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α-catenin switches between a slip and an asymmetric catch bond with F-actin to cooperatively regulate cell junction fluidity

C. Arbore, M. Sergides, L. Gardini, G. Bianchi, A. V. Kashchuk, I. Pertici, P. Bianco, F. S. Pavone and M. Capitanio ()
Additional contact information
C. Arbore: LENS - European Laboratory for Non-linear Spectroscopy, University of Florence
M. Sergides: LENS - European Laboratory for Non-linear Spectroscopy, University of Florence
L. Gardini: LENS - European Laboratory for Non-linear Spectroscopy, University of Florence
G. Bianchi: LENS - European Laboratory for Non-linear Spectroscopy, University of Florence
A. V. Kashchuk: LENS - European Laboratory for Non-linear Spectroscopy, University of Florence
I. Pertici: University of Florence
P. Bianco: University of Florence
F. S. Pavone: LENS - European Laboratory for Non-linear Spectroscopy, University of Florence
M. Capitanio: LENS - European Laboratory for Non-linear Spectroscopy, University of Florence

Nature Communications, 2022, vol. 13, issue 1, 1-11

Abstract: Abstract α-catenin is a crucial protein at cell junctions that provides connection between the actin cytoskeleton and the cell membrane. At adherens junctions (AJs), α-catenin forms heterodimers with β-catenin that are believed to resist force on F-actin. Outside AJs, α-catenin forms homodimers that regulates F-actin organization and directly connect the cell membrane to the actin cytoskeleton, but their mechanosensitive properties are inherently unknown. By using ultra-fast laser tweezers we found that a single α-β-catenin heterodimer does not resist force but instead slips along F-actin in the direction of force. Conversely, the action of 5 to 10 α-β-catenin heterodimers together with force applied toward F-actin pointed end engaged a molecular switch in α-catenin, which unfolded and strongly bound F-actin as a cooperative catch bond. Similarly, an α-catenin homodimer formed an asymmetric catch bond with F-actin triggered by protein unfolding under force. Our data suggest that α-catenin clustering together with intracellular tension engage a fluid-to-solid phase transition at the membrane-cytoskeleton interface.

Date: 2022
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DOI: 10.1038/s41467-022-28779-7

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