Wilkie IC et al. (2015), Mechanical properties of the compass depressors...

ECB-ART-43884

PLoS One 2015 Jan 01;103:e0120339. doi: 10.1371/journal.pone.0120339.

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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.

Wilkie IC , Fassini D , Cullorà E , Barbaglio A , Tricarico S , Sugni M , Del Giacco L , Candia Carnevali MD .

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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.

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Species referenced: Echinodermata
Genes referenced: abcb6 LOC100887844 LOC100888622 LOC105443552 LOC115919910 LOC115924575 LOC576539 LOC577998 LOC579130 LOC583082 LOC591902

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	Fig 1. Photograph of the lantern of Paracentrotus lividus.The view is from the side and slightly above the lantern. Two of the five segments of the lantern (la) are visible. The compasses (co) are partly elevated due to contraction of the compass elevator muscles (ce). Asterisks, compass depressors; pg, perignathic girdle (edge of test); t, tooth.
	Fig 2. Compass depressors of P. lividus and experimental set-up; not to scale.(A,B) Diagrammatic lateral views of components associated with the lantern (la) of P. lividus that are relevant to this investigation. Two compasses (co) and their paired compass depressors (cd) are shown. In A the compasses are fully depressed. Contraction of the compass elevator muscles (ce) effects upwards rotation of the compasses, as shown in B (arrow). pm, peristomial membrane; te, circumoral region of the test. (C) Diagrammatic lateral view of experimental set-up used for creep tests on isolated CDs. ho, hook; le, isotonic lever; lo, load; ro, horizontal rod (shown as transverse section); rs, rubber stop; sc, silver chain. (D) Oblique view of the device designed to grip the test end of each CD. The test fragment to which the CD was attached was trapped in the loop of the wire hook (ho) by a rubber stop (rs) that fitted tightly round the vertical extremity of the hook, but could be slid up and down, as required. (E) Front view of the latter device with a CD in place. tf, test fragment.
	Fig 3. Creep behaviour of P. lividus CDs.(A) Recording of a representative creep curve, showing the primary (1), secondary (2) and tertiary (3) phases, the last leading to rupture (asterisk). The dashed line indicates the slope of the secondary phase, from which the viscosity was calculated. (B) Relationship between strain rate during the secondary phase and stress. The best-fit line generated by linear regression is included (y = 0.0015x + 0.0006; Spearman r = 0.3076; P = 0.0924).
	Fig 4. Force-extension and stress relaxation behaviour of P. lividus CDs.(A) Recording of a representative force-extension test in which the CD was extended by 0.5 mm every 20 s. At each extension the force reached a peak then decayed in two phases (rapid and slow). The asterisk indicates the point at which rupture occurred. (B) Complete set of stress-strain curves derived from force-extension tests on five CDs from one animal. This set of curves is representative in terms of the apparent non-strain rate dependence of the duration of the toe region, the tensile strength and the breaking strain. For the sake of clarity, most of the curves are curtailed before the rupture point. (C) Stress-strain curves of one CD derived from the recording shown in Fig. 4A and which is one of the batch featured in Fig. 4B (strain rate 0.0071 s-1). Comparison of the curves for peak stress, stress 4 s after the peak was reached and stress 8 s after the peak was reached. Considerably more stress relaxation occurred in the 4 s after peak stress than in the subsequent 4 s. The asterisk indicates the point at which rupture occurred. (D) Stress relaxation data from Fig. 4C expressed as mean stress relaxation rates (SRR) during the periods 0–4 s and 4–8 s after each peak stress was reached.
	Fig 5. Recordings showing representative effects of cholinergic agonists (all 1 mmol l-1).In all cases except C, after the agonist was added it was present to the end of the recording; in C, methacholine was present for only the time period indicated by the horizontal bar, after which it was washed out. Vertical and horizontal scalebars indicate respectively extension and time: (A) 0.2 mm, 60 s; (B) 0.1 mm, 30 s; (C) 0.5 mm, 30 s; (D) 0.2 mm, 30 s; (E) 0.2 mm, 30 s.
	Fig 6. Effect of tensilin-like protein (TLP) on the creep behaviour of P. lividus CDs.(A) Recording of a response to 3.0 μg ml-1 TLP; vertical scalebar, 0.2 mm; horizontal scalebar, 60 s. (B, C) Effect of TLP on relative viscosity. CDs were treated with TLP at concentrations of 1.5 μg ml-1 and 3.0 μg ml-1; separate DEB-PPASW and PPASW controls were used for each concentration. (B) Mean relative viscosities for the time period 15–75 s after the start of TLP treatment. (C) Mean relative viscosities for the time period 5–6 min after the start of TLP treatment. Error bars are standard deviations and numbers of CDs in each group are shown above error bars.
	Fig 7. Diagrammatic representation of the CD of P. lividus.This depicts part of a longitudinal section; not to scale. The CD consists of parallel discontinuous collagen fibrils (cf), which are connected by interfibrillar crossbridges containing chondroitin sulphate/dermatan sulphate proteoglycans (ic). Hyaluronic acid (hy) is present but of unknown function (its disposition on the surface of the collagen fibrils is conjectural). Bundles of beaded microfibrils (mf) occur between the collagen fibrils. The main cellular components are the somata and processes of electron-dense granule-containing juxtaligamental cells (jlc). Agranular cell processes, which may be cholinergic axons, are in close contact with the juxtaligamental cells and are shown as transverse sections (ax).
	Fig 8. Comparison of amino acid sequences.Alignment of the amino acid sequences of the immediate N-terminal domains of human and sea-urchin TIMPs, holothurian tensilins and Strongylocentrotus tensilin-like protein. Identical amino acids are highlighted. (Sources: [28–30], [95], [107]).

References [+] :

Ahmadzadeh, Determining the contribution of glycosaminoglycans to tendon mechanical properties with a modified shear-lag model. 2013, Pubmed