A mechanosensing mechanism controls plasma membrane shape homeostasis at the nanoscale

Author:

Quiroga Xarxa12,Walani Nikhil3ORCID,Disanza Andrea4,Chavero Albert5,Mittens Alexandra1,Tebar Francesc5,Trepat Xavier1ORCID,Parton Robert G6ORCID,Geli María Isabel7ORCID,Scita Giorgio48ORCID,Arroyo Marino1910,Le Roux Anabel-Lise1ORCID,Roca-Cusachs Pere12ORCID

Affiliation:

1. Institute for Bioengineering of Catalonia, the Barcelona Institute of Technology (BIST)

2. Departament de Biomedicina, Unitat de Biofísica i Bioenginyeria, Facultat de Medicina i Ciències de la Salut, Universitat de Barcelona

3. Department of Applied Mechanics, IIT Delhi

4. IFOM ETS - The AIRC Institute of Molecular Oncology

5. Departament de Biomedicina, Unitat de Biologia Cel·lular, Facultat de Medicina i Ciències de la Salut, Centre de Recerca Biomèdica CELLEX, Institut d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Universitat de Barcelona

6. Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland

7. Institute for Molecular Biology of Barcelona (CSIC)

8. Department of Oncology and Haemato-Oncology, University of Milan

9. Universitat Politècnica de Catalunya (UPC), Campus Nord, Carrer de Jordi Girona

10. Centre Internacional de Mètodes Numèrics en Enginyeria (CIMNE)

Abstract

As cells migrate and experience forces from their surroundings, they constantly undergo mechanical deformations which reshape their plasma membrane (PM). To maintain homeostasis, cells need to detect and restore such changes, not only in terms of overall PM area and tension as previously described, but also in terms of local, nanoscale topography. Here, we describe a novel phenomenon, by which cells sense and restore mechanically induced PM nanoscale deformations. We show that cell stretch and subsequent compression reshape the PM in a way that generates local membrane evaginations in the 100 nm scale. These evaginations are recognized by I-BAR proteins, which triggers a burst of actin polymerization mediated by Rac1 and Arp2/3. The actin polymerization burst subsequently re-flattens the evagination, completing the mechanochemical feedback loop. Our results demonstrate a new mechanosensing mechanism for PM shape homeostasis, with potential applicability in different physiological scenarios.

Funder

Ministerio de Ciencia e Innovación

European Commission

Generalitat de Catalunya

Fundació la Marató de TV3

'la Caixa' Foundation

Associazione Italiana per la Ricerca sul Cancro

italian ministry of university

European Research Council

Institució Catalana de Recerca i Estudis Avançats

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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