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Bulk-solvent and hydration-shell fluctuations, similar to α- and β-fluctuations in glasses, control protein motions and functions

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Fenimore, P. W., Frauenfelder, Hans, McMahon, B. H., Young, R. D.·2004·Proceedings of the National Academy of Sciences
DOI 10.1073/pnas.0405573101PMC PMC521939
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Abstract

The concept that proteins exist in numerous different conformations or conformational substates, described by an energy landscape, is now accepted, but the dynamics is incompletely explored. We have previously shown that large-scale protein motions, such as the exit of a ligand from the protein interior, follow the dielectric fluctuations in the bulk solvent. Here, we demonstrate, by using mean-square displacements (msd) from Mössbauer and neutron-scattering experiments, that fluctuations in the hydration shell control fast fluctuations in the protein. We call the first type solvent-slaved or α-fluctuations and the second type hydration-shell-coupled or β-fluctuations. Solvent-slaved motions are similar to the α-fluctuations in glasses. Their temperature dependence can be approximated by a Vogel-Tammann-Fulcher relation and they are absent in a solid environment. Hydration-shell-coupled fluctuations are similar to the β-relaxation in glasses. They can be approximated by a Ferry or an Arrhenius relation, are much reduced or absent in dehydrated proteins, and occur in hydrated proteins even if embedded in a solid. They can be responsible for internal processes such as the migration of ligands within myoglobin. The existence of two functionally important fluctuations in proteins, one slaved to bulk motions and the other coupled to hydration-shell fluctuations, implies that the environment can control protein functions through different avenues and that no real protein transition occurs at ≈200 K. The large number of conformational substates is essential; proteins cannot function without this reservoir of entropy, which resides mainly in the hydration shell.

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Authors
Fenimore, P. W., Frauenfelder, H., McMahon, B. H., & Young, R. D.
Affiliations
Los Alamos National Laboratory (US)
Corresponding author
Frauenfelder, Hans
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
National Academy of Sciences
Published
2004-09-24
Volume
101
Issue
40
Pages
14408-14413
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
DOI
10.1073/pnas.0405573101
PMC
PMC521939
OpenAlex
W1977258623
Cited by
524
References
58
Citations by year
2026: 12 · 2025: 10 · 2024: 16 · 2023: 8 · 2022: 19 · 2021: 13 · 2020: 11 · 2019: 21 · 2018: 16 · 2017: 23 · 2016: 24 · 2015: 18 · 2014: 20 · 2013: 28 · 2012: 36
FWCI
9.02
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • U.S. Department of Energy (W-7405, W-7405-ENG-36)
  • Laboratory Directed Research and Development
  • Los Alamos National Laboratory (W‐7405‐ENG‐36)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
  • Physical Sciences › Materials Science › Materials Chemistry › Material Dynamics and Properties
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Electron Spin Resonance Studies
Keywords
protein dynamics, alpha relaxation, beta relaxation, glassy dynamics, protein energy landscape, conformational substates, ligand migration, myoglobin, Arrhenius relaxation, protein dehydration, dielectric fluctuations
MeSH terms
Animals, Glass, Ligands, Models, Molecular, Myoglobin, Protein Conformation, Proteins, Solvents, Thermodynamics, Water, Spectroscopy, Mossbauer, Neutron Diffraction, In Vitro Techniques

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