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NMR Meets Tau: Insights into Its Function and Pathology

Identifieur interne : 000654 ( Pmc/Curation ); précédent : 000653; suivant : 000655

NMR Meets Tau: Insights into Its Function and Pathology

Auteurs : Guy Lippens [France] ; Isabelle Landrieu ; Caroline Smet ; Isabelle Huvent ; Neha S. Gandhi ; Benoît Gigant ; Clément Despres ; Haoling Qi ; Juan Lopez [Pérou]

Source :

RBID : PMC:4919923

Abstract

In this review, we focus on what we have learned from Nuclear Magnetic Resonance (NMR) studies on the neuronal microtubule-associated protein Tau. We consider both the mechanistic details of Tau: the tubulin relationship and its aggregation process. Phosphorylation of Tau is intimately linked to both aspects. NMR spectroscopy has depicted accurate phosphorylation patterns by different kinases, and its non-destructive character has allowed functional assays with the same samples. Finally, we will discuss other post-translational modifications of Tau and its interaction with other cellular factors in relationship to its (dys)function.


Url:
DOI: 10.3390/biom6020028
PubMed: 27338491
PubMed Central: 4919923

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PMC:4919923

Le document en format XML

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<name sortKey="Gandhi, Neha S" sort="Gandhi, Neha S" uniqKey="Gandhi N" first="Neha S." last="Gandhi">Neha S. Gandhi</name>
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<nlm:aff id="af3-biomolecules-06-00028">School of Mathematical Sciences, Queensland University of Technology, Brisbane 4001 QLD, Australia;
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<name sortKey="Gigant, Benoit" sort="Gigant, Benoit" uniqKey="Gigant B" first="Benoît" last="Gigant">Benoît Gigant</name>
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<nlm:aff id="af4-biomolecules-06-00028">Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Sud, Université Paris-Saclay, Gif-sur-Yvette 91190, France;
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<name sortKey="Despres, Clement" sort="Despres, Clement" uniqKey="Despres C" first="Clément" last="Despres">Clément Despres</name>
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<nlm:aff id="af1-biomolecules-06-00028">Unité de Glycobiologie Structurale et Fontionnelle, University of Lille (UGSF), Villeneuve d’Ascq CNRS UMR Lille 8576, France;
<email>isabelle.landrieu@univ-lille1.fr</email>
(I.L.);
<email>caroline.smet@univ-lille1.fr</email>
(C.S.);
<email>isabelle.huvent@univ-lille1.fr</email>
(I.H.);
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<name sortKey="Qi, Haoling" sort="Qi, Haoling" uniqKey="Qi H" first="Haoling" last="Qi">Haoling Qi</name>
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<name sortKey="Lopez, Juan" sort="Lopez, Juan" uniqKey="Lopez J" first="Juan" last="Lopez">Juan Lopez</name>
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<email>isabelle.landrieu@univ-lille1.fr</email>
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<email>caroline.smet@univ-lille1.fr</email>
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<p>In this review, we focus on what we have learned from Nuclear Magnetic Resonance (NMR) studies on the neuronal microtubule-associated protein Tau. We consider both the mechanistic details of Tau: the tubulin relationship and its aggregation process. Phosphorylation of Tau is intimately linked to both aspects. NMR spectroscopy has depicted accurate phosphorylation patterns by different kinases, and its non-destructive character has allowed functional assays with the same samples. Finally, we will discuss other post-translational modifications of Tau and its interaction with other cellular factors in relationship to its (dys)function.</p>
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</TEI>
<pmc article-type="review-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Biomolecules</journal-id>
<journal-id journal-id-type="iso-abbrev">Biomolecules</journal-id>
<journal-id journal-id-type="publisher-id">biomolecules</journal-id>
<journal-title-group>
<journal-title>Biomolecules</journal-title>
</journal-title-group>
<issn pub-type="epub">2218-273X</issn>
<publisher>
<publisher-name>MDPI</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">27338491</article-id>
<article-id pub-id-type="pmc">4919923</article-id>
<article-id pub-id-type="doi">10.3390/biom6020028</article-id>
<article-id pub-id-type="publisher-id">biomolecules-06-00028</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Review</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>NMR Meets Tau: Insights into Its Function and Pathology</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Lippens</surname>
<given-names>Guy</given-names>
