Caveolin-1-Mediated Apolipoprotein A-I Membrane Binding Sites Are Not Required for Cholesterol Efflux
Identifieur interne : 002387 ( Pmc/Checkpoint ); précédent : 002386; suivant : 002388Caveolin-1-Mediated Apolipoprotein A-I Membrane Binding Sites Are Not Required for Cholesterol Efflux
Auteurs : Soazig Le Lay [France] ; Macarena Rodriguez [Australie] ; Wendy Jessup [Australie] ; Carles Rentero [Australie] ; Qiong Li [Australie] ; Siân Cartland [Australie] ; Thomas Grewal [Australie] ; Katharina Gaus [Australie]Source :
- PLoS ONE [ 1932-6203 ] ; 2011.
Abstract
Caveolin-1 (Cav1), a structural protein required for the formation of invaginated membrane domains known as caveolae, has been implicated in cholesterol trafficking and homeostasis. Here we investigated the contribution of Cav1 to apolipoprotein A-I (apoA-I) cell surface binding and intracellular processing using mouse embryonic fibroblasts (MEFs) derived from wild type (WT) or Cav1-deficient (Cav1−/−) animals. We found that cells expressing Cav1 have 2.6-fold more apoA-I binding sites than Cav1−/− cells although these additional binding sites are not associated with detergent-free lipid rafts. Further, Cav1-mediated binding targets apoA-I for internalization and degradation and these processes are not correlated to cholesterol efflux. Despite lower apoA-I binding, cholesterol efflux from Cav1−/− MEFs is 1.7-fold higher than from WT MEFs. Stimulation of ABCA1 expression with an LXR agonist enhances cholesterol efflux from both WT and Cav1−/− cells without increasing apoA-I surface binding or affecting apoA-I processing. Our results indicate that there are at least two independent lipid binding sites for apoA-I; Cav1-mediated apoA-I surface binding and uptake is not linked to cholesterol efflux, indicating that membrane domains other than caveolae regulate ABCA1-mediated cholesterol efflux.
Url:
DOI: 10.1371/journal.pone.0023353
PubMed: 21858084
PubMed Central: 3155548
Affiliations:
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<front><div type="abstract" xml:lang="en"><p>Caveolin-1 (Cav1), a structural protein required for the formation of invaginated membrane domains known as caveolae, has been implicated in cholesterol trafficking and homeostasis. Here we investigated the contribution of Cav1 to apolipoprotein A-I (apoA-I) cell surface binding and intracellular processing using mouse embryonic fibroblasts (MEFs) derived from wild type (WT) or Cav1-deficient (Cav1<sup>−/−</sup>
) animals. We found that cells expressing Cav1 have 2.6-fold more apoA-I binding sites than Cav1<sup>−/−</sup>
cells although these additional binding sites are not associated with detergent-free lipid rafts. Further, Cav1-mediated binding targets apoA-I for internalization and degradation and these processes are not correlated to cholesterol efflux. Despite lower apoA-I binding, cholesterol efflux from Cav1<sup>−/−</sup>
MEFs is 1.7-fold higher than from WT MEFs. Stimulation of ABCA1 expression with an LXR agonist enhances cholesterol efflux from both WT and Cav1<sup>−/−</sup>
cells without increasing apoA-I surface binding or affecting apoA-I processing. Our results indicate that there are at least two independent lipid binding sites for apoA-I; Cav1-mediated apoA-I surface binding and uptake is not linked to cholesterol efflux, indicating that membrane domains other than caveolae regulate ABCA1-mediated cholesterol efflux.</p>
</div>
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</author>
<author><name sortKey="Cavelier, C" uniqKey="Cavelier C">C Cavelier</name>
</author>
<author><name sortKey="Fuchs, S" uniqKey="Fuchs S">S Fuchs</name>
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<author><name sortKey="Volker, W" uniqKey="Volker W">W Volker</name>
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<author><name sortKey="Tall, Ar" uniqKey="Tall A">AR Tall</name>
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<biblStruct><analytic><author><name sortKey="Witting, Sr" uniqKey="Witting S">SR Witting</name>
</author>
<author><name sortKey="Maiorano, Jn" uniqKey="Maiorano J">JN Maiorano</name>
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</listBibl>
</div1>
</back>
</TEI>
<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosone</journal-id>
<journal-title-group><journal-title>PLoS ONE</journal-title>
</journal-title-group>
<issn pub-type="epub">1932-6203</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">21858084</article-id>
<article-id pub-id-type="pmc">3155548</article-id>
<article-id pub-id-type="publisher-id">PONE-D-11-09730</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0023353</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v2"><subject>Biology</subject>
<subj-group><subject>Biochemistry</subject>
<subj-group><subject>Cytochemistry</subject>
<subj-group><subject>Cell Membrane</subject>
<subj-group><subject>Membrane Proteins</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group><subject>Lipids</subject>
<subj-group><subject>Sterols</subject>
</subj-group>
</subj-group>
<subj-group><subject>Proteins</subject>
<subj-group><subject>Lipoproteins</subject>
<subj-group><subject>Apolipoproteins</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group><subject>Model Organisms</subject>
<subj-group><subject>Animal Models</subject>
<subj-group><subject>Mouse</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group><subject>Molecular Cell Biology</subject>
<subj-group><subject>Membranes and Sorting</subject>
</subj-group>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Caveolin-1-Mediated Apolipoprotein A-I Membrane Binding Sites Are Not Required for Cholesterol Efflux</article-title>
