Cells respond to mechanical stress by rapid disassembly of caveolae

The functions of caveolae, the characteristic plasma membrane invaginations, remain debated. Their abundance in cells experiencing mechanical stress led us to investigate their role in membrane-mediated mechanical response. Acute mechanical stress induced by osmotic swelling or by uniaxial stretchin...

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Vydáno v:Cell Ročník 144; číslo 3; s. 402
Hlavní autoři: Sinha, Bidisha, Köster, Darius, Ruez, Richard, Gonnord, Pauline, Bastiani, Michele, Abankwa, Daniel, Stan, Radu V, Butler-Browne, Gillian, Vedie, Benoit, Johannes, Ludger, Morone, Nobuhiro, Parton, Robert G, Raposo, Graça, Sens, Pierre, Lamaze, Christophe, Nassoy, Pierre
Médium: Journal Article
Jazyk:angličtina
Vydáno: United States 04.02.2011
Témata:
ISSN:1097-4172, 1097-4172
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Abstract The functions of caveolae, the characteristic plasma membrane invaginations, remain debated. Their abundance in cells experiencing mechanical stress led us to investigate their role in membrane-mediated mechanical response. Acute mechanical stress induced by osmotic swelling or by uniaxial stretching results in a rapid disappearance of caveolae, in a reduced caveolin/Cavin1 interaction, and in an increase of free caveolins at the plasma membrane. Tether-pulling force measurements in cells and in plasma membrane spheres demonstrate that caveola flattening and disassembly is the primary actin- and ATP-independent cell response that 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 quickly accommodates sudden and acute mechanical stresses.
AbstractList The functions of caveolae, the characteristic plasma membrane invaginations, remain debated. Their abundance in cells experiencing mechanical stress led us to investigate their role in membrane-mediated mechanical response. Acute mechanical stress induced by osmotic swelling or by uniaxial stretching results in a rapid disappearance of caveolae, in a reduced caveolin/Cavin1 interaction, and in an increase of free caveolins at the plasma membrane. Tether-pulling force measurements in cells and in plasma membrane spheres demonstrate that caveola flattening and disassembly is the primary actin- and ATP-independent cell response that 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 quickly accommodates sudden and acute mechanical stresses.The functions of caveolae, the characteristic plasma membrane invaginations, remain debated. Their abundance in cells experiencing mechanical stress led us to investigate their role in membrane-mediated mechanical response. Acute mechanical stress induced by osmotic swelling or by uniaxial stretching results in a rapid disappearance of caveolae, in a reduced caveolin/Cavin1 interaction, and in an increase of free caveolins at the plasma membrane. Tether-pulling force measurements in cells and in plasma membrane spheres demonstrate that caveola flattening and disassembly is the primary actin- and ATP-independent cell response that 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 quickly accommodates sudden and acute mechanical stresses.
The functions of caveolae, the characteristic plasma membrane invaginations, remain debated. Their abundance in cells experiencing mechanical stress led us to investigate their role in membrane-mediated mechanical response. Acute mechanical stress induced by osmotic swelling or by uniaxial stretching results in a rapid disappearance of caveolae, in a reduced caveolin/Cavin1 interaction, and in an increase of free caveolins at the plasma membrane. Tether-pulling force measurements in cells and in plasma membrane spheres demonstrate that caveola flattening and disassembly is the primary actin- and ATP-independent cell response that 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 quickly accommodates sudden and acute mechanical stresses.
Author Sinha, Bidisha
Morone, Nobuhiro
Nassoy, Pierre
Butler-Browne, Gillian
Parton, Robert G
Köster, Darius
Raposo, Graça
Gonnord, Pauline
Ruez, Richard
Johannes, Ludger
Sens, Pierre
Abankwa, Daniel
Lamaze, Christophe
Vedie, Benoit
Stan, Radu V
Bastiani, Michele
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  surname: Sinha
  fullname: Sinha, Bidisha
  organization: Université P. et M. Curie/CNRS UMR, Paris, France
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  givenname: Darius
  surname: Köster
  fullname: Köster, Darius
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  givenname: Richard
  surname: Ruez
  fullname: Ruez, Richard
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  givenname: Pauline
  surname: Gonnord
  fullname: Gonnord, Pauline
– sequence: 5
  givenname: Michele
  surname: Bastiani
  fullname: Bastiani, Michele
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  givenname: Daniel
  surname: Abankwa
  fullname: Abankwa, Daniel
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  fullname: Parton, Robert G
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  fullname: Raposo, Graça
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  fullname: Sens, Pierre
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– sequence: 16
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  surname: Nassoy
  fullname: Nassoy, Pierre
BackLink https://www.ncbi.nlm.nih.gov/pubmed/21295700$$D View this record in MEDLINE/PubMed
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Snippet The functions of caveolae, the characteristic plasma membrane invaginations, remain debated. Their abundance in cells experiencing mechanical stress led us to...
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SubjectTerms Actins - physiology
Adenosine Triphosphate - physiology
Animals
Caveolae - physiology
Caveolae - ultrastructure
Cell Line
Endothelial Cells - cytology
Endothelial Cells - physiology
Humans
Mice
Muscle Cells - cytology
Muscle Cells - physiology
Stress, Mechanical
Title Cells respond to mechanical stress by rapid disassembly of caveolae
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