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.