</name>
<xref ref-type="aff" rid="af1-biomolecules-06-00028">1</xref>
<xref ref-type="aff" rid="af2-biomolecules-06-00028">2</xref>
<xref rid="c1-biomolecules-06-00028" ref-type="corresp">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Landrieu</surname>
<given-names>Isabelle</given-names>
</name>
<xref ref-type="aff" rid="af1-biomolecules-06-00028">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Smet</surname>
<given-names>Caroline</given-names>
</name>
<xref ref-type="aff" rid="af1-biomolecules-06-00028">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Huvent</surname>
<given-names>Isabelle</given-names>
</name>
<xref ref-type="aff" rid="af1-biomolecules-06-00028">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Gandhi</surname>
<given-names>Neha S.</given-names>
</name>
<xref ref-type="aff" rid="af3-biomolecules-06-00028">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Gigant</surname>
<given-names>Benoît</given-names>
</name>
<xref ref-type="aff" rid="af4-biomolecules-06-00028">4</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Despres</surname>
<given-names>Clément</given-names>
</name>
<xref ref-type="aff" rid="af1-biomolecules-06-00028">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Qi</surname>
<given-names>Haoling</given-names>
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<xref ref-type="aff" rid="af1-biomolecules-06-00028">1</xref>
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<contrib contrib-type="author">
<name>
<surname>Lopez</surname>
<given-names>Juan</given-names>
</name>
<xref ref-type="aff" rid="af1-biomolecules-06-00028">1</xref>
<xref ref-type="aff" rid="af5-biomolecules-06-00028">5</xref>
</contrib>
</contrib-group>
<contrib-group>
<contrib contrib-type="editor">
<name>
<surname>Wischik</surname>
<given-names>Claude M.</given-names>
</name>
<role>Academic Editor</role>
</contrib>
<contrib contrib-type="editor">
<name>
<surname>Harrington</surname>
<given-names>Charles</given-names>
</name>
<role>Academic Editor</role>
</contrib>
</contrib-group>
<aff id="af1-biomolecules-06-00028">
<label>1</label>
Unité de Glycobiologie Structurale et Fontionnelle, University of Lille (UGSF), Villeneuve d’Ascq CNRS UMR Lille 8576, France;
<email>isabelle.landrieu@univ-lille1.fr</email>
(I.L.);
<email>caroline.smet@univ-lille1.fr</email>
(C.S.);
<email>isabelle.huvent@univ-lille1.fr</email>
(I.H.);
<email>clement.despres@ed.univ-lille1.fr</email>
(C.D.);
<email>haoling.qi160687@gmail.com</email>
(H.Q.);
<email>juan.lopez@pucp.edu.pe</email>
(J.L.)</aff>
<aff id="af2-biomolecules-06-00028">
<label>2</label>
Laboratoire d'Ingénierie des Systèmes Biologiques et des Procédés (LISBP), University of Toulouse, CNRS, INRA, INSA, Toulouse 31400, France</aff>
<aff id="af3-biomolecules-06-00028">
<label>3</label>
School of Mathematical Sciences, Queensland University of Technology, Brisbane 4001 QLD, Australia;
<email>neha.gandhi@qut.edu.au</email>
</aff>
<aff id="af4-biomolecules-06-00028">
<label>4</label>
Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Sud, Université Paris-Saclay, Gif-sur-Yvette 91190, France;
<email>Benoit.Gigant@i2bc.paris-saclay.fr</email>
</aff>
<aff id="af5-biomolecules-06-00028">
<label>5</label>
Sciences Department-Chemistry, Pontifical Catholic University of Peru (PUCP), Av. Universitaria 1801, Lima 32, Peru</aff>
<author-notes>
<corresp id="c1-biomolecules-06-00028">
<label>*</label>
Correspondence:
<email>Guy.Lippens@insa-toulouse.fr</email>
; Tel.: +33-5-61-55-94-15</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>07</day>
<month>6</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection">
<month>6</month>
<year>2016</year>
</pub-date>
<volume>6</volume>
<issue>2</issue>
<elocation-id>28</elocation-id>
<history>
<date date-type="received">
<day>30</day>
<month>3</month>
<year>2016</year>
</date>
<date date-type="accepted">
<day>26</day>
<month>5</month>
<year>2016</year>
</date>
</history>
<permissions>
<copyright-statement>© 2016 by the authors; licensee MDPI, Basel, Switzerland.</copyright-statement>
<copyright-year>2016</copyright-year>
<license>
<license-p>
<pmc-comment>CREATIVE COMMONS</pmc-comment>
This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC-BY) license (
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
).</license-p>
</license>
</permissions>
<abstract>
<p>In this review, we focus on what we have learned from Nuclear Magnetic Resonance (NMR) studies on the neuronal microtubule-associated protein Tau. We consider both the mechanistic details of Tau: the tubulin relationship and its aggregation process. Phosphorylation of Tau is intimately linked to both aspects. NMR spectroscopy has depicted accurate phosphorylation patterns by different kinases, and its non-destructive character has allowed functional assays with the same samples. Finally, we will discuss other post-translational modifications of Tau and its interaction with other cellular factors in relationship to its (dys)function.</p>
