Dynamical Coupling of Intrinsically Disordered Proteins and Their Hydration Water: Comparison with Folded Soluble and Membrane Proteins
Identifieur interne : 000F40 ( Ncbi/Curation ); précédent : 000F39; suivant : 000F41Dynamical Coupling of Intrinsically Disordered Proteins and Their Hydration Water: Comparison with Folded Soluble and Membrane Proteins
Auteurs : F.-X. Gallat [France] ; A. Laganowsky [États-Unis] ; K. Wood [Australie] ; F. Gabel [France] ; L. Van Eijck [France] ; J. Wuttke [Allemagne] ; M. Moulin [France] ; M. H Rtlein [France] ; D. Eisenberg [États-Unis] ; J.-P. Colletier [France] ; G. Zaccai [France] ; M. Weik [France]Source :
- Biophysical Journal [ 0006-3495 ] ; 2012.
Abstract
Hydration water is vital for various macromolecular biological activities, such as specific ligand recognition, enzyme activity, response to receptor binding, and energy transduction. Without hydration water, proteins would not fold correctly and would lack the conformational flexibility that animates their three-dimensional structures. Motions in globular, soluble proteins are thought to be governed to a certain extent by hydration-water dynamics, yet it is not known whether this relationship holds true for other protein classes in general and whether, in turn, the structural nature of a protein also influences water motions. Here, we provide insight into the coupling between hydration-water dynamics and atomic motions in intrinsically disordered proteins (IDP), a largely unexplored class of proteins that, in contrast to folded proteins, lack a well-defined three-dimensional structure. We investigated the human IDP tau, which is involved in the pathogenic processes accompanying Alzheimer disease. Combining neutron scattering and protein perdeuteration, we found similar atomic mean-square displacements over a large temperature range for the tau protein and its hydration water, indicating intimate coupling between them. This is in contrast to the behavior of folded proteins of similar molecular weight, such as the globular, soluble maltose-binding protein and the membrane protein bacteriorhodopsin, which display moderate to weak coupling, respectively. The extracted mean square displacements also reveal a greater motional flexibility of IDP compared with globular, folded proteins and more restricted water motions on the IDP surface. The results provide evidence that protein and hydration-water motions mutually affect and shape each other, and that there is a gradient of coupling across different protein classes that may play a functional role in macromolecular activity in a cellular context.
Url:
DOI: 10.1016/j.bpj.2012.05.027
PubMed: 22828339
PubMed Central: 3388209
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<wicri:regionArea>Institut Laue-Langevin, Grenoble</wicri:regionArea>
<placeName><region type="region">Auvergne-Rhône-Alpes</region>
<region type="old region">Rhône-Alpes</region>
<settlement type="city">Grenoble</settlement>
</placeName>
</affiliation>
</author>
<author><name sortKey="Wuttke, J" sort="Wuttke, J" uniqKey="Wuttke J" first="J." last="Wuttke">J. Wuttke</name>
<affiliation wicri:level="1"><nlm:aff id="aff9">Forschungszentrum Jülich, Jülich Center for Neutron Science at FRM II, Garching, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Forschungszentrum Jülich, Jülich Center for Neutron Science at FRM II, Garching</wicri:regionArea>
<wicri:noRegion>Garching</wicri:noRegion>
<wicri:noRegion>Garching</wicri:noRegion>
<wicri:noRegion>Garching</wicri:noRegion>
</affiliation>
</author>
<author><name sortKey="Moulin, M" sort="Moulin, M" uniqKey="Moulin M" first="M." last="Moulin">M. Moulin</name>
<affiliation wicri:level="3"><nlm:aff id="aff4">Institut Laue-Langevin, Grenoble, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Institut Laue-Langevin, Grenoble</wicri:regionArea>
<placeName><region type="region">Auvergne-Rhône-Alpes</region>
<region type="old region">Rhône-Alpes</region>
<settlement type="city">Grenoble</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3"><nlm:aff id="aff5">Institut Laue-Langevin/European Molecular Biology Laboratory Deuteration Laboratory, Partnership for Structural Biology, Grenoble, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Institut Laue-Langevin/European Molecular Biology Laboratory Deuteration Laboratory, Partnership for Structural Biology, Grenoble</wicri:regionArea>
<placeName><region type="region">Auvergne-Rhône-Alpes</region>
<region type="old region">Rhône-Alpes</region>
