Filopodia rotate and coil by actively generating twist in their actin shaft

TL;DR

This study reveals that filopodia actively generate twist and rotation in their actin core, which influences their dynamics and functions across various cell types, supported by physical modeling and experimental evidence.

Contribution

It demonstrates that twist and rotation are emergent, active behaviors of filopodia's actin core, a novel insight into their mechanical and functional properties.

Findings

Filopodia exhibit axial twisting and spinning motions.

Filopodia form helical buckles related to accumulated twist.

Twist generation is a universal mechanism across cell types.

Abstract

Filopodia are actin-rich structures, present on the surface of practically every known eukaryotic cell. These structures play a pivotal role in specific cell-cell and cell-matrix interactions by allowing cells to explore their environment, generate mechanical forces, perform chemical signaling, or convey signals via intercellular tunneling nano-bridges. The dynamics of filopodia appear quite complex as they exhibit a rich behavior of buckling, pulling, length and shape changes. Here, we show that filopodia additionally explore their 3D extracellular space by combining growth and shrinking with axial twisting and buckling of their actin rich core. Importantly, the actin core inside filopodia performs a twisting or spinning motion which is observed for a range of highly distinct and cognate cell types spanning from earliest development to highly differentiated tissue cells. Non-equilibrium physical modeling of actin and myosin confirm that twist, and hence rotation, is an emergent phenomenon of active filaments confined in a narrow channel which points to a generic mechanism present in all cells. Our measurements confirm that filopodia exert traction forces and form helical buckles in a range of different cell types that can be ascribed to accumulation of sufficient twist. These results lead us to conclude that activity induced twisting of the actin shaft is a general mechanism underlying fundamental functions of filopodia.