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

Li-Rong Zheng; Liang Hong

doi:10.1007/s10118-019-2312-2

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

FEATURE ARTICLE | Updated：2021-02-18

- Combining Neutron Scattering, Deuteration Technique, and Molecular Dynamics Simulations to Study Dynamics of Protein and Its Surface Water Molecules
- Combining Neutron Scattering, Deuteration Technique, and Molecular Dynamics Simulations to Study Dynamics of Protein and Its Surface Water Molecules
- Chinese Journal of Polymer Science 2019年37卷第11期页码：1083-1091
- Affiliations：
  
  a.School of Physics and Astronomy, Shanghai Jiao Tong University, Shanghai 200240, China
  b.Institute of Natural Sciences, Shanghai Jiao Tong University, Shanghai 200240, China
- Author bio：
  
  hongl3liang@sjtu.edu.cn
- Funds：
  
  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.
- DOI：10.1007/s10118-019-2312-2
  中图分类号： M
- 收稿：2019-04-14，
  
  修回：2019-5-18，
  
  录用：2019-6-3，
  
  网络首发：2019-09-02，
  
  纸质出版：2019-11
- Accepted：
Scan QR Code
Zheng, L. R.; Hong, L. Combining neutron scattering, deuteration technique, and molecular dynamics simulations to study dynamics of protein and its surface water molecules. Chinese J. Polym. Sci. 2019, 37, 1083–1091.

Li-Rong Zheng, Liang Hong. Combining Neutron Scattering, Deuteration Technique, and Molecular Dynamics Simulations to Study Dynamics of Protein and Its Surface Water Molecules[J]. Chinese Journal of Polymer Science, 2019, 37(11): 1083-1091.
Zheng, L. R.; Hong, L. Combining neutron scattering, deuteration technique, and molecular dynamics simulations to study dynamics of protein and its surface water molecules. Chinese J. Polym. Sci. 2019, 37, 1083–1091. DOI： 10.1007/s10118-019-2312-2.

Li-Rong Zheng, Liang Hong. Combining Neutron Scattering, Deuteration Technique, and Molecular Dynamics Simulations to Study Dynamics of Protein and Its Surface Water Molecules[J]. Chinese Journal of Polymer Science, 2019, 37(11): 1083-1091. DOI： 10.1007/s10118-019-2312-2.

摘要

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.

关键词

Keywords

references

Johs, A.; Harwood, I. M.; Parks, J. M.; Nauss, R. E.; Smith, J. C.; Liang, L.; Miller, S. M . Structural characterization of intramolecular Hg 2+ transfer between flexibly linked domains of mercuric ion reductase . J. Mol. Biol. , 2011 . 413 ( 3 ): 639 - 656 . DOI: 10.1016/j.jmb.2011.08.042 http://doi.org/10.1016/j.jmb.2011.08.042 .

Martin, G. S . The hunting of the Src . Nat. Rev. Mol. Cell. Biol. , 2001 . 2 ( 5 ): 47 - 47 . DOI: 10.1038/35073094 http://doi.org/10.1038/35073094 .

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 ( 5716 ): 773 - 777 . DOI: 10.1038/279773a0 http://doi.org/10.1038/279773a0 .

Rupley, J. A.; Careri, G. Protein hydration and function. In Advances in protein chemistry . Elsevier, 1991 , Vol. 41, p. 37−172

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 ( 13 ): 7673 - 7679 . DOI: 10.1021/acs.chemrev.5b00664 http://doi.org/10.1021/acs.chemrev.5b00664 .

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 ( 13 ): 5129 - 5134 . DOI: 10.1073/pnas.0900336106 http://doi.org/10.1073/pnas.0900336106 .

Biman, B . Water dynamics in the hydration layer around proteins and micelles . Chem. Rev. , 2005 . 105 ( 9 ): 3197 - 3219 . DOI: 10.1021/cr020661+ http://doi.org/10.1021/cr020661+ .

Ball, P . Water and life: Seeking the solution . Nature , 2005 . 436 ( 7054 ): 1084 - 1085 . DOI: 10.1038/4361084a http://doi.org/10.1038/4361084a .

Pocker, Y . Water in enzyme reactions: Biophysical aspects of hydration-dehydration processes . Cell. Mol. Life Sci. , 2000 . 57 ( 7 ): 1008 - 1017 . DOI: 10.1007/PL00000741 http://doi.org/10.1007/PL00000741 .

Jian, P.; Todd, S.; Ning, Z.; Catterall, W. A . The crystal structure of a voltage-gated sodium channel . Nature , 2011 . 475 ( 7356 ): 353 - 358 . DOI: 10.1038/nature10238 http://doi.org/10.1038/nature10238 .

Pawlus, S.; Khodadadi, S.; Sokolov, A. P . Conductivity in hydrated proteins: No signs of the fragile-to-strong crossover . Phys. Rev. Lett. , 2008 . 100 ( 10 ): 2197 - 2204 . .

