Molecular basis for the behavioral effects of the odorant degrading enzyme Esterase 6 in Drosophila
Identifieur interne : 000875 ( Pmc/Curation ); précédent : 000874; suivant : 000876Molecular basis for the behavioral effects of the odorant degrading enzyme Esterase 6 in Drosophila
Auteurs : Faisal Younus [Australie] ; Nicholas J. Fraser [Australie] ; Chris W. Coppin [Australie] ; Jian-Wei Liu [Australie] ; Galen J. Correy [Australie] ; Thomas Chertemps [France] ; Gunjan Pandey [Australie] ; Martine Maïbèche [France] ; Colin J. Jackson [Australie] ; John G. Oakeshott [Australie]Source :
- Scientific Reports [ 2045-2322 ] ; 2017.
Abstract
Previous electrophysiological and behavioural studies implicate esterase 6 in the processing of the pheromone cis-vaccenyl acetate and various food odorants that affect aggregation and reproductive behaviours. Here we show esterase 6 has relatively high activity against many of the short-mid chain food esters, but negligible activity against cis-vaccenyl acetate. The crystal structure of esterase 6 confirms its substrate-binding site can accommodate many short-mid chain food esters but not cis-vaccenyl acetate. Immunohistochemical assays show esterase 6 is expressed in non-neuronal cells in the third antennal segment that could be accessory or epidermal cells surrounding numerous olfactory sensilla, including basiconics involved in food odorant detection. Esterase 6 is also produced in trichoid sensilla, but not in the same cell types as the cis-vaccenyl acetate binding protein LUSH. Our data support a model in which esterase 6 acts as a direct odorant degrading enzyme for many bioactive food esters, but not cis-vaccenyl acetate.
Url:
DOI: 10.1038/srep46188
PubMed: 28393888
PubMed Central: 5385555
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Jackson</name><affiliation wicri:level="1"><nlm:aff id="a2"><institution>Research School of Chemistry, Australian National University</institution>, Canberra, ACT, 2601,<country>Australia</country></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Oakeshott, John G" sort="Oakeshott, John G" uniqKey="Oakeshott J" first="John G." last="Oakeshott">John G. Oakeshott</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>CSIRO Land and Water, Black Mountain</institution>, Canberra, ACT, 2601,<country>Australia</country></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></analytic><series><title level="j">Scientific Reports</title><idno type="eISSN">2045-2322</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Previous electrophysiological and behavioural studies implicate esterase 6 in the processing of the pheromone cis-vaccenyl acetate and various food odorants that affect aggregation and reproductive behaviours. Here we show esterase 6 has relatively high activity against many of the short-mid chain food esters, but negligible activity against cis-vaccenyl acetate. The crystal structure of esterase 6 confirms its substrate-binding site can accommodate many short-mid chain food esters but not cis-vaccenyl acetate. Immunohistochemical assays show esterase 6 is expressed in non-neuronal cells in the third antennal segment that could be accessory or epidermal cells surrounding numerous olfactory sensilla, including basiconics involved in food odorant detection. Esterase 6 is also produced in trichoid sensilla, but not in the same cell types as the cis-vaccenyl acetate binding protein LUSH. Our data support a model in which esterase 6 acts as a direct odorant degrading enzyme for many bioactive food esters, but not cis-vaccenyl acetate.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Carey, A F" uniqKey="Carey A">A. F. Carey</name></author><author><name sortKey="Carlson, J R" uniqKey="Carlson J">J. R. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Sci Rep</journal-id><journal-id journal-id-type="iso-abbrev">Sci Rep</journal-id><journal-title-group><journal-title>Scientific Reports</journal-title></journal-title-group><issn pub-type="epub">2045-2322</issn><publisher><publisher-name>Nature Publishing Group</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">28393888</article-id><article-id pub-id-type="pmc">5385555</article-id><article-id pub-id-type="pii">srep46188</article-id><article-id pub-id-type="doi">10.1038/srep46188</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Molecular basis for the behavioral effects of the odorant degrading enzyme Esterase 6 in <italic>Drosophila</italic></article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Younus</surname><given-names>Faisal</given-names></name><xref ref-type="aff" rid="a1">1</xref><xref ref-type="aff" rid="a2">2</xref></contrib><contrib contrib-type="author"><name><surname>Fraser</surname><given-names>Nicholas J.</given-names></name><xref ref-type="aff" rid="a2">2</xref></contrib><contrib contrib-type="author"><name><surname>Coppin</surname><given-names>Chris W.