Contribution of Shape and Charge to the Inhibition of a Family GH99 endo-α-1,2-Mannanase
Identifieur interne : 000A45 ( Pmc/Checkpoint ); précédent : 000A44; suivant : 000A46Contribution of Shape and Charge to the Inhibition of a Family GH99 endo-α-1,2-Mannanase
Auteurs : Marija Petricevic [Australie] ; Lukasz F. Sobala [Royaume-Uni] ; Pearl Z. Fernandes [Australie] ; Lluís Raich [Espagne] ; Andrew J. Thompson [Royaume-Uni] ; Ganeko Bernardo-Seisdedos [Espagne] ; Oscar Millet [Espagne] ; Sha Zhu [France] ; Matthieu Sollogoub [France] ; Jesús Jiménez-Barbero [Espagne] ; Carme Rovira [Espagne] ; Gideon J. Davies [Royaume-Uni] ; Spencer J. Williams [Australie]Source :
- Journal of the American Chemical Society [ 0002-7863 ] ; 2016.
Abstract
Inhibitor
design incorporating features of the reaction coordinate
and transition-state structure has emerged as a powerful approach
for the development of enzyme inhibitors. Such inhibitors find use
as mechanistic probes, chemical biology tools, and therapeutics.
Url:
DOI: 10.1021/jacs.6b10075
PubMed: 27992199
PubMed Central: 5269645
Affiliations:
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of Shape and Charge to the Inhibition
of a Family GH99 <italic>endo</italic>
-α-1,2-Mannanase</title>
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, Parkville 3010,<country>Australia</country>
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<country xml:lang="fr">Australie</country>
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<author><name sortKey="Sobala, Lukasz F" sort="Sobala, Lukasz F" uniqKey="Sobala L" first="Lukasz F." last="Sobala">Lukasz F. Sobala</name>
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, York YO10 5DD,<country>United Kingdom</country>
</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
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<author><name sortKey="Fernandes, Pearl Z" sort="Fernandes, Pearl Z" uniqKey="Fernandes P" first="Pearl Z." last="Fernandes">Pearl Z. Fernandes</name>
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, Parkville 3010,<country>Australia</country>
</nlm:aff>
<country xml:lang="fr">Australie</country>
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<author><name sortKey="Raich, Lluis" sort="Raich, Lluis" uniqKey="Raich L" first="Lluís" last="Raich">Lluís Raich</name>
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, Martí i Franquès 1, 08028 Barcelona,<country>Spain</country>
</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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, York YO10 5DD,<country>United Kingdom</country>
</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
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<author><name sortKey="Bernardo Seisdedos, Ganeko" sort="Bernardo Seisdedos, Ganeko" uniqKey="Bernardo Seisdedos G" first="Ganeko" last="Bernardo-Seisdedos">Ganeko Bernardo-Seisdedos</name>
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<author><name sortKey="Millet, Oscar" sort="Millet, Oscar" uniqKey="Millet O" first="Oscar" last="Millet">Oscar Millet</name>
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</nlm:aff>
<country xml:lang="fr">Espagne</country>
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<author><name sortKey="Zhu, Sha" sort="Zhu, Sha" uniqKey="Zhu S" first="Sha" last="Zhu">Sha Zhu</name>
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</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Sollogoub, Matthieu" sort="Sollogoub, Matthieu" uniqKey="Sollogoub M" first="Matthieu" last="Sollogoub">Matthieu Sollogoub</name>
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</nlm:aff>
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<author><name sortKey="Jimenez Barbero, Jesus" sort="Jimenez Barbero, Jesus" uniqKey="Jimenez Barbero J" first="Jesús" last="Jiménez-Barbero">Jesús Jiménez-Barbero</name>
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</nlm:aff>
