Caveolae disassemble upon membrane lesioning and foster cell survival
Summary: Repair of lesions in the plasma membrane is key to sustaining cellular homeostasis. Cells maintain cytoplasmic as well as membrane-bound stores of repair proteins that can rapidly precipitate at the site of membrane lesions. However, little is known about the origins of lipids and proteins...
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Format: | Article |
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Elsevier
2024-02-01
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Series: | iScience |
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Online Access: | http://www.sciencedirect.com/science/article/pii/S2589004224000701 |
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author | Martin Štefl Masanari Takamiya Volker Middel Miyase Tekpınar Karin Nienhaus Tanja Beil Sepand Rastegar Uwe Strähle Gerd Ulrich Nienhaus |
author_facet | Martin Štefl Masanari Takamiya Volker Middel Miyase Tekpınar Karin Nienhaus Tanja Beil Sepand Rastegar Uwe Strähle Gerd Ulrich Nienhaus |
author_sort | Martin Štefl |
collection | DOAJ |
description | Summary: Repair of lesions in the plasma membrane is key to sustaining cellular homeostasis. Cells maintain cytoplasmic as well as membrane-bound stores of repair proteins that can rapidly precipitate at the site of membrane lesions. However, little is known about the origins of lipids and proteins for resealing and repair of the plasma membrane. Here we study the dynamics of caveolar proteins after laser-induced lesioning of plasma membranes of mammalian C2C12 tissue culture cells and muscle cells of intact zebrafish embryos. Single-molecule diffusivity measurements indicate that caveolar clusters break up into smaller entities after wounding. Unlike Annexins and Dysferlin, caveolar proteins do not accumulate at the lesion patch. In caveolae-depleted cavin1a knockout zebrafish embryos, lesion patch formation is impaired, and injured cells show reduced survival. Our data suggest that caveolae disassembly releases surplus plasma membrane near the lesion to facilitate membrane repair after initial patch formation for emergency sealing. |
first_indexed | 2024-03-08T12:47:38Z |
format | Article |
id | doaj.art-b4511a54e95f4dbc9f67e39a510c4315 |
institution | Directory Open Access Journal |
issn | 2589-0042 |
language | English |
last_indexed | 2024-03-08T12:47:38Z |
publishDate | 2024-02-01 |
publisher | Elsevier |
record_format | Article |
series | iScience |
spelling | doaj.art-b4511a54e95f4dbc9f67e39a510c43152024-01-21T05:09:56ZengElsevieriScience2589-00422024-02-01272108849Caveolae disassemble upon membrane lesioning and foster cell survivalMartin Štefl0Masanari Takamiya1Volker Middel2Miyase Tekpınar3Karin Nienhaus4Tanja Beil5Sepand Rastegar6Uwe Strähle7Gerd Ulrich Nienhaus8Institute of Applied Physics (APH), Karlsruhe Institute of Technology (KIT), Wolfgang Gaede-Strasse 1, 76131 Karlsruhe, GermanyInstitute of Biological and Chemical Systems (IBCS), Karlsruhe Institute of Technology (KIT), PO Box 3640, 76021 Karlsruhe, GermanyInstitute of Biological and Chemical Systems (IBCS), Karlsruhe Institute of Technology (KIT), PO Box 3640, 76021 Karlsruhe, GermanyInstitute of Applied Physics (APH), Karlsruhe Institute of Technology (KIT), Wolfgang Gaede-Strasse 1, 76131 Karlsruhe, GermanyInstitute of Applied Physics (APH), Karlsruhe Institute of Technology (KIT), Wolfgang Gaede-Strasse 1, 76131 Karlsruhe, GermanyInstitute of Biological and Chemical Systems (IBCS), Karlsruhe Institute of Technology (KIT), PO Box 3640, 76021 Karlsruhe, GermanyInstitute of Biological and Chemical Systems (IBCS), Karlsruhe Institute of Technology (KIT), PO Box 3640, 76021 Karlsruhe, GermanyInstitute of Biological and Chemical Systems (IBCS), Karlsruhe Institute of Technology (KIT), PO Box 3640, 76021 Karlsruhe, Germany; Centre for Organismal Studies (COS), Heidelberg University, Im Neuenheimer Feld 230, 69120 Heidelberg, Germany; Corresponding authorInstitute of Applied Physics (APH), Karlsruhe Institute of Technology (KIT), Wolfgang Gaede-Strasse 1, 76131 Karlsruhe, Germany; Institute of Biological and Chemical Systems (IBCS), Karlsruhe Institute of Technology (KIT), PO Box 3640, 76021 Karlsruhe, Germany; Institute of Nanotechnology (INT), Karlsruhe Institute of Technology (KIT), PO Box 3640, 76021 Karlsruhe, Germany; Department of Physics, University of Illinois at Urbana−Champaign, Urbana, IL 61801, USA; Corresponding authorSummary: Repair of lesions in the plasma membrane is key to sustaining cellular homeostasis. Cells maintain cytoplasmic as well as membrane-bound stores of repair proteins that can rapidly precipitate at the site of membrane lesions. However, little is known about the origins of lipids and proteins for resealing and repair of the plasma membrane. Here we study the dynamics of caveolar proteins after laser-induced lesioning of plasma membranes of mammalian C2C12 tissue culture cells and muscle cells of intact zebrafish embryos. Single-molecule diffusivity measurements indicate that caveolar clusters break up into smaller entities after wounding. Unlike Annexins and Dysferlin, caveolar proteins do not accumulate at the lesion patch. In caveolae-depleted cavin1a knockout zebrafish embryos, lesion patch formation is impaired, and injured cells show reduced survival. Our data suggest that caveolae disassembly releases surplus plasma membrane near the lesion to facilitate membrane repair after initial patch formation for emergency sealing.http://www.sciencedirect.com/science/article/pii/S2589004224000701Membrane architectureCell biology |
spellingShingle | Martin Štefl Masanari Takamiya Volker Middel Miyase Tekpınar Karin Nienhaus Tanja Beil Sepand Rastegar Uwe Strähle Gerd Ulrich Nienhaus Caveolae disassemble upon membrane lesioning and foster cell survival iScience Membrane architecture Cell biology |
title | Caveolae disassemble upon membrane lesioning and foster cell survival |
title_full | Caveolae disassemble upon membrane lesioning and foster cell survival |
title_fullStr | Caveolae disassemble upon membrane lesioning and foster cell survival |
title_full_unstemmed | Caveolae disassemble upon membrane lesioning and foster cell survival |
title_short | Caveolae disassemble upon membrane lesioning and foster cell survival |
title_sort | caveolae disassemble upon membrane lesioning and foster cell survival |
topic | Membrane architecture Cell biology |
url | http://www.sciencedirect.com/science/article/pii/S2589004224000701 |
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