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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Main Authors: Martin Štefl, Masanari Takamiya, Volker Middel, Miyase Tekpınar, Karin Nienhaus, Tanja Beil, Sepand Rastegar, Uwe Strähle, Gerd Ulrich Nienhaus
Format: Article
Language:English
Published: Elsevier 2024-02-01
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.
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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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