<country xml:lang="fr">Espagne</country>
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</nlm:aff>
<country xml:lang="fr">Espagne</country>
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<author><name sortKey="Rovira, Carme" sort="Rovira, Carme" uniqKey="Rovira C" first="Carme" last="Rovira">Carme Rovira</name>
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, Martí i Franquès 1, 08028 Barcelona,<country>Spain</country>
</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<affiliation wicri:level="1"><nlm:aff id="aff6"><institution>Institució Catalana de Recerca i Estudis Avançats (ICREA)</institution>
, Pg. Lluís Companys 23, 08010 Barcelona,<country>Spain</country>
</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
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, York YO10 5DD,<country>United Kingdom</country>
</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
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, Parkville 3010,<country>Australia</country>
</nlm:aff>
<country xml:lang="fr">Australie</country>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Contribution
of Shape and Charge to the Inhibition
of a Family GH99 <italic>endo</italic>
-α-1,2-Mannanase</title>
<author><name sortKey="Petricevic, Marija" sort="Petricevic, Marija" uniqKey="Petricevic M" first="Marija" last="Petricevic">Marija Petricevic</name>
<affiliation wicri:level="1"><nlm:aff id="aff1">School of Chemistry and Bio21 Molecular Science and Biotechnology Institute,<institution>University of Melbourne</institution>
, Parkville 3010,<country>Australia</country>
</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Sobala, Lukasz F" sort="Sobala, Lukasz F" uniqKey="Sobala L" first="Lukasz F." last="Sobala">Lukasz F. Sobala</name>
<affiliation wicri:level="1"><nlm:aff id="aff2">York Structural Biology Laboratory, Department of Chemistry,<institution>University of York</institution>
, York YO10 5DD,<country>United Kingdom</country>
</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Fernandes, Pearl Z" sort="Fernandes, Pearl Z" uniqKey="Fernandes P" first="Pearl Z." last="Fernandes">Pearl Z. Fernandes</name>
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, Parkville 3010,<country>Australia</country>
</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Raich, Lluis" sort="Raich, Lluis" uniqKey="Raich L" first="Lluís" last="Raich">Lluís Raich</name>
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, Martí i Franquès 1, 08028 Barcelona,<country>Spain</country>
</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
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<author><name sortKey="Thompson, Andrew J" sort="Thompson, Andrew J" uniqKey="Thompson A" first="Andrew J." last="Thompson">Andrew J. Thompson</name>
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, York YO10 5DD,<country>United Kingdom</country>
</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
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<author><name sortKey="Bernardo Seisdedos, Ganeko" sort="Bernardo Seisdedos, Ganeko" uniqKey="Bernardo Seisdedos G" first="Ganeko" last="Bernardo-Seisdedos">Ganeko Bernardo-Seisdedos</name>
<affiliation wicri:level="1"><nlm:aff id="aff4">Molecular Recognition and Host−Pathogen Interactions, CIC bioGUNE, Bizkaia Technology Park, Building 800, 48160 Derio,<country>Spain</country>
</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
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<author><name sortKey="Millet, Oscar" sort="Millet, Oscar" uniqKey="Millet O" first="Oscar" last="Millet">Oscar Millet</name>
<affiliation wicri:level="1"><nlm:aff id="aff4">Molecular Recognition and Host−Pathogen Interactions, CIC bioGUNE, Bizkaia Technology Park, Building 800, 48160 Derio,<country>Spain</country>
</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Zhu, Sha" sort="Zhu, Sha" uniqKey="Zhu S" first="Sha" last="Zhu">Sha Zhu</name>
