Disordered Topography Mediates Filopodial Extension and Morphology of Cells on Stiff Materials

Abstract

In cell–material interactions, cells use filopodia to sense external biochemical and mechanical cues, and subsequently dictate their survival. In an effort toward understanding how disordered topography of stiff materials influences filopodial recognition, diamond films with grain sizes varying from nano‐ to micrometers are fabricated for the investigation of osteoblast filopodial extension. Interestingly, straight filopodia with pronounced cell–substrate adhesion are observed on a nanocrystalline diamond (NCD) region, whereas filopodia on a microcrystalline diamond (MCD) surface only adhere to, and get deflected by, large diamond grains. More importantly, filopodia on NCD keep propagating with a constant velocity, whereas the same process takes place in a slow and intermittent manner on MCD. A theoretical model is also developed and it suggests that the contact between the disordered topography and the filopodial tip plays a key role in altering filopodial growth dynamics. In particular, it is predicted that large surface asperities can block the movement of the filopodial tip, delay its extension, and cause bending of the structure, in quantitative agreement with experimental observations. These findings reveal previously underappreciated effects of random, stiff topographies on the response of cells, and hence can provide new insights for the design of future implant biomaterials.