Caveolae disassemble upon membrane lesioning and foster cell survival

Martin Štefl; Masanari Takamiya; Volker Middel; Miyase Tekpınar; Karin Nienhaus; Tanja Beil; Sepand Rastegar; Uwe Strähle; Gerd Ulrich Nienhaus

doi:10.1016/j.isci.2024.108849

Caveolae disassemble upon membrane lesioning and foster cell survival

iScience. 2024 Jan 9;27(2):108849. doi: 10.1016/j.isci.2024.108849. eCollection 2024 Feb 16.

Authors

Martin Štefl¹, Masanari Takamiya², Volker Middel², Miyase Tekpınar¹, Karin Nienhaus¹, Tanja Beil², Sepand Rastegar², Uwe Strähle^{2

3}, Gerd Ulrich Nienhaus^{1

2

4

5}

Affiliations

¹ Institute of Applied Physics (APH), Karlsruhe Institute of Technology (KIT), Wolfgang Gaede-Strasse 1, 76131 Karlsruhe, Germany.
² Institute of Biological and Chemical Systems (IBCS), Karlsruhe Institute of Technology (KIT), PO Box 3640, 76021 Karlsruhe, Germany.
³ Centre for Organismal Studies (COS), Heidelberg University, Im Neuenheimer Feld 230, 69120 Heidelberg, Germany.
⁴ Institute of Nanotechnology (INT), Karlsruhe Institute of Technology (KIT), PO Box 3640, 76021 Karlsruhe, Germany.
⁵ Department of Physics, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA.

Abstract

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.

Keywords: Cell biology; Membrane architecture.