<affiliation wicri:level="1"><nlm:aff id="aff3">Sorbonne Universités, UPMC Univ Paris 06, CNRS, Institut Parisien de Chimie Moléculaire (IPCM), UMR 8232, 4, place Jussieu, 75005 Paris,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Sollogoub, Matthieu" sort="Sollogoub, Matthieu" uniqKey="Sollogoub M" first="Matthieu" last="Sollogoub">Matthieu Sollogoub</name>
<affiliation wicri:level="1"><nlm:aff id="aff3">Sorbonne Universités, UPMC Univ Paris 06, CNRS, Institut Parisien de Chimie Moléculaire (IPCM), UMR 8232, 4, place Jussieu, 75005 Paris,<country>France</country>
</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Jimenez Barbero, Jesus" sort="Jimenez Barbero, Jesus" uniqKey="Jimenez Barbero J" first="Jesús" last="Jiménez-Barbero">Jesús Jiménez-Barbero</name>
<affiliation wicri:level="1"><nlm:aff id="aff4">Molecular Recognition and Host−Pathogen Interactions, CIC bioGUNE, Bizkaia Technology Park, Building 800, 48160 Derio,<country>Spain</country>
</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff7">Ikerbasque, Basque Foundation for Science, María Díaz de Haro 3, 48013 Bilbao,<country>Spain</country>
</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Rovira, Carme" sort="Rovira, Carme" uniqKey="Rovira C" first="Carme" last="Rovira">Carme Rovira</name>
<affiliation wicri:level="1"><nlm:aff id="aff5">Departament de Química Inorgànica i Orgànica (Secció de Química Orgànica) & Institut de Química Teòrica i Computacional (IQTCUB),<institution>Universitat de Barcelona</institution>
, Martí i Franquès 1, 08028 Barcelona,<country>Spain</country>
</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff6"><institution>Institució Catalana de Recerca i Estudis Avançats (ICREA)</institution>
, Pg. Lluís Companys 23, 08010 Barcelona,<country>Spain</country>
</nlm:aff>
<country xml:lang="fr">Espagne</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Davies, Gideon J" sort="Davies, Gideon J" uniqKey="Davies G" first="Gideon J." last="Davies">Gideon J. Davies</name>
<affiliation wicri:level="1"><nlm:aff id="aff2">York Structural Biology Laboratory, Department of Chemistry,<institution>University of York</institution>
, York YO10 5DD,<country>United Kingdom</country>
</nlm:aff>
<country xml:lang="fr">Royaume-Uni</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Williams, Spencer J" sort="Williams, Spencer J" uniqKey="Williams S" first="Spencer J." last="Williams">Spencer J. Williams</name>
<affiliation wicri:level="1"><nlm:aff id="aff1">School of Chemistry and Bio21 Molecular Science and Biotechnology Institute,<institution>University of Melbourne</institution>
, Parkville 3010,<country>Australia</country>
</nlm:aff>
<country xml:lang="fr">Australie</country>
<wicri:regionArea># see nlm:aff country strict</wicri:regionArea>
</affiliation>
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<series><title level="j">Journal of the American Chemical Society</title>
<idno type="ISSN">0002-7863</idno>
<idno type="eISSN">1520-5126</idno>
<imprint><date when="2016">2016</date>
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<front><div type="abstract" xml:lang="en"><p content-type="toc-graphic"><graphic xlink:href="ja-2016-10075v_0008" id="ab-tgr1"></graphic>
</p>
<p>Inhibitor
design incorporating features of the reaction coordinate
and transition-state structure has emerged as a powerful approach
for the development of enzyme inhibitors. Such inhibitors find use
as mechanistic probes, chemical biology tools, and therapeutics. <italic>Endo</italic>
-α-1,2-mannosidases and <italic>endo</italic>
-α-1,2-mannanases,
members of glycoside hydrolase family 99 (GH99), are interesting targets
for inhibitor development as they play key roles in N-glycan maturation
and microbiotal yeast mannan degradation, respectively. These enzymes
are proposed to act via a 1,2-anhydrosugar “epoxide”
mechanism that proceeds through an unusual conformational itinerary.