</given-names></name><xref ref-type="aff" rid="a1">1</xref></contrib><contrib contrib-type="author"><name><surname>Liu</surname><given-names>Jian-Wei</given-names></name><xref ref-type="aff" rid="a1">1</xref></contrib><contrib contrib-type="author"><name><surname>Correy</surname><given-names>Galen J.</given-names></name><xref ref-type="aff" rid="a2">2</xref></contrib><contrib contrib-type="author"><name><surname>Chertemps</surname><given-names>Thomas</given-names></name><xref ref-type="aff" rid="a3">3</xref></contrib><contrib contrib-type="author"><name><surname>Pandey</surname><given-names>Gunjan</given-names></name><xref ref-type="aff" rid="a1">1</xref></contrib><contrib contrib-type="author"><name><surname>Maïbèche</surname><given-names>Martine</given-names></name><xref ref-type="aff" rid="a3">3</xref></contrib><contrib contrib-type="author"><name><surname>Jackson</surname><given-names>Colin J.</given-names></name><xref ref-type="aff" rid="a2">2</xref></contrib><contrib contrib-type="author"><name><surname>Oakeshott</surname><given-names>John G.</given-names></name><xref ref-type="corresp" rid="c1">a</xref><xref ref-type="aff" rid="a1">1</xref></contrib><aff id="a1"><label>1</label><institution>CSIRO Land and Water, Black Mountain</institution>, Canberra, ACT, 2601,<country>Australia</country></aff><aff id="a2"><label>2</label><institution>Research School of Chemistry, Australian National University</institution>, Canberra, ACT, 2601,<country>Australia</country></aff><aff id="a3"><label>3</label><institution>Université Pierre et Marie Curie, Institut d’Ecologie et des Sciences de l’Environnement de Paris</institution>, 75252, Paris,<country>France</country></aff></contrib-group><author-notes><corresp id="c1"><label>a</label><email>john.oakeshott@csiro.au</email></corresp></author-notes><pub-date pub-type="epub"><day>10</day><month>04</month><year>2017</year></pub-date><pub-date pub-type="collection"><year>2017</year></pub-date><volume>7</volume><elocation-id>46188</elocation-id><history><date date-type="received"><day>15</day><month>12</month><year>2016</year></date><date date-type="accepted"><day>10</day><month>03</month><year>2017</year></date></history><permissions><copyright-statement>Copyright © 2017, The Author(s)</copyright-statement><copyright-year>2017</copyright-year><copyright-holder>The Author(s)</copyright-holder><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit <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>Previous electrophysiological and behavioural studies implicate esterase 6 in the processing of the pheromone cis-vaccenyl acetate and various food odorants that affect aggregation and reproductive behaviours. Here we show esterase 6 has relatively high activity against many of the short-mid chain food esters, but negligible activity against cis-vaccenyl acetate. The crystal structure of esterase 6 confirms its substrate-binding site can accommodate many short-mid chain food esters but not cis-vaccenyl acetate. Immunohistochemical assays show esterase 6 is expressed in non-neuronal cells in the third antennal segment that could be accessory or epidermal cells surrounding numerous olfactory sensilla, including basiconics involved in food odorant detection. Esterase 6 is also produced in trichoid sensilla, but not in the same cell types as the cis-vaccenyl acetate binding protein LUSH. Our data support a model in which esterase 6 acts as a direct odorant degrading enzyme for many bioactive food esters, but not cis-vaccenyl acetate.</p></abstract></article-meta></front><floats-group><fig id="f1"><label>Figure 1</label><caption><title>EST6 <italic>k</italic><sub>cat</sub>/<italic>K</italic><sub>M</sub><sup>Est</sup> and biological source of the most active substrates tested and other substrates of particular structural or physiological significance.</title><p>Alcohol moieties are listed on the vertical and are grouped according to structural similarity. Acid moieties are listed on the horizontal. An ellipsis (…) demarcates a break in an otherwise incremental series. Data on the biological source of the substrates are taken from <xref ref-type="supplementary-material" rid="S1">Supplementary Table S2</xref>. Activity results for all 87 compounds tested are given in <xref ref-type="supplementary-material" rid="S1">Supplementary Table S1</xref>.</p></caption><graphic xlink:href="srep46188-f1"></graphic></fig><fig id="f2"><label>Figure 2</label><caption><title>The structure of EST6 from <italic>D. melanogaster</italic>.