Abstract
Scaffolds for tissue engineering application may be made from a collagenous extracellular matrix (ECM) of connective tissues because the ECM can mimic the functions of the target tissue. The primary sources of collagenous ECM material are calf skin and bone. However, these sources are associated with the risk of having bovine spongiform encephalopathy or transmissible spongiform encephalopathy. Alternative sources for collagenous ECM materials may be derived from livestock, e.g., pigs, and from marine animals, e.g., sea urchins. Collagenous ECM of the sea urchin possesses structural features and mechanical properties that are similar to those of mammalian ones. However, even more intriguing is that some tissues such as the ligamentous catch apparatus can exhibit mutability, namely rapid reversible changes in the tissue mechanical properties. These tissues are known as mutable collagenous tissues (MCTs). The mutability of these tissues has been the subject of on-going investigations, covering the biochemistry, structural biology and mechanical properties of the collagenous components. Recent studies point to a nerve-control system for regulating the ECM macromolecules that are involved in the sliding action of collagen fibrils in the MCT. This review discusses the key attributes of the structure and function of the ECM of the sea urchin ligaments that are related to the fibril-fibril sliding action—the focus is on the respective components within the hierarchical architecture of the tissue. In this context, structure refers to size, shape and separation distance of the ECM components while function is associated with mechanical properties e.g., strength and stiffness. For simplicity, the components that address the different length scale from the largest to the smallest are as follows: collagen fibres, collagen fibrils, interfibrillar matrix and collagen molecules. Application of recent theories of stress transfer and fracture mechanisms in fibre reinforced composites to a wide variety of collagen reinforcing (non-mutable) connective tissue, has allowed us to draw general conclusions concerning the mechanical response of the MCT at specific mechanical states, namely the stiff and complaint states. The intent of this review is to provide the latest insights, as well as identify technical challenges and opportunities, that may be useful for developing methods for effective mechanical support when adapting decellularised connective tissues from the sea urchin for tissue engineering or for the design of a synthetic analogue.
Highlights
W1. iItnhtrroedguacrtdiosnto biomaterials for tissue engineering, the key areas that must be addressed are the cells, scaffolds and growth-stimulating signals [1,2,3]
At the microscopic length scale corresponding to cells, the structural environment is well-preserved in the extracellular matrix (ECM)-DT; this means that the matrix microenvironment may be effective in directing cellular phenotype via geometric cues [4,36] as well as growth factors for cell attachment, proliferation, migration, and differentiation [3]
Two interesting findings arise from this study: (1) the surface nucleation and accretion process can result in a fibril with smoothly tapered end and (2) there is a limit to the increase in diameter as the fibril grow axially—it appears that beyond a length of 13 μm (200 D periods) a maximum diameter of about 600 kDa/nm is reached [127]
Summary
One of the most intriguing properties of the sea urchin connective tissues, such as the ligamentous CA (Figure 1) [66], is that they can switch from the viscoelastic fluid state to the solid state, reversibly, on a timescale of the order of 1 s [14,15,16,67,68]. We present fresh arguments to explain how the stiff state is associated with the elastic stress transfer mechanism (Section 3.3) while the compliant state is associated with the plastic stress transfer mechanism (Section 3.4) As they can change from one state to another in a short span of time, these tissues are regarded as “smart” or “intelligent” tissues [66]. It follows that the mechanical states of the tissue are mediated by the interactions of collagen fibrils with the surrounding matrix [69] governed by elastic stress transfer at low loads [80,81] and plastic stress transfer at higher loads [80,81]. While a detailed molecular mechanism for the regulation of collagen-fibril associations in the sea cucumber dermis has yet to be developed, it raises the question of whether any related phenomena occur in vertebrate tissues. A new biomimetic research strategy has been proposed to further characterize the properties of MCTs so as to gain deeper insights—the aim is to develop innovative ECM biomaterials with dynamic mechanical properties that finds applications in vitro as well as in vivo [57,85]
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