Here, we explore how shape and charge contribute to binding of diverse
inhibitors of these enzymes. We report the synthesis of neutral dideoxy,
glucal and cyclohexenyl disaccharide inhibitors, their binding to
GH99 <italic>endo</italic>
-α-1,2-mannanases, and their structural
analysis by X-ray crystallography. Quantum mechanical calculations
of the free energy landscapes reveal how the neutral inhibitors provide
shape but not charge mimicry of the proposed intermediate and transition
state structures. Building upon the knowledge of shape and charge
contributions to inhibition of family GH99 enzymes, we design and
synthesize α-Man-1,3-noeuromycin, which is revealed to be the
most potent inhibitor (<italic>K</italic>
<sub>D</sub>
13 nM for <italic>Bacteroides xylanisolvens</italic>
GH99 enzyme) of these enzymes
yet reported. This work reveals how shape and charge mimicry of transition
state features can enable the rational design of potent inhibitors.</p>
</div>
</front>
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<pmc article-type="research-article" xml:lang="EN"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Am Chem Soc</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Am. Chem. Soc</journal-id>
<journal-id journal-id-type="publisher-id">ja</journal-id>
<journal-id journal-id-type="coden">jacsat</journal-id>
<journal-title-group><journal-title>Journal of the American Chemical Society</journal-title>
</journal-title-group>
<issn pub-type="ppub">0002-7863</issn>
<issn pub-type="epub">1520-5126</issn>
<publisher><publisher-name>American Chemical
Society</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27992199</article-id>
<article-id pub-id-type="pmc">5269645</article-id>
<article-id pub-id-type="doi">10.1021/jacs.6b10075</article-id>
<article-categories><subj-group><subject>Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Contribution
of Shape and Charge to the Inhibition
of a Family GH99 <italic>endo</italic>
-α-1,2-Mannanase</article-title>
</title-group>
<contrib-group><contrib contrib-type="author" id="ath1"><name><surname>Petricevic</surname>
<given-names>Marija</given-names>
</name>
<xref rid="aff1" ref-type="aff">†</xref>
</contrib>
<contrib contrib-type="author" id="ath2"><name><surname>Sobala</surname>
<given-names>Lukasz F.</given-names>
</name>
<xref rid="aff2" ref-type="aff">‡</xref>
</contrib>
<contrib contrib-type="author" id="ath3"><name><surname>Fernandes</surname>
<given-names>Pearl Z.</given-names>
</name>
<xref rid="aff1" ref-type="aff">†</xref>
</contrib>
<contrib contrib-type="author" id="ath4"><name><surname>Raich</surname>
<given-names>Lluís</given-names>
</name>
<xref rid="aff5" ref-type="aff">⊥</xref>
</contrib>
<contrib contrib-type="author" id="ath5"><name><surname>Thompson</surname>
<given-names>Andrew J.</given-names>
</name>
<xref rid="aff2" ref-type="aff">‡</xref>
</contrib>
<contrib contrib-type="author" id="ath6"><name><surname>Bernardo-Seisdedos</surname>
<given-names>Ganeko</given-names>
</name>
<xref rid="aff4" ref-type="aff">∥</xref>
</contrib>
<contrib contrib-type="author" id="ath7"><name><surname>Millet</surname>
<given-names>Oscar</given-names>
</name>
<xref rid="aff4" ref-type="aff">∥</xref>
</contrib>
<contrib contrib-type="author" id="ath8"><name><surname>Zhu</surname>
<given-names>Sha</given-names>
</name>
<xref rid="aff3" ref-type="aff">§</xref>
</contrib>
<contrib contrib-type="author" id="ath9"><name><surname>Sollogoub</surname>
<given-names>Matthieu</given-names>
</name>
<xref rid="aff3" ref-type="aff">§</xref>
</contrib>
<contrib contrib-type="author" id="ath10"><name><surname>Jiménez-Barbero</surname>
<given-names>Jesús</given-names>
</name>
<xref rid="aff4" ref-type="aff">∥</xref>
<xref rid="aff7" ref-type="aff">∇</xref>
</contrib>
<contrib contrib-type="author" corresp="yes" id="ath11"><name><surname>Rovira</surname>
<given-names>Carme</given-names>
</name>
<xref rid="cor1" ref-type="other">*</xref>
