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Cells Respond to Mechanical Stress by Rapid Disassembly of Caveolae

Identifieur interne : 000978 ( Ncbi/Curation ); précédent : 000977; suivant : 000979

Cells Respond to Mechanical Stress by Rapid Disassembly of Caveolae

Auteurs : Bidisha Sinha [France] ; Darius Köster [France] ; Richard Ruez [France] ; Pauline Gonnord [France] ; Michele Bastiani [Australie] ; Daniel Abankwa [Australie] ; Radu. V. Stan [États-Unis] ; Gillian Butler-Browne [France] ; Benoit Vedie [France] ; Ludger Johannes [France] ; Nobuhiro Morone [Japon] ; Robert G. Parton [Australie] ; Graça Raposo [France] ; Pierre Sens [France] ; Christophe Lamaze [France] ; Pierre Nassoy [France]

Source :

RBID : PMC:3042189

Abstract

SUMMARY

The precise role of caveolae, the characteristic plasma membrane invaginations present in many cells, still remains debated. The high density of caveolae in cells experiencing mechanical stress led us to investigate their role in membrane-mediated mechanical response. Acute mechanical stress induced by cell osmotic swelling or by uniaxial stretching results in the immediate disappearance of caveolae, which is associated with a reduced caveolin/Cavin1 interaction, and an increase of free caveolins at the plasma membrane. Tether pulling force measurements in live cells and in plasma membrane spheres demonstrate that caveola flattening and disassembly is the primary actin and ATP-independent cell response which buffers membrane tension surges during mechanical stress. Conversely, stress release leads to complete caveola reassembly in an actin and ATP-dependent process. The absence of a functional caveola reservoir in myotubes from muscular dystrophic patients enhanced membrane fragility under mechanical stress. Our findings support a new role for caveolae as a physiological membrane reservoir that allows cells to quickly accommodate sudden and acute mechanical stresses.


