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Lipid accumulation controls the balance between surface connection and scission of caveolae

Caveolae are bulb-shaped invaginations of the plasma membrane (PM) that undergo scission and fusion at the cell surface and are enriched in specific lipids. However, the influence of lipid composition on caveolae surface stability is not well described or understood. Accordingly, we inserted specifi...

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Autores principales: Hubert, Madlen, Larsson, Elin, Vegesna, Naga Venkata Gayathri, Ahnlund, Maria, Johansson, Annika I, Moodie, Lindon WK, Lundmark, Richard
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7239661/
https://www.ncbi.nlm.nih.gov/pubmed/32364496
http://dx.doi.org/10.7554/eLife.55038
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author Hubert, Madlen
Larsson, Elin
Vegesna, Naga Venkata Gayathri
Ahnlund, Maria
Johansson, Annika I
Moodie, Lindon WK
Lundmark, Richard
author_facet Hubert, Madlen
Larsson, Elin
Vegesna, Naga Venkata Gayathri
Ahnlund, Maria
Johansson, Annika I
Moodie, Lindon WK
Lundmark, Richard
author_sort Hubert, Madlen
collection PubMed
description Caveolae are bulb-shaped invaginations of the plasma membrane (PM) that undergo scission and fusion at the cell surface and are enriched in specific lipids. However, the influence of lipid composition on caveolae surface stability is not well described or understood. Accordingly, we inserted specific lipids into the cell PM via membrane fusion and studied their acute effects on caveolae dynamics. We demonstrate that sphingomyelin stabilizes caveolae to the cell surface, whereas cholesterol and glycosphingolipids drive caveolae scission from the PM. Although all three lipids accumulated specifically in caveolae, cholesterol and sphingomyelin were actively sequestered, whereas glycosphingolipids diffused freely. The ATPase EHD2 restricts lipid diffusion and counteracts lipid-induced scission. We propose that specific lipid accumulation in caveolae generates an intrinsically unstable domain prone to scission if not restrained by EHD2 at the caveolae neck. This work provides a mechanistic link between caveolae and their ability to sense the PM lipid composition.
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spelling pubmed-72396612020-05-22 Lipid accumulation controls the balance between surface connection and scission of caveolae Hubert, Madlen Larsson, Elin Vegesna, Naga Venkata Gayathri Ahnlund, Maria Johansson, Annika I Moodie, Lindon WK Lundmark, Richard eLife Biochemistry and Chemical Biology Caveolae are bulb-shaped invaginations of the plasma membrane (PM) that undergo scission and fusion at the cell surface and are enriched in specific lipids. However, the influence of lipid composition on caveolae surface stability is not well described or understood. Accordingly, we inserted specific lipids into the cell PM via membrane fusion and studied their acute effects on caveolae dynamics. We demonstrate that sphingomyelin stabilizes caveolae to the cell surface, whereas cholesterol and glycosphingolipids drive caveolae scission from the PM. Although all three lipids accumulated specifically in caveolae, cholesterol and sphingomyelin were actively sequestered, whereas glycosphingolipids diffused freely. The ATPase EHD2 restricts lipid diffusion and counteracts lipid-induced scission. We propose that specific lipid accumulation in caveolae generates an intrinsically unstable domain prone to scission if not restrained by EHD2 at the caveolae neck. This work provides a mechanistic link between caveolae and their ability to sense the PM lipid composition. eLife Sciences Publications, Ltd 2020-05-04 /pmc/articles/PMC7239661/ /pubmed/32364496 http://dx.doi.org/10.7554/eLife.55038 Text en © 2020, Hubert et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Biochemistry and Chemical Biology
Hubert, Madlen
Larsson, Elin
Vegesna, Naga Venkata Gayathri
Ahnlund, Maria
Johansson, Annika I
Moodie, Lindon WK
Lundmark, Richard
Lipid accumulation controls the balance between surface connection and scission of caveolae
title Lipid accumulation controls the balance between surface connection and scission of caveolae
title_full Lipid accumulation controls the balance between surface connection and scission of caveolae
title_fullStr Lipid accumulation controls the balance between surface connection and scission of caveolae
title_full_unstemmed Lipid accumulation controls the balance between surface connection and scission of caveolae
title_short Lipid accumulation controls the balance between surface connection and scission of caveolae
title_sort lipid accumulation controls the balance between surface connection and scission of caveolae
topic Biochemistry and Chemical Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7239661/
https://www.ncbi.nlm.nih.gov/pubmed/32364496
http://dx.doi.org/10.7554/eLife.55038
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