Otting, G.; Liepinsh, E.; Wuthrich, K . Protein hydration in aqueous solution . Science , 1991 . 254 ( 5034 ): 974 - 980 . DOI: 10.1126/science.1948083 http://doi.org/10.1126/science.1948083 .

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 ( 37 ): 12800 - 12807 . DOI: 10.1021/ja504441h http://doi.org/10.1021/ja504441h .

Yang, J.; Wang, Y.; Wang, L.; Zhong, D . Mapping hydration dynamics around a β -barrel protein . J. Am. Chem. Soc. , 2017 . 139 ( 12 ): 4399 - 4408 . DOI: 10.1021/jacs.6b12463 http://doi.org/10.1021/jacs.6b12463 .

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 ( 3 ): 367 - 377 . DOI: 10.1016/j.molcel.2011.03.024 http://doi.org/10.1016/j.molcel.2011.03.024 .

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 ( 10 ): e1600886 DOI: 10.1126/sciadv.1600886 http://doi.org/10.1126/sciadv.1600886 .

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 ( 2 ): 393 - 400 . DOI: 10.1016/j.bpj.2014.06.013 http://doi.org/10.1016/j.bpj.2014.06.013 .

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 ( 14 ): 148102 DOI: 10.1103/PhysRevLett.107.148102 http://doi.org/10.1103/PhysRevLett.107.148102 .

Hong, L.; Smolin, N.; Smith, J. C . de Gennes narrowing describes the relative motion of protein domains . Phys. Rev. Lett. , 2014 . 112 ( 15 ): 158102 DOI: 10.1103/PhysRevLett.112.158102 http://doi.org/10.1103/PhysRevLett.112.158102 .

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 ( 4 ): 048101 DOI: 10.1103/PhysRevLett.119.048101 http://doi.org/10.1103/PhysRevLett.119.048101 .

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 ( 7 ): 1566 - 1575 . DOI: 10.1016/j.bpj.2012.08.046 http://doi.org/10.1016/j.bpj.2012.08.046 .

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 ( 24 ): 248101 DOI: 10.1103/PhysRevLett.120.248101 http://doi.org/10.1103/PhysRevLett.120.248101 .

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 ( 23 ): 238102 DOI: 10.1103/PhysRevLett.108.238102 http://doi.org/10.1103/PhysRevLett.108.238102 .

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 ( 2 ): 028104 DOI: 10.1103/PhysRevLett.110.028104 http://doi.org/10.1103/PhysRevLett.110.028104 .

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 ( 43 ): 9956 - 9961 . DOI: 10.1021/acs.jpcb.8b09355 http://doi.org/10.1021/acs.jpcb.8b09355 .

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 ( 43 ): E10049 - E10058 . DOI: 10.1073/pnas.1807473115 http://doi.org/10.1073/pnas.1807473115 .

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 ( 19 ): 4035 - 4038 . DOI: 10.1103/PhysRevLett.77.4035 http://doi.org/10.1103/PhysRevLett.77.4035 .

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 ( 9 ): 2182 - 2187 . DOI: 10.1016/j.bpj.2013.09.029 http://doi.org/10.1016/j.bpj.2013.09.029 .

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 DOI: 10.1103/PhysRevB.12.2391 http://doi.org/10.1103/PhysRevB.12.2391 .

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 ( suppl_2, 1 ): W610 - W614 . .

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 ( 45 ): 14273 - 14280 . DOI: 10.1021/jp8059807 http://doi.org/10.1021/jp8059807 .

Modig, K.; Liepinsh, E.; Otting, G.; Halle, B . Dynamics of protein and peptide hydration . J. Am. Chem. Soc. , 2004 . 126 ( 1 ): 102 - 114 . DOI: 10.1021/ja038325d http://doi.org/10.1021/ja038325d .

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 ( 52 ): 20749 - 20752 . DOI: 10.1073/pnas.0709207104 http://doi.org/10.1073/pnas.0709207104 .

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 ( 45 ): 18705 - 18712 . DOI: 10.1021/ja307401r http://doi.org/10.1021/ja307401r .

Vitkup, D.; Ringe, D.; Petsko, G. A.; Karplus, M . Solvent mobility and the protein 'glass' transition . Nat. Struct. Biol. , 2000 . 7 ( 1 ): 34 - 38 . DOI: 10.1038/71231 http://doi.org/10.1038/71231 .

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 ( 7 ): 2573 - 2588 . DOI: 10.1529/biophysj.106.082214 http://doi.org/10.1529/biophysj.106.082214 .

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 ( 6377 ): 423 - 424 . DOI: 10.1038/357423a0 http://doi.org/10.1038/357423a0 .

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 ( 17 ): 178103 DOI: 10.1103/PhysRevLett.101.178103 http://doi.org/10.1103/PhysRevLett.101.178103 .

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 ( 20 ): 9668 - 9672 . DOI: 10.1073/pnas.90.20.9668 http://doi.org/10.1073/pnas.90.20.9668 .

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