<xref rid="aff5" ref-type="aff">⊥</xref>
<xref rid="aff6" ref-type="aff">#</xref>
</contrib>
<contrib contrib-type="author" corresp="yes" id="ath12"><name><surname>Davies</surname>
<given-names>Gideon J.</given-names>
</name>
<xref rid="cor2" ref-type="other">*</xref>
<xref rid="aff2" ref-type="aff">‡</xref>
</contrib>
<contrib contrib-type="author" corresp="yes" id="ath13"><name><surname>Williams</surname>
<given-names>Spencer J.</given-names>
</name>
<xref rid="cor3" ref-type="other">*</xref>
<xref rid="aff1" ref-type="aff">†</xref>
</contrib>
<aff id="aff1"><label>†</label>
School of Chemistry and Bio21 Molecular Science and Biotechnology Institute,<institution>University of Melbourne</institution>
, Parkville 3010,<country>Australia</country>
</aff>
<aff id="aff2"><label>‡</label>
York Structural Biology Laboratory, Department of Chemistry,<institution>University of York</institution>
, York YO10 5DD,<country>United Kingdom</country>
</aff>
<aff id="aff3"><label>§</label>
Sorbonne Universités, UPMC Univ Paris 06, CNRS, Institut Parisien de Chimie Moléculaire (IPCM), UMR 8232, 4, place Jussieu, 75005 Paris,<country>France</country>
</aff>
<aff id="aff4"><label>∥</label>
Molecular Recognition and Host−Pathogen Interactions, CIC bioGUNE, Bizkaia Technology Park, Building 800, 48160 Derio,<country>Spain</country>
</aff>
<aff id="aff5"><label>⊥</label>
Departament de Química Inorgànica i Orgànica (Secció de Química Orgànica) & Institut de Química Teòrica i Computacional (IQTCUB),<institution>Universitat de Barcelona</institution>
, Martí i Franquès 1, 08028 Barcelona,<country>Spain</country>
</aff>
<aff id="aff6"><label>#</label>
<institution>Institució Catalana de Recerca i Estudis Avançats (ICREA)</institution>
, Pg. Lluís Companys 23, 08010 Barcelona,<country>Spain</country>
</aff>
<aff id="aff7"><label>∇</label>
Ikerbasque, Basque Foundation for Science, María Díaz de Haro 3, 48013 Bilbao,<country>Spain</country>
</aff>
</contrib-group>
<author-notes><corresp id="cor1"><label>*</label>
<email>c.rovira@ub.edu</email>
</corresp>
<corresp id="cor2"><label>*</label>
<email>gideon.davies@york.ac.uk</email>
</corresp>
<corresp id="cor3"><label>*</label>
<email>sjwill@unimelb.edu.au</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>19</day>
<month>12</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="ppub"><day>25</day>
<month>01</month>
<year>2017</year>
</pub-date>
<volume>139</volume>
<issue>3</issue>
<fpage>1089</fpage>
<lpage>1097</lpage>
<history><date date-type="received"><day>25</day>
<month>09</month>
<year>2016</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2016 American Chemical Society</copyright-statement>
<copyright-year>2016</copyright-year>
<copyright-holder>American Chemical Society</copyright-holder>
<license><license-p>This is an open access article published under an ACS AuthorChoice <ext-link ext-link-type="uri" xlink:href="http://pubs.acs.org/page/policy/authorchoice_termsofuse.html">License</ext-link>
, which permits copying and redistribution of the article or any adaptations for non-commercial purposes.</license-p>
</license>
</permissions>
<abstract><p content-type="toc-graphic"><graphic xlink:href="ja-2016-10075v_0008" id="ab-tgr1"></graphic>
</p>
<p>Inhibitor
design incorporating features of the reaction coordinate
and transition-state structure has emerged as a powerful approach
for the development of enzyme inhibitors. Such inhibitors find use
as mechanistic probes, chemical biology tools, and therapeutics. <italic>Endo</italic>
-α-1,2-mannosidases and <italic>endo</italic>
-α-1,2-mannanases,
members of glycoside hydrolase family 99 (GH99), are interesting targets
for inhibitor development as they play key roles in N-glycan maturation
and microbiotal yeast mannan degradation, respectively. These enzymes
are proposed to act via a 1,2-anhydrosugar “epoxide”
mechanism that proceeds through an unusual conformational itinerary.
