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The biomechanics of intermediate filament-based materials : insights from hagfish slime threads Fudge, Douglas Steven

Abstract

Intermediate filaments (IFs) provide mechanical integrity to a wide range of biomaterials, from soft epithelia to hard keratins such as nail and horn. Although much is known about the mechanical properties of IF-rich materials such as hair, the mechanical properties of individual IFs are unknown. In this thesis, I employed hagfish slime threads, which are composed almost exclusively of highly aligned IFs, as a model for exploring the mechanics of IFs both in living cells and keratinized tissues. Experiments with hydrated slime threads suggest that IFs in cells are extremely soft, extensible, strong, and tough when compared to actin filaments and microtubules. These data support the view that the main role of IFs in cells is to provide mechanical integrity and strength. The data also suggest that IFs are likely to provide the primary passive mechanism by which cells recover from large deformations. Structural data suggest that post-yield deformation of IFs leads to an irreversible α→β transition, which may be used by cells as a mechanosensory cue. Tensile tests in air revealed that dehydrated IFs behave similarly to hard akeratins in water, suggesting that one role of the hard α -keratin matrix is to maintain IFs in a dehydrated state, even when immersed in water. Recovery tests suggest that an additional role of the matrix is to permit full recovery from postyield deformations by both inhibiting β-sheet formation and providing a restoring force in parallel to the IFs. The dramatic difference in properties between wet and dry slime threads suggests that hydrated IFs consist of soft and rigid components arranged in series. These components correspond to the terminal and coiled coil domains of the IF protein dimers, respectively. This arrangement of components is the key to understanding the remarkable mechanical versatility of IFs. Experiments on hagfish slime revealed aspects of the slime's mechanical properties, its mechanism of formation, and some behavioral aspects of its release. Results from these experiments suggest that hagfish slime does not behave as a fibre-reinforced composite, but as an extremely dilute assemblage of protein threads and mucins that functions to protect hagfishes from gill-breathing predators.

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