<alt-title alt-title-type="running-head">Caveolin-1 and Apolipoprotein A-I</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Le Lay</surname>
<given-names>Soazig</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Rodriguez</surname>
<given-names>Macarena</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jessup</surname>
<given-names>Wendy</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Rentero</surname>
<given-names>Carles</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="author-notes" rid="fn1"><sup>¤</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Li</surname>
<given-names>Qiong</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Cartland</surname>
<given-names>Siân</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Grewal</surname>
<given-names>Thomas</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gaus</surname>
<given-names>Katharina</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>*</sup>
</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>1</label>
<addr-line>Centre de Recherche des Cordeliers, INSERM, U872, Paris, France</addr-line>
</aff>
<aff id="aff2"><label>2</label>
<addr-line>Centre for Vascular Research, University of New South Wales, Sydney, Australia</addr-line>
</aff>
<aff id="aff3"><label>3</label>
<addr-line>Faculty of Pharmacy, University of Sydney, Sydney, Australia</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Johannes</surname>
<given-names>Ludger</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1">Institut Curie, France</aff>
<author-notes><corresp id="cor1">* E-mail: <email>k.gaus@unsw.edu.au</email>
</corresp>
<fn fn-type="con"><p>Conceived and designed the experiments: KG TG WJ. Performed the experiments: SLL MR WJ CR QL SC KG. Analyzed the data: SLL MR WJ CR QL SC KG. Contributed reagents/materials/analysis tools: SLL WJ KG. Wrote the paper: TG KG.</p>
</fn>
<fn id="fn1" fn-type="current-aff"><label>¤</label>
<p>Current address: Departament de Biologia Cel·lular, Immunologia i Neurociències, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Facultat de Medicina, Universitat de Barcelona, Barcelona, Spain</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><year>2011</year>
</pub-date>
<pub-date pub-type="epub"><day>12</day>
<month>8</month>
<year>2011</year>
</pub-date>
<volume>6</volume>
<issue>8</issue>
<elocation-id>e23353</elocation-id>
<history><date date-type="received"><day>30</day>
<month>5</month>
<year>2011</year>
</date>
<date date-type="accepted"><day>13</day>
<month>7</month>
<year>2011</year>
</date>
</history>
<permissions><copyright-statement>Le Lay et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</copyright-statement>
<copyright-year>2011</copyright-year>
</permissions>
<abstract><p>Caveolin-1 (Cav1), a structural protein required for the formation of invaginated membrane domains known as caveolae, has been implicated in cholesterol trafficking and homeostasis. Here we investigated the contribution of Cav1 to apolipoprotein A-I (apoA-I) cell surface binding and intracellular processing using mouse embryonic fibroblasts (MEFs) derived from wild type (WT) or Cav1-deficient (Cav1<sup>−/−</sup>
) animals. We found that cells expressing Cav1 have 2.6-fold more apoA-I binding sites than Cav1<sup>−/−</sup>
cells although these additional binding sites are not associated with detergent-free lipid rafts. Further, Cav1-mediated binding targets apoA-I for internalization and degradation and these processes are not correlated to cholesterol efflux. Despite lower apoA-I binding, cholesterol efflux from Cav1<sup>−/−</sup>
MEFs is 1.7-fold higher than from WT MEFs. Stimulation of ABCA1 expression with an LXR agonist enhances cholesterol efflux from both WT and Cav1<sup>−/−</sup>
cells without increasing apoA-I surface binding or affecting apoA-I processing. Our results indicate that there are at least two independent lipid binding sites for apoA-I; Cav1-mediated apoA-I surface binding and uptake is not linked to cholesterol efflux, indicating that membrane domains other than caveolae regulate ABCA1-mediated cholesterol efflux.</p>
</abstract>
<counts><page-count count="11"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Australie</li>
<li>France</li>
</country>
<region><li>Nouvelle-Galles du Sud</li>
<li>Île-de-France</li>
</region>
<settlement><li>Paris</li>
<li>Sydney</li>
</settlement>
<orgName><li>Université de Sydney</li>
</orgName>
</list>
<tree><country name="France"><region name="Île-de-France"><name sortKey="Le Lay, Soazig" sort="Le Lay, Soazig" uniqKey="Le Lay S" first="Soazig" last="Le Lay">Soazig Le Lay</name>
</region>
</country>
<country name="Australie"><region name="Nouvelle-Galles du Sud"><name sortKey="Rodriguez, Macarena" sort="Rodriguez, Macarena" uniqKey="Rodriguez M" first="Macarena" last="Rodriguez">Macarena Rodriguez</name>
</region>
<name sortKey="Cartland, Sian" sort="Cartland, Sian" uniqKey="Cartland S" first="Siân" last="Cartland">Siân Cartland</name>
<name sortKey="Gaus, Katharina" sort="Gaus, Katharina" uniqKey="Gaus K" first="Katharina" last="Gaus">Katharina Gaus</name>
<name sortKey="Grewal, Thomas" sort="Grewal, Thomas" uniqKey="Grewal T" first="Thomas" last="Grewal">Thomas Grewal</name>
<name sortKey="Jessup, Wendy" sort="Jessup, Wendy" uniqKey="Jessup W" first="Wendy" last="Jessup">Wendy Jessup</name>
<name sortKey="Li, Qiong" sort="Li, Qiong" uniqKey="Li Q" first="Qiong" last="Li">Qiong Li</name>
<name sortKey="Rentero, Carles" sort="Rentero, Carles" uniqKey="Rentero C" first="Carles" last="Rentero">Carles Rentero</name>
</country>
</tree>
</affiliations>
</record>
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