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The Mutable Collagenous Tissue of Echinoderms: Biological, Biomedical, and Biomimetic...
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The Mutable Collagenous Tissue of Echinoderms: Biological, Biomedical, and Biomimetic Aspects

A special issue of Marine Drugs (ISSN 1660-3397). This special issue belongs to the section "Biomaterials of Marine Origin".

Deadline for manuscript submissions: closed (31 August 2023) | Viewed by 10484

Special Issue Editors

Dr. Iain C. Wilkie

E-Mail Website
Guest Editor
School of Biodiversity, One Health and Veterinary Medicine, University of Glasgow, Glasgow G12 8QQ, UK
Interests: functional morphology; biomechanics and physiology of Echinodermata; mechanically adaptable collagenous tissue; autotomy and other animal detachment mechanisms
Prof. Dr. M. Daniela Candia Carnevali

E-Mail Website
Guest Editor
Department of Environmental Science and Policy, University of Milan, Via Celoria, 2, 20133 Milan, Italy
Interests: functional biology of marine invertebrates (echinoderms; sponges); regenerative and reproductive biology of echinoderms; effects of exposure to environmental contaminants on reproductive and developmental processes

Special Issue Information

Dear Colleagues,

Mutable collagenous tissue (MCT, also known as catch connective tissue), which has the capacity to drastically alter its mechanical properties within a timescale of seconds under nervous control, is unique to echinoderms (starfish, sea-urchins, and their close relations) and is of central importance to their biology.

Although MCT has been the subject of intense research activity for over 50 years, serious gaps in knowledge remain: for example, the molecular mechanism(s) modulating MCT tensility and the precise role of juxtaligamental cells as effectors of tensile change remain to be fully elucidated. Recent investigations offer hope that the application of transcriptomic, metabolomic, and other “-omics” methodologies will help to rectify these deficiencies.

MCT is also attracting increasing interest as a source of constituents for the assembly of novel materials with potential biomedical applications and as a source of inspiration for the design of entirely artificial materials and devices with adaptable and controllable mechanical properties.

We therefore believe that the time is right for a Special Issue that demonstrates the full range of current MCT-related studies. We invite articles that provide insights into aspects of basic MCT biology (e.g., cellular and molecular processes modulating mechanical adaptability, neural control pathways, functional biology) and applied aspects—both biomedical applications of MCT-derived components and MCT-inspired biomimetic solutions to biomedical or engineering challenges.

Dr. Iain C. Wilkie
Prof. Dr. M. Daniela Candia Carnevali
Guest Editors

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Marine Drugs is an international peer-reviewed open access monthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2900 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

  • mutable collagenous tissue
  • collagen
  • Echinodermata
  • biomechanics
  • biomimetics
  • biomedical applications
  • biomaterials
  • detachment mechanisms
  • autotomy

Published Papers (6 papers)