<settlement type="city">Grenoble</settlement>
</placeName>
</affiliation>
</author>
<author><name sortKey="H Rtlein, M" sort="H Rtlein, M" uniqKey="H Rtlein M" first="M." last="H Rtlein">M. H Rtlein</name>
<affiliation wicri:level="3"><nlm:aff id="aff4">Institut Laue-Langevin, Grenoble, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Institut Laue-Langevin, Grenoble</wicri:regionArea>
<placeName><region type="region">Auvergne-Rhône-Alpes</region>
<region type="old region">Rhône-Alpes</region>
<settlement type="city">Grenoble</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3"><nlm:aff id="aff5">Institut Laue-Langevin/European Molecular Biology Laboratory Deuteration Laboratory, Partnership for Structural Biology, Grenoble, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Institut Laue-Langevin/European Molecular Biology Laboratory Deuteration Laboratory, Partnership for Structural Biology, Grenoble</wicri:regionArea>
<placeName><region type="region">Auvergne-Rhône-Alpes</region>
<region type="old region">Rhône-Alpes</region>
<settlement type="city">Grenoble</settlement>
</placeName>
</affiliation>
</author>
<author><name sortKey="Eisenberg, D" sort="Eisenberg, D" uniqKey="Eisenberg D" first="D." last="Eisenberg">D. Eisenberg</name>
<affiliation wicri:level="2"><nlm:aff id="aff7">Department of Energy Institute of Genomics and Proteomics, University of California, Los Angeles, California</nlm:aff>
<country>États-Unis</country>
<placeName><region type="state">Californie</region>
</placeName>
<wicri:cityArea>Department of Energy Institute of Genomics and Proteomics, University of California, Los Angeles</wicri:cityArea>
</affiliation>
</author>
<author><name sortKey="Colletier, J P" sort="Colletier, J P" uniqKey="Colletier J" first="J.-P." last="Colletier">J.-P. Colletier</name>
<affiliation wicri:level="3"><nlm:aff id="aff1">Comissariat à l'Energie Atomique, Institut de Biologie Structurale, Grenoble, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Comissariat à l'Energie Atomique, Institut de Biologie Structurale, Grenoble</wicri:regionArea>
<placeName><region type="region">Auvergne-Rhône-Alpes</region>
<region type="old region">Rhône-Alpes</region>
<settlement type="city">Grenoble</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3"><nlm:aff id="aff2">Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5075, Grenoble, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5075, Grenoble</wicri:regionArea>
<placeName><region type="region">Auvergne-Rhône-Alpes</region>
<region type="old region">Rhône-Alpes</region>
<settlement type="city">Grenoble</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="4"><nlm:aff id="aff3">Université Joseph Fourier, Grenoble, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Université Joseph Fourier, Grenoble</wicri:regionArea>
<placeName><region type="region">Auvergne-Rhône-Alpes</region>
<region type="old region">Rhône-Alpes</region>
<settlement type="city">Grenoble</settlement>
</placeName>
<orgName type="university">Université Joseph Fourier</orgName>
</affiliation>
</author>
<author><name sortKey="Zaccai, G" sort="Zaccai, G" uniqKey="Zaccai G" first="G." last="Zaccai">G. Zaccai</name>
<affiliation wicri:level="3"><nlm:aff id="aff1">Comissariat à l'Energie Atomique, Institut de Biologie Structurale, Grenoble, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Comissariat à l'Energie Atomique, Institut de Biologie Structurale, Grenoble</wicri:regionArea>
<placeName><region type="region">Auvergne-Rhône-Alpes</region>
<region type="old region">Rhône-Alpes</region>
<settlement type="city">Grenoble</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3"><nlm:aff id="aff2">Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5075, Grenoble, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5075, Grenoble</wicri:regionArea>
<placeName><region type="region">Auvergne-Rhône-Alpes</region>
<region type="old region">Rhône-Alpes</region>
<settlement type="city">Grenoble</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="4"><nlm:aff id="aff3">Université Joseph Fourier, Grenoble, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Université Joseph Fourier, Grenoble</wicri:regionArea>
<placeName><region type="region">Auvergne-Rhône-Alpes</region>
<region type="old region">Rhône-Alpes</region>
<settlement type="city">Grenoble</settlement>
</placeName>
<orgName type="university">Université Joseph Fourier</orgName>
</affiliation>