Url:
DOI: 10.1016/j.cell.2010.12.031
PubMed: 21295700
PubMed Central: 3042189

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PMC:3042189

Le document en format XML

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</placeName>
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<nlm:aff id="A4"> Institut Curie, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires, 26 rue d’Ulm, 75248 Paris Cedex 05, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea> Institut Curie, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires, 26 rue d’Ulm, 75248 Paris Cedex 05</wicri:regionArea>
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<region type="region" nuts="2">Île-de-France</region>
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</affiliation>
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<name sortKey="Gonnord, Pauline" sort="Gonnord, Pauline" uniqKey="Gonnord P" first="Pauline" last="Gonnord">Pauline Gonnord</name>
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<nlm:aff id="A3"> CNRS UMR144, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires, 26 rue d’Ulm, 75248 Paris Cedex 05, France</nlm:aff>
<country xml:lang="fr">France</country>
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<region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Paris</settlement>
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<nlm:aff id="A4"> Institut Curie, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires, 26 rue d’Ulm, 75248 Paris Cedex 05, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea> Institut Curie, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires, 26 rue d’Ulm, 75248 Paris Cedex 05</wicri:regionArea>
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<settlement type="city">Paris</settlement>
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<name sortKey="Bastiani, Michele" sort="Bastiani, Michele" uniqKey="Bastiani M" first="Michele" last="Bastiani">Michele Bastiani</name>
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<name sortKey="Stan, Radu V" sort="Stan, Radu V" uniqKey="Stan R" first="Radu. V." last="Stan">Radu. V. Stan</name>
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<nlm:aff id="A10"> Dartmouth Medical School, Borwell 502W, HB7600, One Medical Center Drive, 03756 Lebanon, NH, USA</nlm:aff>
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<region type="state">New Hampshire</region>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Butler Browne, Gillian" sort="Butler Browne, Gillian" uniqKey="Butler Browne G" first="Gillian" last="Butler-Browne">Gillian Butler-Browne</name>
<affiliation wicri:level="3">
<nlm:aff id="A11"> Institut de Myologie – Hôpital Pitié-Salpétrière, UM76 UPMC, U974 Inserm, UMR7215 - CNRS-AIM, 47, bld de l’hôpital, 75651 Paris cedex 13, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea> Institut de Myologie – Hôpital Pitié-Salpétrière, UM76 UPMC, U974 Inserm, UMR7215 - CNRS-AIM, 47, bld de l’hôpital, 75651 Paris cedex 13</wicri:regionArea>
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<region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Paris</settlement>
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<name sortKey="Vedie, Benoit" sort="Vedie, Benoit" uniqKey="Vedie B" first="Benoit" last="Vedie">Benoit Vedie</name>
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<nlm:aff id="A12"> Laboratoire de Biochimie, Hôpital Européen Georges Pompidou, 20 rue Leblanc, 75015 Paris, France</nlm:aff>
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<wicri:regionArea> Laboratoire de Biochimie, Hôpital Européen Georges Pompidou, 20 rue Leblanc, 75015 Paris</wicri:regionArea>
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<region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Paris</settlement>
</placeName>
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<name sortKey="Johannes, Ludger" sort="Johannes, Ludger" uniqKey="Johannes L" first="Ludger" last="Johannes">Ludger Johannes</name>
<affiliation wicri:level="3">
<nlm:aff id="A3"> CNRS UMR144, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires, 26 rue d’Ulm, 75248 Paris Cedex 05, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea> CNRS UMR144, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires, 26 rue d’Ulm, 75248 Paris Cedex 05</wicri:regionArea>
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<region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Paris</settlement>
</placeName>
</affiliation>
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<nlm:aff id="A4"> Institut Curie, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires, 26 rue d’Ulm, 75248 Paris Cedex 05, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea> Institut Curie, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires, 26 rue d’Ulm, 75248 Paris Cedex 05</wicri:regionArea>
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<region type="region" nuts="2">Île-de-France</region>
<settlement type="city">Paris</settlement>
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</affiliation>
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<name sortKey="Morone, Nobuhiro" sort="Morone, Nobuhiro" uniqKey="Morone N" first="Nobuhiro" last="Morone">Nobuhiro Morone</name>
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<nlm:aff id="A13"> National Center of Neurology and Psychiatry, National Institute of Neuroscience, Department of Ultrastructural Research, 4-1-1 Ogawa-Higashi, Kodaira, Tokyo 187-8502, Japan</nlm:aff>
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<nlm:aff id="A8"> The University of Queensland, Institute for Molecular Bioscience, Brisbane, Queensland 4072, Australia</nlm:aff>
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<wicri:regionArea> The University of Queensland, Institute for Molecular Bioscience, Brisbane, Queensland 4072</wicri:regionArea>
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<nlm:aff id="A9"> Center for Microscopy and Microanalysis, Brisbane, Queensland 4072, Australia</nlm:aff>
