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...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2020-05-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/55038 |
| _version_ | 1811181028325195776 |
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| author | Madlen Hubert Elin Larsson Naga Venkata Gayathri Vegesna Maria Ahnlund Annika I Johansson Lindon WK Moodie Richard Lundmark |
| author_facet | Madlen Hubert Elin Larsson Naga Venkata Gayathri Vegesna Maria Ahnlund Annika I Johansson Lindon WK Moodie Richard Lundmark |
| author_sort | Madlen Hubert |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-11T09:11:28Z |
| format | Article |
| id | doaj.art-464ee09725cb4eab999f68a395c71564 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:11:28Z |
| publishDate | 2020-05-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-464ee09725cb4eab999f68a395c715642022-12-22T04:32:29ZengeLife Sciences Publications LtdeLife2050-084X2020-05-01910.7554/eLife.55038Lipid accumulation controls the balance between surface connection and scission of caveolaeMadlen Hubert0Elin Larsson1Naga Venkata Gayathri Vegesna2Maria Ahnlund3Annika I Johansson4Lindon WK Moodie5Richard Lundmark6https://orcid.org/0000-0001-9104-724XDepartment of Integrative Medical Biology, Umeå University, Umeå, SwedenDepartment of Integrative Medical Biology, Umeå University, Umeå, SwedenDepartment of Integrative Medical Biology, Umeå University, Umeå, SwedenSwedish Metabolomics Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå, SwedenSwedish Metabolomics Centre, Department of Molecular Biology, Umeå University, Umeå, SwedenDepartment of Chemistry, Umeå University, Umeå, SwedenDepartment of Integrative Medical Biology, Umeå University, Umeå, SwedenCaveolae 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.https://elifesciences.org/articles/55038caveolaeEHD2Lipidscell surface stabilitycholesterolfusogenic liposomes |
| spellingShingle | Madlen Hubert Elin Larsson Naga Venkata Gayathri Vegesna Maria Ahnlund Annika I Johansson Lindon WK Moodie Richard Lundmark Lipid accumulation controls the balance between surface connection and scission of caveolae eLife caveolae EHD2 Lipids cell surface stability cholesterol fusogenic liposomes |
| 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 | caveolae EHD2 Lipids cell surface stability cholesterol fusogenic liposomes |
| url | https://elifesciences.org/articles/55038 |
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