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

Lolo FN, Walani N, Seemann E, Zalvidea D, Maria Pavon D, Cojoc G, Zamai M, Viaris De Lesegno C, Martinez De Benito F, Sanchez-Alvarez M, Jose Uriarte J, Echarri A, Jimenez-Carretero D, Escolano JC, Sanchez SA, Caiolfa VR, Navajas D, Trepat X, Guck J, Lamaze C, Roca-Cusachs P, Kessels MM, Qualmann B, Arroyo M, Del Pozo MA (2023)

Publication Type: Journal article

Publication year: 2023

Journal

Nature Cell Biology Nature Research

Book Volume: 25

Pages Range: 120-133

Journal Issue: 1

DOI: 10.1038/s41556-022-01034-3

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.

Authors with CRIS profile

Jochen Guck

Involved external institutions

Spanish National Center for Cardiovascular Research / Centro Nacional de Investigaciones Cardiovasculares Carlos III (CNIC) ES Spain (ES) Instituto de Bioingeniería de Cataluña / Institute for Bioengineering of Catalonia ES Spain (ES) Friedrich-Schiller-Universität Jena DE Germany (DE) Barcelona Institute of Science and Technology - BIST ES Spain (ES) Technische Universität Dresden DE Germany (DE) PSL Research University / Université de recherche Paris Sciences et Lettres FR France (FR) Universitat de Barcelona (UB) / University of Barcelona ES Spain (ES) Universidad de Concepcion CL Chile (CL)

How to cite

APA:

Lolo, F.-N., Walani, N., Seemann, E., Zalvidea, D., Maria Pavon, D., Cojoc, G.,... Del Pozo, M.A. (2023). Caveolin-1 dolines form a distinct and rapid caveolae-independent mechanoadaptation system. Nature Cell Biology, 25(1), 120-133. https://doi.org/10.1038/s41556-022-01034-3

MLA:

Lolo, Fidel-Nicolas, et al. "Caveolin-1 dolines form a distinct and rapid caveolae-independent mechanoadaptation system." Nature Cell Biology 25.1 (2023): 120-133.

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