<affiliation wicri:level="3"><nlm:aff id="aff4">Institut Laue-Langevin, Grenoble, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Institut Laue-Langevin, Grenoble</wicri:regionArea>
<placeName><region type="region">Auvergne-Rhône-Alpes</region>
<region type="old region">Rhône-Alpes</region>
<settlement type="city">Grenoble</settlement>
</placeName>
</affiliation>
</author>
<author><name sortKey="Weik, M" sort="Weik, M" uniqKey="Weik M" first="M." last="Weik">M. Weik</name>
<affiliation wicri:level="3"><nlm:aff id="aff1">Comissariat à l'Energie Atomique, Institut de Biologie Structurale, Grenoble, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Comissariat à l'Energie Atomique, Institut de Biologie Structurale, Grenoble</wicri:regionArea>
<placeName><region type="region">Auvergne-Rhône-Alpes</region>
<region type="old region">Rhône-Alpes</region>
<settlement type="city">Grenoble</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="3"><nlm:aff id="aff2">Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5075, Grenoble, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Centre National de la Recherche Scientifique, Unité Mixte de Recherche 5075, Grenoble</wicri:regionArea>
<placeName><region type="region">Auvergne-Rhône-Alpes</region>
<region type="old region">Rhône-Alpes</region>
<settlement type="city">Grenoble</settlement>
</placeName>
</affiliation>
<affiliation wicri:level="4"><nlm:aff id="aff3">Université Joseph Fourier, Grenoble, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>Université Joseph Fourier, Grenoble</wicri:regionArea>
<placeName><region type="region">Auvergne-Rhône-Alpes</region>
<region type="old region">Rhône-Alpes</region>
<settlement type="city">Grenoble</settlement>
</placeName>
<orgName type="university">Université Joseph Fourier</orgName>
</affiliation>
<affiliation wicri:level="3"><nlm:aff id="aff6">European Synchrotron Radiation Facility, Grenoble, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea>European Synchrotron Radiation Facility, Grenoble</wicri:regionArea>
<placeName><region type="region">Auvergne-Rhône-Alpes</region>
<region type="old region">Rhône-Alpes</region>
<settlement type="city">Grenoble</settlement>
</placeName>
</affiliation>
</author>
</analytic>
<series><title level="j">Biophysical Journal</title>
<idno type="ISSN">0006-3495</idno>
<idno type="eISSN">1542-0086</idno>
<imprint><date when="2012">2012</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass></textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"><p>Hydration water is vital for various macromolecular biological activities, such as specific ligand recognition, enzyme activity, response to receptor binding, and energy transduction. Without hydration water, proteins would not fold correctly and would lack the conformational flexibility that animates their three-dimensional structures. Motions in globular, soluble proteins are thought to be governed to a certain extent by hydration-water dynamics, yet it is not known whether this relationship holds true for other protein classes in general and whether, in turn, the structural nature of a protein also influences water motions. Here, we provide insight into the coupling between hydration-water dynamics and atomic motions in intrinsically disordered proteins (IDP), a largely unexplored class of proteins that, in contrast to folded proteins, lack a well-defined three-dimensional structure. We investigated the human IDP tau, which is involved in the pathogenic processes accompanying Alzheimer disease. Combining neutron scattering and protein perdeuteration, we found similar atomic mean-square displacements over a large temperature range for the tau protein and its hydration water, indicating intimate coupling between them. This is in contrast to the behavior of folded proteins of similar molecular weight, such as the globular, soluble maltose-binding protein and the membrane protein bacteriorhodopsin, which display moderate to weak coupling, respectively. The extracted mean square displacements also reveal a greater motional flexibility of IDP compared with globular, folded proteins and more restricted water motions on the IDP surface. The results provide evidence that protein and hydration-water motions mutually affect and shape each other, and that there is a gradient of coupling across different protein classes that may play a functional role in macromolecular activity in a cellular context.</p>
</div>
</front>
</TEI>
</record>
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