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Research

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20 pages, 1697 KiB  
Article
Is Stress Relaxation in Sea Cucumber Dermis Chemoelastic?
by Ettore Barbieri and Himadri Shikhar Gupta
Mar. Drugs 2023, 21(12), 610; https://doi.org/10.3390/md21120610 - 25 Nov 2023
Viewed by 1064
Abstract
Echinoderms, such as sea cucumbers, have the remarkable property of changing the stiffness of their dermis according to the surrounding chemical environments. When sea cucumber dermal specimens are constantly strained, stress decays exponentially with time. Such stress relaxation is a hallmark of visco-elastic [...] Read more.
Echinoderms, such as sea cucumbers, have the remarkable property of changing the stiffness of their dermis according to the surrounding chemical environments. When sea cucumber dermal specimens are constantly strained, stress decays exponentially with time. Such stress relaxation is a hallmark of visco-elastic mechanical behavior. In this paper, in contrast, we attempted to interpret stress relaxation from the chemoelasticity viewpoint. We used a finite element model for the microstructure of the sea cucumber dermis. We varied stiffness over time and framed such changes against the first-order reactions of the interfibrillar matrix. Within this hypothetical scenario, we found that stress relaxation would then occur primarily due to fast crosslink splitting between the chains and a much slower macro-chain scission, with characteristic reaction times compatible with relaxation times measured experimentally. A byproduct of the model is that the concentration of undamaged macro-chains in the softened state is low, less than 10%, which tallies with physical intuition. Although this study is far from being conclusive, we believe it opens an alternative route worthy of further investigation. Full article
(This article belongs to the Special Issue The Mutable Collagenous Tissue of Echinoderms: Biological, Biomedical, and Biomimetic Aspects)
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14 pages, 14602 KiB  
Article
Mutable Collagenous Tissue Isolated from Echinoderms Leads to the Production of a Dermal Template That Is Biocompatible and Effective for Wound Healing in Rats
by Anna Carolo, Luca Melotti, Giulia Zivelonghi, Roberta Sacchetto, Eylem Emek Akyürek, Tiziana Martinello, Andrea Venerando, Ilaria Iacopetti, Michela Sugni, Giordana Martinelli, Margherita Roncoroni, Stefania Marzorati, Silvia Barbon, Martina Contran, Damiana Incendi, Filippo Perozzo, Andrea Porzionato, Vincenzo Vindigni and Marco Patruno
Mar. Drugs 2023, 21(10), 506; https://doi.org/10.3390/md21100506 - 26 Sep 2023
Cited by 3 | Viewed by 1126
Abstract
The mutable collagenous tissue (MCT) of echinoderms possesses biological peculiarities that facilitate native collagen extraction and employment for biomedical applications such as regenerative purposes for the treatment of skin wounds. Strategies for skin regeneration have been developed and dermal substitutes have been used [...] Read more.
The mutable collagenous tissue (MCT) of echinoderms possesses biological peculiarities that facilitate native collagen extraction and employment for biomedical applications such as regenerative purposes for the treatment of skin wounds. Strategies for skin regeneration have been developed and dermal substitutes have been used to cover the lesion to facilitate cell proliferation, although very little is known about the application of novel matrix obtained from marine collagen. From food waste we isolated eco-friendly collagen, naturally enriched with glycosaminoglycans, to produce an innovative marine-derived biomaterial assembled as a novel bi-layered skin substitute (Marine Collagen Dermal Template or MCDT). The present work carried out a preliminary experimental in vivo comparative analysis between the MCDT and Integra, one of the most widely used dermal templates for wound management, in a rat model of full-thickness skin wounds. Clinical, histological, and molecular evaluations showed that the MCDT might be a valuable tool in promoting and supporting skin wound healing: it is biocompatible, as no adverse reactions were observed, along with stimulating angiogenesis and the deposition of mature collagen. Therefore, the two dermal templates used in this study displayed similar biocompatibility and outcome with focus on full-thickness skin wounds, although a peculiar cellular behavior involving the angiogenesis process was observed for the MCDT. Full article
(This article belongs to the Special Issue The Mutable Collagenous Tissue of Echinoderms: Biological, Biomedical, and Biomimetic Aspects)
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11 pages, 1282 KiB  
Communication
Possible Mechanisms of Stiffness Changes Induced by Stiffeners and Softeners in Catch Connective Tissue of Echinoderms
by Masaki Tamori and Akira Yamada
Mar. Drugs 2023, 21(3), 140; https://doi.org/10.3390/md21030140 - 23 Feb 2023
Cited by 2 | Viewed by 1429
Abstract
The catch connective, or mutable collagenous, tissue of echinoderms changes its mechanical properties in response to stimulation. The body wall dermis of sea cucumbers is a typical catch connective tissue. The dermis assumes three mechanical states: soft, standard, and stiff. Proteins that change [...] Read more.
The catch connective, or mutable collagenous, tissue of echinoderms changes its mechanical properties in response to stimulation. The body wall dermis of sea cucumbers is a typical catch connective tissue. The dermis assumes three mechanical states: soft, standard, and stiff. Proteins that change the mechanical properties have been purified from the dermis. Tensilin and the novel stiffening factor are involved in the soft to standard and standard to stiff transitions, respectively. Softenin softens the dermis in the standard state. Tensilin and softenin work directly on the extracellular matrix (ECM). This review summarizes the current knowledge regarding such stiffeners and softeners. Attention is also given to the genes of tensilin and its related proteins in echinoderms. In addition, we provide information on the morphological changes of the ECM associated with the stiffness change of the dermis. Ultrastructural study suggests that tensilin induces an increase in the cohesive forces with the lateral fusion of collagen subfibrils in the soft to standard transition, that crossbridge formation between fibrils occurs in both the soft to standard and standard to stiff transitions, and that the bond which accompanies water exudation produces the stiff dermis from the standard state. Full article
(This article belongs to the Special Issue The Mutable Collagenous Tissue of Echinoderms: Biological, Biomedical, and Biomimetic Aspects)
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Review

