Traction Dynamics of Filopodia on Compliant Substrates

Cells sense the environment's mechanical stiffness to control their own shape, migration, and fate. To better understand stiffness sensing, we constructed a stochastic model of the "motor-clutch" force transmission system, where molecular clutches link F-actin to the substrate and mechanically resist myosin- driven F- actin retrograde flow. The model predicts two distinct regimes: ( i) "frictional slippage," with fast retrograde flow and low traction forces on stiff substrates and ( ii) oscillatory "load-and-fail" dynamics, with slower retrograde flow and higher traction forces on soft substrates. We experimentally confirmed these model predictions in embryonic chick forebrain neurons by measuring the nanoscale dynamics of single- growth- cone filopodia. Furthermore, we experimentally observed a model- predicted switch in F- actin dynamics around an elastic modulus of 1 kilopascal. Thus, a motor- clutch system inherently senses and responds to the mechanical stiffness of the local environment.