Caveolin-1 dolines form a distinct and rapid caveolae-independent mechanoadaptation system

Research output: Contribution to journalResearch articleContributedpeer-review

Contributors

  • Fidel Nicolás Lolo - , Instituto de Salud Carlos III (Author)
  • Nikhil Walani - , UPC Polytechnic University of Catalonia (Barcelona Tech) (Author)
  • Eric Seemann - , Friedrich Schiller University Jena (Author)
  • Dobryna Zalvidea - , Institute for Bioengineering of Catalonia, PreciPoint GmbH (Author)
  • Dácil María Pavón - , Instituto de Salud Carlos III, Allergy Therapeutics S.L. (Parque Tecnológico Tecnoalcala) (Author)
  • Gheorghe Cojoc - , Chair of Cellular Machines (Author)
  • Moreno Zamai - , Instituto de Salud Carlos III (Author)
  • Christine Viaris de Lesegno - , INSERM - Institut national de la santé et de la recherche médicale (Author)
  • Fernando Martínez de Benito - , Instituto de Salud Carlos III, CIBER - Center for Biomedical Research Network (Author)
  • Miguel Sánchez-Álvarez - , Instituto de Salud Carlos III (Author)
  • Juan José Uriarte - , University of Barcelona (Author)
  • Asier Echarri - , Instituto de Salud Carlos III (Author)
  • Daniel Jiménez-Carretero - , Instituto de Salud Carlos III (Author)
  • Joan Carles Escolano - , TUD Dresden University of Technology, Max Planck Institute for the Science of Light (Author)
  • Susana A. Sánchez - , Universidad de Concepción (Author)
  • Valeria R. Caiolfa - , Instituto de Salud Carlos III, Vita-Salute San Raffaele University (Author)
  • Daniel Navajas - , Institute for Bioengineering of Catalonia, University of Barcelona (Author)
  • Xavier Trepat - , Institute for Bioengineering of Catalonia, University of Barcelona, ICREA, CIBER - Center for Biomedical Research Network (Author)
  • Jochen Guck - , Chair of Cellular Machines, Max Planck Institute for the Science of Light (Author)
  • Christophe Lamaze - , INSERM - Institut national de la santé et de la recherche médicale (Author)
  • Pere Roca-Cusachs - , Institute for Bioengineering of Catalonia, University of Barcelona (Author)
  • Michael M. Kessels - , Friedrich Schiller University Jena (Author)
  • Britta Qualmann - , Friedrich Schiller University Jena (Author)
  • Marino Arroyo - , UPC Polytechnic University of Catalonia (Barcelona Tech), Institute for Bioengineering of Catalonia (Author)
  • Miguel A. del Pozo - , Instituto de Salud Carlos III (Author)

Abstract

In response to different types and intensities of mechanical force, cells modulate their physical properties and adapt their plasma membrane (PM). Caveolae are PM nano-invaginations that contribute to mechanoadaptation, buffering tension changes. However, whether core caveolar proteins contribute to PM tension accommodation independently from the caveolar assembly is unknown. Here we provide experimental and computational evidence supporting that caveolin-1 confers deformability and mechanoprotection independently from caveolae, through modulation of PM curvature. Freeze-fracture electron microscopy reveals that caveolin-1 stabilizes non-caveolar invaginations—dolines—capable of responding to low-medium mechanical forces, impacting downstream mechanotransduction and conferring mechanoprotection to cells devoid of caveolae. Upon cavin-1/PTRF binding, doline size is restricted and membrane buffering is limited to relatively high forces, capable of flattening caveolae. Thus, caveolae and dolines constitute two distinct albeit complementary components of a buffering system that allows cells to adapt efficiently to a broad range of mechanical stimuli.

Details

Original languageEnglish
Pages (from-to)120-133
Number of pages14
JournalNature cell biology
Volume25
Issue number1
Publication statusPublished - Jan 2023
Peer-reviewedYes

External IDs

PubMed 36543981

Keywords

ASJC Scopus subject areas

Keywords

  • Proteins/metabolism, Mechanotransduction, Cellular, Cell Membrane/metabolism, Caveolin 1/metabolism, Caveolae/metabolism