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<wicri:regionArea> Center for Microscopy and Microanalysis, Brisbane, Queensland 4072</wicri:regionArea>
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<name sortKey="Raposo, Graca" sort="Raposo, Graca" uniqKey="Raposo G" first="Graça" last="Raposo">Graça Raposo</name>
<affiliation wicri:level="1">
<nlm:aff id="A3"> CNRS UMR144, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires, 26 rue d’Ulm, 75248 Paris Cedex 05, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea> CNRS UMR144, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires, 26 rue d’Ulm, 75248 Paris Cedex 05</wicri:regionArea>
<wicri:noRegion>75248 Paris Cedex 05</wicri:noRegion>
<wicri:noRegion>75248 Paris Cedex 05</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="A5"> PICT IBiSA Institut Curie, Laboratoire Structure et Compartiments Membranaires, Institut Curie, 26 rue d’Ulm, 75248 Paris Cedex 05, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea> PICT IBiSA Institut Curie, Laboratoire Structure et Compartiments Membranaires, Institut Curie, 26 rue d’Ulm, 75248 Paris Cedex 05</wicri:regionArea>
<wicri:noRegion>75248 Paris Cedex 05</wicri:noRegion>
<wicri:noRegion>75248 Paris Cedex 05</wicri:noRegion>
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<nlm:aff id="A6"> Centre de Recherche, Laboratoire Structure et Compartiments Membranaires, Institut Curie, 26 rue d’Ulm, 75248 Paris Cedex 05, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea> Centre de Recherche, Laboratoire Structure et Compartiments Membranaires, Institut Curie, 26 rue d’Ulm, 75248 Paris Cedex 05</wicri:regionArea>
<wicri:noRegion>75248 Paris Cedex 05</wicri:noRegion>
<wicri:noRegion>75248 Paris Cedex 05</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Sens, Pierre" sort="Sens, Pierre" uniqKey="Sens P" first="Pierre" last="Sens">Pierre Sens</name>
<affiliation wicri:level="1">
<nlm:aff id="A7"> ESPCI, CNRS-UMR 7083 - Physico-Chimie Théorique, 10 rue Vauquelin, 75231 Paris Cedex 05, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea> ESPCI, CNRS-UMR 7083 - Physico-Chimie Théorique, 10 rue Vauquelin, 75231 Paris Cedex 05</wicri:regionArea>
<wicri:noRegion>75231 Paris Cedex 05</wicri:noRegion>
<wicri:noRegion>75231 Paris Cedex 05</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Lamaze, Christophe" sort="Lamaze, Christophe" uniqKey="Lamaze C" first="Christophe" last="Lamaze">Christophe Lamaze</name>
<affiliation wicri:level="1">
<nlm:aff id="A3"> CNRS UMR144, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires, 26 rue d’Ulm, 75248 Paris Cedex 05, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea> CNRS UMR144, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires, 26 rue d’Ulm, 75248 Paris Cedex 05</wicri:regionArea>
<wicri:noRegion>75248 Paris Cedex 05</wicri:noRegion>
<wicri:noRegion>75248 Paris Cedex 05</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="A4"> Institut Curie, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires, 26 rue d’Ulm, 75248 Paris Cedex 05, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea> Institut Curie, Centre de Recherche, Laboratoire Trafic, Signalisation et Ciblage Intracellulaires, 26 rue d’Ulm, 75248 Paris Cedex 05</wicri:regionArea>
<wicri:noRegion>75248 Paris Cedex 05</wicri:noRegion>
<wicri:noRegion>75248 Paris Cedex 05</wicri:noRegion>
</affiliation>
</author>
<author>
<name sortKey="Nassoy, Pierre" sort="Nassoy, Pierre" uniqKey="Nassoy P" first="Pierre" last="Nassoy">Pierre Nassoy</name>
<affiliation wicri:level="1">
<nlm:aff id="A1"> Université P. et M. Curie/CNRS UMR168, Centre de Recherche, Laboratoire Physico-Chimie, 26 rue d’Ulm, 75248 Paris Cedex 05, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea> Université P. et M. Curie/CNRS UMR168, Centre de Recherche, Laboratoire Physico-Chimie, 26 rue d’Ulm, 75248 Paris Cedex 05</wicri:regionArea>
<wicri:noRegion>75248 Paris Cedex 05</wicri:noRegion>
<wicri:noRegion>75248 Paris Cedex 05</wicri:noRegion>
</affiliation>
<affiliation wicri:level="1">
<nlm:aff id="A2"> Institut Curie, Centre de Recherche, Laboratoire Physico-Chimie, 26 rue d’Ulm, 75248 Paris Cedex 05, France</nlm:aff>
<country xml:lang="fr">France</country>
<wicri:regionArea> Institut Curie, Centre de Recherche, Laboratoire Physico-Chimie, 26 rue d’Ulm, 75248 Paris Cedex 05</wicri:regionArea>
<wicri:noRegion>75248 Paris Cedex 05</wicri:noRegion>
<wicri:noRegion>75248 Paris Cedex 05</wicri:noRegion>
</affiliation>
</author>
</analytic>
<series>
<title level="j">Cell</title>
<idno type="ISSN">0092-8674</idno>
<idno type="eISSN">1097-4172</idno>
<imprint>
<date when="2011">2011</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc>
<textClass></textClass>
</profileDesc>
</teiHeader>
<front>
<div type="abstract" xml:lang="en">
<title>SUMMARY</title>
<p id="P3">The precise role of caveolae, the characteristic plasma membrane invaginations present in many cells, still remains debated. The high density of caveolae in cells experiencing mechanical stress led us to investigate their role in membrane-mediated mechanical response. Acute mechanical stress induced by cell osmotic swelling or by uniaxial stretching results in the immediate disappearance of caveolae, which is associated with a reduced caveolin/Cavin1 interaction, and an increase of free caveolins at the plasma membrane. Tether pulling force measurements in live cells and in plasma membrane spheres demonstrate that caveola flattening and disassembly is the primary actin and ATP-independent cell response which buffers membrane tension surges during mechanical stress. Conversely, stress release leads to complete caveola reassembly in an actin and ATP-dependent process. The absence of a functional caveola reservoir in myotubes from muscular dystrophic patients enhanced membrane fragility under mechanical stress. Our findings support a new role for caveolae as a physiological membrane reservoir that allows cells to quickly accommodate sudden and acute mechanical stresses.</p>
</div>
</front>
</TEI>
</record>

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