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Molecular mechanism for direct actin force-sensing by α-catenin.

Elife. 2020 Sep 24;9
Lin Mei 1 , Santiago Espinosa de Los Reyes 2 , Matthew J Reynolds 2 , Rachel Leicher 3 , Shixin Liu 3 , Gregory M Alushin 2
Lin Mei 1 , Santiago Espinosa de Los Reyes 2 , Matthew J Reynolds 2 , Rachel Leicher 3 , Shixin Liu 3 , Gregory M Alushin 2
+ et al

[No authors listed]

Author information
  • 1 Tri-Institutional PhD Program in Chemical Biology, The Rockefeller University, New York, United States.
  • 2 Laboratory of Structural Biophysics and Mechanobiology, The Rockefeller University, New York, United States.
  • 3 Laboratory of Nanoscale Biophysics and Biochemistry, The Rockefeller University, New York, United States.

摘要


The actin cytoskeleton mediates mechanical coupling between cells and their tissue microenvironments. The architecture and composition of actin networks are modulated by force; however, it is unclear how interactions between actin filaments (F-actin) and associated proteins are mechanically regulated. Here we employ both optical trapping and biochemical reconstitution with myosin motor proteins to show single piconewton forces applied solely to F-actin enhance binding by the human version of the essential cell-cell adhesion protein αE-catenin but not its homolog vinculin. Cryo-electron microscopy structures of both proteins bound to F-actin reveal unique rearrangements that facilitate their flexible C-termini refolding to engage distinct interfaces. Truncating α-catenin's C-terminus eliminates force-activated F-actin binding, and addition of this motif to vinculin confers force-activated binding, demonstrating that α-catenin's C-terminus is a modular detector of F-actin tension. Our studies establish that piconewton force on F-actin can enhance partner binding, which we propose mechanically regulates cellular adhesion through α-catenin.

KEYWORDS: actin cytoskeleton, cell adhesion, cell biology, chicken, cryo-electron microscopy, human, mechanobiology, mechanosensation, molecular biophysics, single molecule biophysics, structural biology