</title><p>(<bold>a</bold>) Topology representation of EST6 displaying the conserved α/β-hydrolase fold (grey), secondary structure found in the structurally similar proteins (blue) and unique secondary structure (red). S, D, H represent the Ser188, Asp319 and His445 residues that make up the catalytic triad. The oxyanion hole is located in the loop following sheet 4 (marked by a red x). (<bold>b</bold>) Cartoon diagram of EST6 with features shown in the topology model similarly coloured. The location of the active site is indicated. (<bold>c</bold>) The active site of EST6 with 2<italic>mF</italic><sub>o</sub>−<italic>dF</italic><sub>c</sub> electron density contoured at 1.5 σ. The active site serine and histidine from the catalytic triad are coloured cyan, the oxyanion hole (Gly108, Gly109, Ala110) is coloured green. (<bold>d</bold>) An overlay of EST6 (cyan), <italic>Lc</italic>αE7 (tan; 4FNM), <italic>Dm</italic>AChE (green; 1QO9) and <italic>Ms</italic>JHE (pink; 2FJ0). Conservation of the core β-sheet and conserved α-helices is apparent, but the structures diverge in the region that forms the active site entrance. These regions, either side of the active site, are boxed for clarity. (<bold>e</bold>) A superposition of EST6, LcαE7, DmAChE and MsJHE, with cut-aways through the middle of the active site. The location of the active site entrance difference between EST6 (cyan) and the other related insect carboxylesterases <italic>Lc</italic>αE7 (tan; 4FNM), <italic>Dm</italic>AChE (green; 1QO9) and <italic>Ms</italic>JHE (pink; 2FJ0).</p></caption><graphic xlink:href="srep46188-f2"></graphic></fig><fig id="f3"><label>Figure 3</label><caption><title>The substrate binding site of EST6.</title><p>(<bold>a</bold>) The surface of the substrate binding site is shaded grey and the residues that comprise the small and large pockets are shown (grey) as is the catalytic serine (orange). The small site consists of Ala110, Trp221, Phe276, Tyr322, Phe397 and His445, and the large site consists of Gln70, Phe71, Phe113, Gly114, Gln118, Asn119, Ile429, Tyr449, Phe450, Asn455, Phe456, and Val457. (<bold>b</bold>) An overlay of representative acylated enzyme intermediates covalently docked into EST6: the efficiently hydrolyzed substrates pentyl butyrate (magenta), octyl propionate (cyan), geranyl acetate (green) and phenethyl acetate (yellow) all produce acylated intermediates that are accommodated by the substrate binding site.</p></caption><graphic xlink:href="srep46188-f3"></graphic></fig><fig id="f4"><label>Figure 4</label><caption><title>EST6 and <italic>Orco</italic> expression in the third antennal segment, longitudinal sections.</title><p>(<bold>a</bold>) Membrane-tethered RFP expressed with the <italic>Orco</italic> promoter (<italic>Orco</italic><sup><italic>Gal4</italic></sup><italic>/UAS-mCD8::RFP</italic> transgenic flies). (<bold>b</bold>) EST6 protein localization in the same section. (<bold>c</bold>) Merge image of (<bold>a</bold>,<bold>b</bold>): Est-6 and <italic>Orco</italic> are not expressed in the same cells. (<bold>d</bold>) Higher magnifications of (<bold>c</bold>): EST6 protein surrounds the Orco<sup><sup>+</sup></sup> dendrites. Arrows indicate the dendrites of <italic>Orco</italic> expressing ORNs. Western blots and immunohistochemistry showing the specificity of the anti-EST6 antibody are shown in <xref ref-type="supplementary-material" rid="S1">Supplementary Fig. S6</xref>.</p></caption><graphic xlink:href="srep46188-f4"></graphic></fig><table-wrap position="float" id="t1"><label>Table 1</label><caption><title>Active site volume calculated using the CASTp server.</title></caption><table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col><col align="center"></col><col align="center"></col></colgroup><thead valign="bottom"><tr><th align="left" valign="top" charoff="50">Protein</th><th align="center" valign="top" charoff="50">Active Site Volume (Å<sup>3</sup>)</th><th align="center" valign="top" charoff="50">Distance from surface to active site Serine (Å)</th></tr></thead><tbody valign="top"><tr><td align="left" valign="top" charoff="50">EST6 WT FoldX Model</td><td align="center" valign="top" charoff="50">408</td><td align="center" valign="top" charoff="50">15.1</td></tr><tr><td align="left" valign="top" charoff="50">EST6-1 Crystal Structure</td><td align="center" valign="top" charoff="50">935</td><td align="center" valign="top" charoff="50">15.1</td></tr><tr><td align="left" valign="top" charoff="50"><italic>Lc</italic>αE7 (4FNG)</td><td align="center" valign="top" charoff="50">2727</td><td align="center" valign="top" charoff="50">20.2</td></tr><tr><td align="left" valign="top" charoff="50"><italic>Dm</italic>AChE (1QO9)</td><td align="center" valign="top" charoff="50">782</td><td align="center" valign="top" charoff="50">17.2</td></tr><tr><td align="left" valign="top" charoff="50"><italic>Ms</italic>JHE (2FJ0)</td><td align="center" valign="top" charoff="50">1308</td><td align="center" valign="top" charoff="50">18.1</td></tr><tr><td align="left" valign="top" charoff="50">Lipase (1AQL)</td><td align="center" valign="top" charoff="50">3074</td><td align="center" valign="top" charoff="50">17.4</td></tr></tbody></table></table-wrap></floats-group></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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