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

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....

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Veröffentlicht in:PloS one 2015-03, Vol.10 (3), p.e0120339
Hauptverfasser: Wilkie, Iain C, Fassini, Dario, Cullorà, Emanuele, Barbaglio, Alice, Tricarico, Serena, Sugni, Michela, Del Giacco, Luca, Candia Carnevali, M Daniela
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creator Wilkie, Iain C
Fassini, Dario
Cullorà, Emanuele
Barbaglio, Alice
Tricarico, Serena
Sugni, Michela
Del Giacco, Luca
Candia Carnevali, M Daniela
description 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.
doi_str_mv 10.1371/journal.pone.0120339
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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. 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This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2015 Wilkie et al 2015 Wilkie et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c684t-b953cda2fe08cae2492223519b9bb48d0ed552551f0b4e3ec79488556cafee223</citedby><cites>FETCH-LOGICAL-c684t-b953cda2fe08cae2492223519b9bb48d0ed552551f0b4e3ec79488556cafee223</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4365025/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4365025/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,865,886,2103,2929,23871,27929,27930,53796,53798</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25786033$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Ianora, Adrianna</contributor><creatorcontrib>Wilkie, Iain C</creatorcontrib><creatorcontrib>Fassini, Dario</creatorcontrib><creatorcontrib>Cullorà, Emanuele</creatorcontrib><creatorcontrib>Barbaglio, Alice</creatorcontrib><creatorcontrib>Tricarico, Serena</creatorcontrib><creatorcontrib>Sugni, Michela</creatorcontrib><creatorcontrib>Del Giacco, Luca</creatorcontrib><creatorcontrib>Candia Carnevali, M Daniela</creatorcontrib><title>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</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The compass depressors (CDs) of the sea-urchin lantern are ligaments consisting mainly of discontinuous collagen fibrils associated with a small population of myocytes. 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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. 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pharmacology</topic><topic>Acetylcholine receptors (muscarinic)</topic><topic>Acids</topic><topic>Animals</topic><topic>Arecoline - pharmacology</topic><topic>Biomechanical Phenomena</topic><topic>Cholinergic Agonists - pharmacology</topic><topic>Chondroitin ABC lyase</topic><topic>Chondroitin ABC Lyase - pharmacology</topic><topic>Collagen</topic><topic>Collagen - metabolism</topic><topic>Creep tests</topic><topic>Echinodermata</topic><topic>Echinoidea</topic><topic>Enzymes</topic><topic>Epinephrine</topic><topic>Fibrils</topic><topic>GABA</topic><topic>Glutamic acid</topic><topic>Glycosaminoglycans</topic><topic>Hyaluronic acid</topic><topic>Hyaluronoglucosaminidase - pharmacology</topic><topic>Ligaments</topic><topic>Ligaments - drug effects</topic><topic>Ligaments - physiology</topic><topic>Load transfer</topic><topic>Mechanical properties</topic><topic>Mechanotransduction, Cellular</topic><topic>Methacholine</topic><topic>Methacholine Chloride - pharmacology</topic><topic>Modulus of elasticity</topic><topic>Morphology</topic><topic>Movement - drug effects</topic><topic>Muscarinic Agonists - pharmacology</topic><topic>Muscle Cells - drug effects</topic><topic>Muscle Cells - physiology</topic><topic>Myocytes</topic><topic>Neurotransmitters</topic><topic>Nicotine</topic><topic>Nicotine - pharmacology</topic><topic>Nicotinic Agonists - pharmacology</topic><topic>Ontogeny</topic><topic>Paracentrotus - drug effects</topic><topic>Paracentrotus - physiology</topic><topic>Paracentrotus lividus</topic><topic>Phylogeny</topic><topic>Physiology</topic><topic>Piperazine</topic><topic>Piperazines - pharmacology</topic><topic>Proteins</topic><topic>Serotonin</topic><topic>Stiffening</topic><topic>Strain</topic><topic>Stress, Mechanical</topic><topic>Stress-strain curves</topic><topic>Stress-strain relationships</topic><topic>Tensile Strength</topic><topic>Tissues</topic><topic>Transfer functions</topic><topic>Viscosity</topic><topic>γ-Aminobutyric acid</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wilkie, Iain C</creatorcontrib><creatorcontrib>Fassini, Dario</creatorcontrib><creatorcontrib>Cullorà, Emanuele</creatorcontrib><creatorcontrib>Barbaglio, Alice</creatorcontrib><creatorcontrib>Tricarico, Serena</creatorcontrib><creatorcontrib>Sugni, Michela</creatorcontrib><creatorcontrib>Del Giacco, Luca</creatorcontrib><creatorcontrib>Candia Carnevali, M Daniela</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing &amp; Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological &amp; Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science &amp; Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies &amp; Aerospace Collection</collection><collection>Agricultural &amp; Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing &amp; Allied Health Database (Alumni Edition)</collection><collection>Meteorological &amp; Geoastrophysical Abstracts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wilkie, Iain C</au><au>Fassini, Dario</au><au>Cullorà, Emanuele</au><au>Barbaglio, Alice</au><au>Tricarico, Serena</au><au>Sugni, Michela</au><au>Del Giacco, Luca</au><au>Candia Carnevali, M Daniela</au><au>Ianora, Adrianna</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>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</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-03-18</date><risdate>2015</risdate><volume>10</volume><issue>3</issue><spage>e0120339</spage><pages>e0120339-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25786033</pmid><doi>10.1371/journal.pone.0120339</doi><oa>free_for_read</oa></addata></record>
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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
title 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
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