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

• Published in: PloS one 2015-03, Vol.10 (3), p.e0120339
• Main Authors: Wilkie, Iain C, Fassini, Dario, Cullorà, Emanuele, Barbaglio, Alice, Tricarico, Serena, Sugni, Michela, Del Giacco, Luca, Candia Carnevali, M Daniela
• Format: Article
• Language: English
• Subjects: Acetylcholine - pharmacology; Acetylcholine receptors (muscarinic); Acids; Animals; Arecoline - pharmacology; Biomechanical Phenomena; Cholinergic Agonists - pharmacology; Chondroitin ABC lyase; Chondroitin ABC Lyase - pharmacology; Collagen; Collagen - metabolism; Creep tests; Echinodermata; Echinoidea; Enzymes; Epinephrine; Fibrils; GABA; Glutamic acid; Glycosaminoglycans; Hyaluronic acid; Hyaluronoglucosaminidase - pharmacology; Ligaments; Ligaments - drug effects; Ligaments - physiology; Load transfer; Mechanical properties; Mechanotransduction, Cellular; Methacholine; Methacholine Chloride - pharmacology; Modulus of elasticity; Morphology; Movement - drug effects; Muscarinic Agonists - pharmacology; Muscle Cells - drug effects; Muscle Cells - physiology; Myocytes; Neurotransmitters; Nicotine; Nicotine - pharmacology; Nicotinic Agonists - pharmacology; Ontogeny; Paracentrotus - drug effects; Paracentrotus - physiology; Paracentrotus lividus; Phylogeny; Physiology; Piperazine; Piperazines - pharmacology; Proteins; Serotonin; Stiffening; Strain; Stress, Mechanical; Stress-strain curves; Stress-strain relationships; Tensile Strength; Tissues; Transfer functions; Viscosity; γ-Aminobutyric acid
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0120339

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.