The Mechanical Properties of Hydrated Intermediate Filaments: Insights from Hagfish Slime Threads

Abstract

Intermediate filaments (IFs) impart mechanical integrity to cells, yet IF mechanics are poorly understood. It is assumed that IFs in cells are as stiff as hard α-keratin, F-actin, and microtubules, but the high bending flexibility of IFs and the low stiffness of soft α-keratins suggest that hydrated IFs may be quite soft. To test this hypothesis, we measured the tensile mechanics of the keratin-like threads from hagfish slime, which are an ideal model for exploring the mechanics of IF bundles and IFs because they consist of tightly packed and aligned IFs. Tensile tests suggest that hydrated IF bundles possess low initial stiffness (Ei=6.4MPa) and remarkable elasticity (up to strains of 0.34), which we attribute to soft elastomeric IF protein terminal domains in series with stiffer coiled coils. The high tensile strength (180MPa) and toughness (130 MJ/m3) of IF bundles support the notion that IFs lend mechanical integrity to cells. Their long-range elasticity suggests that IFs may also allow cells to recover from large deformations. X-ray diffraction and congo-red staining indicate that post-yield deformation leads to an irreversible α→β conformational transition in IFs, which leads to plastic deformation, and may be used by cells as a mechanosensory cue.