Chowdhuri, Z.; Gregory, R. B.; Sokolov, A. P. Influence of hydration on the dynamics of lysozyme. Biophys. J. 2006, 91, 2573–2588.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Rasmussen, B. F.; Stock, A. M.; Ringe, D.; Petsko, G. A. Crystalline ribonuclease A loses function below the dynamic transition at 220 K. Nature 1992, 357, 423–424.CrossRefPubMedGoogle Scholar
  38. 38.
    He, Y.; Ku, P. I.; Knab, J. R.; Chen, J. Y.; Markelz, A. G. Protein dynamical transition does not require protein structure. Phys. Rev. Lett. 2008, 101, 178103.CrossRefPubMedGoogle Scholar
  39. 39.
    Ferrand, M.; Dianoux, A. J.; Petry, W.; Zaccaï, G. Thermal motions and function of bacteriorhodopsin in purple membranes: Effects of temperature and hydration studied by neutron scattering. Proc. Natl. Acad. Sci. 1993, 90, 9668–9672.CrossRefPubMedGoogle Scholar

Copyright information

© Chinese Chemical Society Institute of Chemistry, Chinese Academy of Sciences Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Physics and AstronomyShanghai Jiao Tong UniversityShanghaiChina
  2. 2.Institute of Natural SciencesShanghai Jiao Tong UniversityShanghaiChina

Personalised recommendations