Morphology and biomechanics of the microfibrillar network of sea cucumber dermis

Abstract

The principal component of the body wall of the sea cucumber Cucumaria frondosa is a dermis consisting of collagen fibrils, microfibrils, proteoglycans and other soluble and insoluble components. A major structural constituent of the dermis is a network of 10­14 nm diameter microfibrils, which surrounds and penetrates bundles of collagen fibrils. This network has been extracted and purified using guanidine and bacterial collagenase. Tensile testing of the microfibrillar network in artificial sea water demonstrates that it is reversibly extensible up to approximately 300 % of its initial length. It behaves like a viscoelastic solid, having a long-range elastic component as well as a time-dependent viscous component. Reduction and alkylation of the cysteine residues in the network do not change its breaking strain or strength, but greatly increase the compliance of the network until, near the breaking strain, the tensile resistance rapidly increases. These data suggest that the strength of the network is due to non-reducible crosslinks, while its elasticity is dependent upon disulfide bonds. In deionized water, the network becomes swollen and, although it remains elastic, is much more compliant than when tested in artificial sea water. Examination of whole tissues and purified networks with the electron microscope reveals structures similar to vertebrate fibrillin-containing microfibrils. Considering that the dermis of C. frondosa is a mechanically mutable tissue in which elongation is accompanied by the sliding of collagen fibrils past one another, the microfibrillar network may act to maintain the orientation of fibrillar components during movement and may also provide a long-range restoring force.