Membrane tension controls adhesion positioning at the leading edge of cells

Author:

Pontes Bruno12,Monzo Pascale13ORCID,Gole Laurent1,Le Roux Anabel-Lise4ORCID,Kosmalska Anita Joanna4,Tam Zhi Yang1,Luo Weiwei1,Kan Sophie1,Viasnoff Virgile15,Roca-Cusachs Pere46,Tucker-Kellogg Lisa17,Gauthier Nils C.13ORCID

Affiliation:

1. Mechanobiology Institute, National University of Singapore, Singapore

2. Laboratório de Pinças Óticas, Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil

3. Institute FIRC (Italian Foundation for Cancer Research) of Molecular Oncology (IFOM-FIRC), Milan, Italy

4. Institute for Bioengineering of Catalonia, The Barcelona Institute of Science and Technology, Barcelona, Spain

5. Centre National de la Recherche Scientifique, École Supérieure de Physique et de Chimie Industrielles Paristech, Paris, France

6. University of Barcelona, Barcelona, Spain

7. Centre for Computational Biology, Duke–National University of Singapore Graduate Medical School, Singapore

Abstract

Cell migration is dependent on adhesion dynamics and actin cytoskeleton remodeling at the leading edge. These events may be physically constrained by the plasma membrane. Here, we show that the mechanical signal produced by an increase in plasma membrane tension triggers the positioning of new rows of adhesions at the leading edge. During protrusion, as membrane tension increases, velocity slows, and the lamellipodium buckles upward in a myosin II–independent manner. The buckling occurs between the front of the lamellipodium, where nascent adhesions are positioned in rows, and the base of the lamellipodium, where a vinculin-dependent clutch couples actin to previously positioned adhesions. As membrane tension decreases, protrusion resumes and buckling disappears, until the next cycle. We propose that the mechanical signal of membrane tension exerts upstream control in mechanotransduction by periodically compressing and relaxing the lamellipodium, leading to the positioning of adhesions at the leading edge of cells.

Funder

Mechanobiology Institute

National Research Foundation Singapore

Ministry of Education of Singapore

Istituto Fondazione Italiana per la Ricerca sul Cancro di Oncologia Molecolare

Conselho Nacional de Desenvolvimento Científico

Fundação de Amparo à Pesquisa do Rio de Janeiro

Ministry of Economy and Competitiveness

European Commission

Publisher

Rockefeller University Press

Subject

Cell Biology

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