</abstract>
<kwd-group>
<kwd>Tau</kwd>
<kwd>NMR spectroscopy</kwd>
<kwd>intrinsically disordered protein</kwd>
<kwd>tubulin</kwd>
<kwd>aggregation</kwd>
<kwd>phosphorylation</kwd>
<kwd>protein/protein interactions</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group>
<fig id="biomolecules-06-00028-f001" position="float">
<label>Figure 1</label>
<caption>
<p>(
<bold>A</bold>
) Schematic view of the primary sequence of Tau441, the longest isoform of Tau. Different isoforms are characterized by the insertion of 0, one or two N-terminal inserts (N1 and N2), and three (R1-R3-R4) or four (R1-4) repeats (leading to the 3R or 4R forms). The repeats are preceded by a proline-rich region (PRR). The two hexapeptides PHF6 and PHF6* are indicated as red rectangles in R1 and R2, whereas Tau’s two cysteine residues (Cys291 and Cys322) are indicated as yellow circles in R2 and R3. The fragment TauF4 spans part of the PRR, the first two repeats and a small part of R3; (
<bold>B</bold>
) The
<sup>1</sup>
H,
<sup>15</sup>
N HSQC spectra of
<sup>15</sup>
N-labeled wild-type (black) and
<sup>15</sup>
N,
<sup>13</sup>
C-labeled P301L (red) Tau441 show that only a couple of residues directly adjacent to the mutation show chemical shift differences. Residues Val
<sub>309</sub>
-Tyr
<sub>310</sub>
-Lys
<sub>311</sub>
of the PHF6 peptide are identical in chemical shift and intensity in both proteins; (
<bold>C</bold>
) Zoom of the
<sup>1</sup>
H,
<sup>15</sup>
N spectrum of CDK2 phosphorylated Tau around the resonance of pThr231, showing several peaks for the same phosphorylated residue.</p>
</caption>
<graphic xlink:href="biomolecules-06-00028-g001"></graphic>
</fig>
<fig id="biomolecules-06-00028-f002" position="float">
<label>Figure 2</label>
<caption>
<p>(
<bold>A</bold>
) The
<sup>1</sup>
H,
<sup>15</sup>
N TROSY spectrum of TauF4 in its complex with T
<sub>2</sub>
R. Residues in the R1 repeat whose resonances are absent in the TauF4-T
<sub>2</sub>
R spectrum are labeled in red; (
<bold>B</bold>
) Model of the swing movement of TauF4 on the curved T
<sub>2</sub>
R surface [
<xref rid="B76-biomolecules-06-00028" ref-type="bibr">76</xref>
].</p>
</caption>
<graphic xlink:href="biomolecules-06-00028-g002"></graphic>
</fig>
<fig id="biomolecules-06-00028-f003" position="float">
<label>Figure 3</label>
<caption>
<p>Crystal structure of the PHF6 peptide in complex with orange G (PDB code 3OVL), seen along the fiber axis from the top. Inserts show the antiparallel dry interface between opposing peptides, or the parallel stacking between adjacent peptides in the same plane. Orange G has two sulfate groups separated by 5 Å, and thereby compensates the lysine side-chain positive charges of two adjacent peptides [
<xref rid="B120-biomolecules-06-00028" ref-type="bibr">120</xref>
].</p>
</caption>
<graphic xlink:href="biomolecules-06-00028-g003"></graphic>
</fig>
<fig id="biomolecules-06-00028-f004" position="float">
<label>Figure 4</label>
<caption>
<p>Electron microscopy of (
<bold>A</bold>
) heparin-induced synthetic fibers of Tau441 show the morphology of paired helical filaments, whereas (
<bold>B</bold>
) those of a TauF4 fragment devoid of cysteine residues show a morphology of two flat ribbons twisted around one another [
<xref rid="B126-biomolecules-06-00028" ref-type="bibr">126</xref>
]. This morphology is found in the
<italic>ex vivo</italic>
3R fibers characterizing Pick’s disease [
<xref rid="B127-biomolecules-06-00028" ref-type="bibr">127</xref>
]; (
<bold>C)</bold>
TauP301L after phosphorylation by Erk2 forms fibers without heparin. Scale bar = 100 nm.</p>
</caption>
<graphic xlink:href="biomolecules-06-00028-g004"></graphic>
</fig>
<fig id="biomolecules-06-00028-f005" position="float">
<label>Figure 5</label>
<caption>
<p>Structure of the AT8 motif in solution [
<xref rid="B56-biomolecules-06-00028" ref-type="bibr">56</xref>
] or in complex with the AT8 Fab fragment ([
<xref rid="B142-biomolecules-06-00028" ref-type="bibr">142</xref>
]; PDB code 5E2W). The helical turn stabilized by the interaction between the Gly
<sub>207</sub>
HN and the phosphate group of pThr
<sub>205</sub>
(left) is not maintained in its complex with the AT8 antibody (right). The phosphate group of pSer
<sub>208</sub>
makes additional interactions with residues of the antibody. The AT8 Fab is in green, with the variable loops of the light and heavy chain in yellow, respectively, orange.</p>
</caption>
<graphic xlink:href="biomolecules-06-00028-g005"></graphic>
</fig>
</floats-group>
</pmc>
</record>

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