New Insights into Mutable Collagenous Tissue: Correlations between the Microstructure and Mechanical State of a Sea-Urchin Ligament

Ana R Ribeiro,Alice Barbaglio,Maria D C Carnevali,Cristiano D Benedetto,Mário A Barbosa,Cristina C Ribeiro,Iain C Wilkie,Anna Mitraki

doi:10.1371/journal.pone.0024822

Abstract

The mutable collagenous tissue (MCT) of echinoderms has the ability to undergo rapid and reversible changes in passive mechanical properties that are initiated and modulated by the nervous system. Since the mechanism of MCT mutability is poorly understood, the aim of this work was to provide a detailed morphological analysis of a typical mutable collagenous structure in its different mechanical states. The model studied was the compass depressor ligament (CDL) of a sea urchin (Paracentrotus lividus), which was characterized in different functional states mimicking MCT mutability. Transmission electron microscopy, histochemistry, cryo-scanning electron microscopy, focused ion beam/scanning electron microscopy, and field emission gun-environmental scanning electron microscopy were used to visualize CDLs at the micro- and nano-scales. This investigation has revealed previously unreported differences in both extracellular and cellular constituents, expanding the current knowledge of the relationship between the organization of the CDL and its mechanical state. Scanning electron microscopies in particular provided a three-dimensional overview of CDL architecture at the micro- and nano-scales, and clarified the micro-organization of the ECM components that are involved in mutability. Further evidence that the juxtaligamental cells are the effectors of these changes in mechanical properties was provided by a correlation between their cytology and the tensile state of the CDLs.

Highlights

IntroductionThe ‘mutable’ collagenous tissue (MCT) of echinoderms (starfish, sea-urchins and their relations) has the capacity to undergo reversible changes in mechanical properties (viscosity, tensile strength, and stiffness) within timescales of around 1 s that are under the control of the nervous system [1,2]
The ‘mutable’ collagenous tissue (MCT) of echinoderms has the capacity to undergo reversible changes in mechanical properties within timescales of around 1 s that are under the control of the nervous system [1,2]
The fibrils were enclosed within a coelomic epithelium, which became a myoepithelium on one side of the compass depressor ligament (CDL) (Fig. 2A)

Summary

Introduction

The ‘mutable’ collagenous tissue (MCT) of echinoderms (starfish, sea-urchins and their relations) has the capacity to undergo reversible changes in mechanical properties (viscosity, tensile strength, and stiffness) within timescales of around 1 s that are under the control of the nervous system [1,2]. MCT is present in all living echinoderm classes, in the form of dermal connective tissue, interossicular ligaments and tendons [2]. In addition to fulfilling the mechanical functions associated with ‘conventional’ collagenous structures (i.e. energy storage, transmission and dissipation), MCT provides mechanisms for the detachment of appendages or body parts in response to disease, trauma or predator attack [2] and for the energy-sparing maintenance of posture [3]. Most mutable collagenous structures consist largely of parallel aggregations of collagen fibrils to which proteoglycans are covalently and non-covalently attached, as in mammalian connective tissue [2,3,4,5,6,7,8,9,10,11]. One constant morphological feature appearing in all MCTs is the presence of juxtaligamental cells (JLCs), which contain large electron-dense granules and come into close contact with motor axons [2,14,15]

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