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37 pages, 8767 KiB  
Review
Extracellular Matrix of Echinoderms
by Igor Yu. Dolmatov and Vladimir A. Nizhnichenko
Mar. Drugs 2023, 21(7), 417; https://doi.org/10.3390/md21070417 - 22 Jul 2023
Viewed by 1558
Abstract
This review considers available data on the composition of the extracellular matrix (ECM) in echinoderms. The connective tissue in these animals has a rather complex organization. It includes a wide range of structural ECM proteins, as well as various proteases and their inhibitors. [...] Read more.
This review considers available data on the composition of the extracellular matrix (ECM) in echinoderms. The connective tissue in these animals has a rather complex organization. It includes a wide range of structural ECM proteins, as well as various proteases and their inhibitors. Members of almost all major groups of collagens, various glycoproteins, and proteoglycans have been found in echinoderms. There are enzymes for the synthesis of structural proteins and their modification by polysaccharides. However, the ECM of echinoderms substantially differs from that of vertebrates by the lack of elastin, fibronectins, tenascins, and some other glycoproteins and proteoglycans. Echinoderms have a wide variety of proteinases, with serine, cysteine, aspartic, and metal peptidases identified among them. Their active centers have a typical structure and can break down various ECM molecules. Echinoderms are also distinguished by a wide range of proteinase inhibitors. The complex ECM structure and the variety of intermolecular interactions evidently explain the complexity of the mechanisms responsible for variations in the mechanical properties of connective tissue in echinoderms. These mechanisms probably depend not only on the number of cross-links between the molecules, but also on the composition of ECM and the properties of its proteins. Full article
(This article belongs to the Special Issue The Mutable Collagenous Tissue of Echinoderms: Biological, Biomedical, and Biomimetic Aspects)
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31 pages, 11679 KiB  
Review
Morphological and Physiological Aspects of Mutable Collagenous Tissue at the Autotomy Plane of the Starfish Asterias rubens L. (Echinodermata, Asteroidea): An Echinoderm Paradigm
by Iain C. Wilkie and M. Daniela Candia Carnevali
Mar. Drugs 2023, 21(3), 138; https://doi.org/10.3390/md21030138 - 22 Feb 2023
Cited by 5 | Viewed by 3165
Abstract
The mutable collagenous tissue (MCT) of echinoderms has the capacity to undergo changes in its tensile properties within a timescale of seconds under the control of the nervous system. All echinoderm autotomy (defensive self-detachment) mechanisms depend on the extreme destabilisation of mutable collagenous [...] Read more.
The mutable collagenous tissue (MCT) of echinoderms has the capacity to undergo changes in its tensile properties within a timescale of seconds under the control of the nervous system. All echinoderm autotomy (defensive self-detachment) mechanisms depend on the extreme destabilisation of mutable collagenous structures at the plane of separation. This review illustrates the role of MCT in autotomy by bringing together previously published and new information on the basal arm autotomy plane of the starfish Asterias rubens L. It focuses on the MCT components of breakage zones in the dorsolateral and ambulacral regions of the body wall, and details data on their structural organisation and physiology. Information is also provided on the extrinsic stomach retractor apparatus whose involvement in autotomy has not been previously recognised. We show that the arm autotomy plane of A. rubens is a tractable model system for addressing outstanding problems in MCT biology. It is amenable to in vitro pharmacological investigations using isolated preparations and provides an opportunity for the application of comparative proteomic analysis and other “-omics” methods which are aimed at the molecular profiling of different mechanical states and characterising effector cell functions. Full article
(This article belongs to the Special Issue The Mutable Collagenous Tissue of Echinoderms: Biological, Biomedical, and Biomimetic Aspects)
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17 pages, 4135 KiB  
Review
Morphological, Physiological and Mechanical Features of the Mutable Collagenous Tissues Associated with Autotomy and Evisceration in Dendrochirotid Holothuroids
by Maria Byrne
Mar. Drugs 2023, 21(3), 134; https://doi.org/10.3390/md21030134 - 21 Feb 2023
Cited by 2 | Viewed by 1277
Abstract
Evisceration in dendrochirotid sea cucumbers leads to expulsion of the digestive tract, pharyrngeal complex and coelomic fluid through rupture of the anterior body wall. This process involves failure of three mutable collagenous tissue (MCT) structures, the introvert, the pharyngeal retractor muscle tendon, and [...] Read more.
Evisceration in dendrochirotid sea cucumbers leads to expulsion of the digestive tract, pharyrngeal complex and coelomic fluid through rupture of the anterior body wall. This process involves failure of three mutable collagenous tissue (MCT) structures, the introvert, the pharyngeal retractor muscle tendon, and the intestine-cloacal junction. These are complex structures composed of several tissue strata. The MCT in the three autotomy structures contains collagen fibrils, unstriated microfibrils, and interfibrillar molecules. Neurosecretory-like processes (juxtaligamental-type) with large dense vesicles (LDVs) are prominent in the autotomy structures. Biomechanical tests show that these structures are not inherently weak. Failure of the autotomy structures can be elicited by manipulating the ionic environment and the changes are blocked by anaesthetics. Autotomy and evisceration are under neural control, but local neural elements and neurosecretory-like processes do not appear to be a source of factors that cause MCT destabilisation. The LDVs remain intact while the tissue destabilises. The coelomic fluid contains an evisceration inducing factor indicating a neurosecretory-like mediation of autotomy. This factor elicits muscle contraction and MCT destabilisation. As the autotomy structures are completely or partially surrounded by coelomic fluid, the agent(s) of change may be located in the coelom (systemic origin) as well as originate from cells within the MCT. The biochemistry and mechanism(s) of action of the evisceration factor are not known. This factor is a promising candidate for biodiscovery investigation. Full article
(This article belongs to the Special Issue The Mutable Collagenous Tissue of Echinoderms: Biological, Biomedical, and Biomimetic Aspects)
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