Here, we explore how shape and charge contribute to binding of diverse
inhibitors of these enzymes. We report the synthesis of neutral dideoxy,
glucal and cyclohexenyl disaccharide inhibitors, their binding to
GH99 <italic>endo</italic>
-α-1,2-mannanases, and their structural
analysis by X-ray crystallography. Quantum mechanical calculations
of the free energy landscapes reveal how the neutral inhibitors provide
shape but not charge mimicry of the proposed intermediate and transition
state structures. Building upon the knowledge of shape and charge
contributions to inhibition of family GH99 enzymes, we design and
synthesize α-Man-1,3-noeuromycin, which is revealed to be the
most potent inhibitor (<italic>K</italic>
<sub>D</sub>
13 nM for <italic>Bacteroides xylanisolvens</italic>
GH99 enzyme) of these enzymes
yet reported. This work reveals how shape and charge mimicry of transition
state features can enable the rational design of potent inhibitors.</p>
</abstract>
<custom-meta-group><custom-meta><meta-name>document-id-old-9</meta-name>
<meta-value>ja6b10075</meta-value>
</custom-meta>
<custom-meta><meta-name>document-id-new-14</meta-name>
<meta-value>ja-2016-10075v</meta-value>
</custom-meta>
<custom-meta><meta-name>ccc-price</meta-name>
<meta-value></meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Australie</li>
<li>Espagne</li>
<li>France</li>
<li>Royaume-Uni</li>
</country>
</list>
<tree><country name="Australie"><noRegion><name sortKey="Petricevic, Marija" sort="Petricevic, Marija" uniqKey="Petricevic M" first="Marija" last="Petricevic">Marija Petricevic</name>
</noRegion>
<name sortKey="Fernandes, Pearl Z" sort="Fernandes, Pearl Z" uniqKey="Fernandes P" first="Pearl Z." last="Fernandes">Pearl Z. Fernandes</name>
<name sortKey="Williams, Spencer J" sort="Williams, Spencer J" uniqKey="Williams S" first="Spencer J." last="Williams">Spencer J. Williams</name>
</country>
<country name="Royaume-Uni"><noRegion><name sortKey="Sobala, Lukasz F" sort="Sobala, Lukasz F" uniqKey="Sobala L" first="Lukasz F." last="Sobala">Lukasz F. Sobala</name>
</noRegion>
<name sortKey="Davies, Gideon J" sort="Davies, Gideon J" uniqKey="Davies G" first="Gideon J." last="Davies">Gideon J. Davies</name>
<name sortKey="Thompson, Andrew J" sort="Thompson, Andrew J" uniqKey="Thompson A" first="Andrew J." last="Thompson">Andrew J. Thompson</name>
</country>
<country name="Espagne"><noRegion><name sortKey="Raich, Lluis" sort="Raich, Lluis" uniqKey="Raich L" first="Lluís" last="Raich">Lluís Raich</name>
</noRegion>
<name sortKey="Bernardo Seisdedos, Ganeko" sort="Bernardo Seisdedos, Ganeko" uniqKey="Bernardo Seisdedos G" first="Ganeko" last="Bernardo-Seisdedos">Ganeko Bernardo-Seisdedos</name>
<name sortKey="Jimenez Barbero, Jesus" sort="Jimenez Barbero, Jesus" uniqKey="Jimenez Barbero J" first="Jesús" last="Jiménez-Barbero">Jesús Jiménez-Barbero</name>
<name sortKey="Jimenez Barbero, Jesus" sort="Jimenez Barbero, Jesus" uniqKey="Jimenez Barbero J" first="Jesús" last="Jiménez-Barbero">Jesús Jiménez-Barbero</name>
<name sortKey="Millet, Oscar" sort="Millet, Oscar" uniqKey="Millet O" first="Oscar" last="Millet">Oscar Millet</name>
<name sortKey="Rovira, Carme" sort="Rovira, Carme" uniqKey="Rovira C" first="Carme" last="Rovira">Carme Rovira</name>
<name sortKey="Rovira, Carme" sort="Rovira, Carme" uniqKey="Rovira C" first="Carme" last="Rovira">Carme Rovira</name>
</country>
<country name="France"><noRegion><name sortKey="Zhu, Sha" sort="Zhu, Sha" uniqKey="Zhu S" first="Sha" last="Zhu">Sha Zhu</name>
</noRegion>
<name sortKey="Sollogoub, Matthieu" sort="Sollogoub, Matthieu" uniqKey="Sollogoub M" first="Matthieu" last="Sollogoub">Matthieu Sollogoub</name>
</country>
</tree>
</affiliations>
</record>
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