Mechanical Properties of the Compass Depressors of the Sea-Urchin Paracentrotus lividus (Echinodermata, Echinoidea) and the Effects of Enzymes, Neurotransmitters and Synthetic Tensilin-Like Protein

Abstract

The compass depressors (CDs) of the sea-urchin lantern are ligaments consisting mainly of discontinuous collagen fibrils associated with a small population of myocytes. They are mutable collagenous structures, which can change their mechanical properties rapidly and reversibly under nervous control. The aims of this investigation were to characterise the baseline (i.e. unmanipulated) static mechanical properties of the CDs of Paracentrotus lividus by means of creep tests and incremental force-extension tests, and to determine the effects on their mechanical behaviour of a range of agents. Under constant load the CDs exhibited a three-phase creep curve, the mean coefficient of viscosity being 561±365 MPa.s. The stress-strain curve showed toe, linear and yield regions; the mean strain at the toe-linear inflection was 0.86±0.61; the mean Young’s modulus was 18.62±10.30 MPa; and the mean tensile strength was 8.14±5.73 MPa. Hyaluronidase from Streptomyces hyalurolyticus had no effect on creep behaviour, whilst chondroitinase ABC prolonged primary creep but had no effect on secondary creep or on any force-extension parameters; it thus appears that neither hyaluronic acid nor sulphated glycosaminoglycans have an interfibrillar load transfer function in the CD. Acetylcholine, the muscarinic agonists arecoline and methacholine, and the nicotinic agonists nicotine and 1-[1-(3,4-dimethyl-phenyl)-ethyl]-piperazine produced an abrupt increase in CD viscosity; the CDs were not differentially sensitive to muscarinic or nicotinic agonists. CDs showed either no, or no consistent, response to adrenaline, L-glutamic acid, 5-hydroxytryptamine and γ-aminobutyric acid. Synthetic echinoid tensilin-like protein had a weak and inconsistent stiffening effect, indicating that, in contrast to holothurian tensilins, the echinoid molecule may not be involved in the regulation of collagenous tissue tensility. We compare in detail the mechanical behaviour of the CD with that of mammalian tendon and highlight its potential as a model system for investigating poorly understood aspects of the ontogeny and phylogeny of vertebrate collagenous tissues.

Phylotranscriptomic analysis uncovers a wealth of tissue inhibitor of metalloproteinases variants in echinoderms

“…This suggests that apodans rely on an older suite of TIMPs that resemble and may perform many of the same functions as vertebrate TIMPs. It may be that apodans, all echinoderms and even chordates use some TIMPs to control the mechanical properties of specific ligaments and membranes within their bodies, as has been documented in echinoids [ 14 , 15 ].

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“…The large number of echinoderm TIMPs we uncovered here may explain why a tensilin-like gene identified from S. pupuratus [ 15 ] and galardin (a synthetic TIMP) [ 14 ] had only a weak effect on echinoid MCT. We found 20 echinoid TIMPs, including seven different sequences in S. purpuratus .…”

“…Different factors stiffen the tissue even further and reverse the effects. Less visible than holothuroid body-wall liquefaction, but critically important, is the role of MCT in the functioning of the echinoid (sea urchin) feeding apparatus [ 14 , 15 ]. These MCT ligaments demonstrate three levels of stiffness (reminiscent of holothuroid MCT) [ 15 ] and respond to changes in concentrations of MMPs, an echinoid tensilin-like protein and a synthetic MMP inhibitor (although only weakly in the latter two cases) [ 14 , 15 ].…”

Do genes lie? Mitochondrial capture masks the Red Sea collector urchin’s true identity (Echinodermata: Echinoidea: Tripneustes)

“…Our findings ratify Dafni's observations and demonstrate additional morphological differences in the distal part of the lantern's compass ossicles and periproct size. These five rodlike ossicles are believed to be involved in a rhythmic upwards and downwards motion that primarily serves as a respiratory pump whose role is to oxygenate the lantern muscles (Wilkie et al, 2015). While in T. gratilla these skeletal elements have a slender, deeply bifurcated structure, in RS Tripneustes they take a flattened robust appearance (Fig.…”

Interfibrillar stiffening of echinoderm mutable collagenous tissue demonstrated at the nanoscale

“…A notable exception is the mutable collagenous tissue (MCT) of echinoderms (e.g., starfish, sea urchins, sea cucumbers), which undergoes rapid changes in stiffness under the control of the nervous system via ATP-independent mechanisms (10)(11)(12). MCT is ubiquitous in echinoderms (12), for example, in the dermis (skin) of sea cucumbers (13,14), in the compass depressor ligament (CDL) of sea urchins (15)(16)(17), and in the arms of feather stars (18). The presence of MCT enables functionally diverse behaviors; for example in starfish, MCT enables body wall stiffening during feeding on prey and it also enables irreversible body wall softening before arm autotomy as a defense against predation (12).…”