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      Body wall structure in the starfish Asterias rubens

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          Abstract

          The body wall of starfish is composed of magnesium calcite ossicles connected by collagenous tissue and muscles and it exhibits remarkable variability in stiffness, which is attributed to the mechanical mutability of the collagenous component. Using the common European starfish Asterias rubens as an experimental animal, here we have employed a variety of techniques to gain new insights into the structure of the starfish body wall. The structure and organisation of muscular and collagenous components of the body wall were analysed using trichrome staining. The muscle system comprises interossicular muscles as well as muscle strands that connect ossicles with the circular muscle layer of the coelomic lining. The collagenous tissue surrounding the ossicle network contains collagen fibres that form loop‐shaped straps that wrap around calcite struts near to the surface of ossicles. The 3D architecture of the calcareous endoskeleton was visualised for the first time using X‐ray microtomography, revealing the shapes and interactions of different ossicle types. Furthermore, analysis of the anatomical organisation of the ossicles indicates how changes in body shape may be achieved by local contraction/relaxation of interossicular muscles. Scanning synchrotron small‐angle X‐ray diffraction ( SAXD) scans of the starfish aboral body wall and ambulacrum were used to study the collagenous tissue component at the fibrillar level. Collagen fibrils in aboral body wall were found to exhibit variable degrees of alignment, with high levels of alignment probably corresponding to regions where collagenous tissue is under tension. Collagen fibrils in the ambulacrum had a uniformly low degree of orientation, attributed to macrocrimp of the fibrils and the presence of slanted as well as horizontal fibrils connecting antimeric ambulacral ossicles. Body wall collagen fibril D‐period lengths were similar to previously reported mammalian D‐periods, but were significantly different between the aboral and ambulacral samples. The overlap/D‐period length ratio within fibrils was higher than reported for mammalian tissues. Collectively, the data reported here provide new insights into the anatomy of the body wall in A. rubens and a foundation for further studies investigating the structural basis of the mechanical properties of echinoderm body wall tissue composites.

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          Calcitic microlenses as part of the photoreceptor system in brittlestars.

          Photosensitivity in most echinoderms has been attributed to 'diffuse' dermal receptors. Here we report that certain single calcite crystals used by brittlestars for skeletal construction are also a component of specialized photosensory organs, conceivably with the function of a compound eye. The analysis of arm ossicles in Ophiocoma showed that in light-sensitive species, the periphery of the labyrinthic calcitic skeleton extends into a regular array of spherical microstructures that have a characteristic double-lens design. These structures are absent in light-indifferent species. Photolithographic experiments in which a photoresist film was illuminated through the lens array showed selective exposure of the photoresist under the lens centres. These results provide experimental evidence that the microlenses are optical elements that guide and focus the light inside the tissue. The estimated focal distance (4-7 micrometer below the lenses) coincides with the location of nerve bundles-the presumed primary photoreceptors. The lens array is designed to minimize spherical aberration and birefringence and to detect light from a particular direction. The optical performance is further optimized by phototropic chromatophores that regulate the dose of illumination reaching the receptors. These structures represent an example of a multifunctional biomaterial that fulfills both mechanical and optical functions.
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            Cooperative deformation of mineral and collagen in bone at the nanoscale.

            In biomineralized tissues such as bone, the recurring structural motif at the supramolecular level is an anisotropic stiff inorganic component reinforcing the soft organic matrix. The high toughness and defect tolerance of natural biomineralized composites is believed to arise from these nanometer scale structural motifs. Specifically, load transfer in bone has been proposed to occur by a transfer of tensile strains between the stiff inorganic (mineral apatite) particles via shearing in the intervening soft organic (collagen) layers. This raises the question as to how and to what extent do the mineral particles and fibrils deform concurrently in response to tissue deformation. Here we show that both mineral nanoparticles and the enclosing mineralized fibril deform initially elastically, but to different degrees. Using in situ tensile testing with combined high brilliance synchrotron X-ray diffraction and scattering on the same sample, we show that tissue, fibrils, and mineral particles take up successively lower levels of strain, in a ratio of 12:5:2. The maximum strain seen in mineral nanoparticles (approximately 0.15-0.20%) can reach up to twice the fracture strain calculated for bulk apatite. The results are consistent with a staggered model of load transfer in bone matrix, exemplifying the hierarchical nature of bone deformation. We believe this process results in a mechanism of fibril-matrix decoupling for protecting the brittle mineral phase in bone, while effectively redistributing the strain energy within the bone tissue.
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              On the tear resistance of skin

              Tear resistance is of vital importance in the various functions of skin, especially protection from predatorial attack. Here, we mechanistically quantify the extreme tear resistance of skin and identify the underlying structural features, which lead to its sophisticated failure mechanisms. We explain why it is virtually impossible to propagate a tear in rabbit skin, chosen as a model material for the dermis of vertebrates. We express the deformation in terms of four mechanisms of collagen fibril activity in skin under tensile loading that virtually eliminate the possibility of tearing in pre-notched samples: fibril straightening, fibril reorientation towards the tensile direction, elastic stretching and interfibrillar sliding, all of which contribute to the redistribution of the stresses at the notch tip.
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                Author and article information

                Contributors
                h.gupta@qmul.ac.uk
                m.r.elphick@qmul.ac.uk
                Journal
                J Anat
                J. Anat
                10.1111/(ISSN)1469-7580
                JOA
                Journal of Anatomy
                John Wiley and Sons Inc. (Hoboken )
                0021-8782
                1469-7580
                16 July 2017
                September 2017
                16 July 2017
                : 231
                : 3 ( doiID: 10.1111/joa.2017.231.issue-3 )
                : 325-341
                Affiliations
                [ 1 ] School of Biological & Chemical Sciences Queen Mary University of London London UK
                [ 2 ] School of Engineering & Materials Science Queen Mary University of London London UK
                [ 3 ] Institute of Dentistry Barts and The London School of Medicine and Dentistry Queen Mary University of London London UK
                [ 4 ] Diamond Light Source Ltd Didcot Oxfordshire UK
                Author notes
                [*] [* ] Correspondence

                Maurice R. Elphick, School of Biological & Chemical Sciences, Queen Mary University of London, London E1 4NS, UK. T: + 44 0207 8825290; F: + 44 0207 8827732; E: m.r.elphick@ 123456qmul.ac.uk ; Himadri S. Gupta, School of Engineering & Materials Science, Queen Mary University of London, London E1 4NS, UK. T: + 44 0207 8828867; F: + 44 0207 8823390; E: h.gupta@ 123456qmul.ac.uk

                Author information
                http://orcid.org/0000-0002-9169-0048
                Article
                JOA12646
                10.1111/joa.12646
                5554833
                28714118
                76300cf4-e864-47f8-b414-fa817b0194c8
                © 2017 The Authors. Journal of Anatomy published by John Wiley & Sons Ltd on behalf of Anatomical Society.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 25 April 2017
                Page count
                Figures: 6, Tables: 0, Pages: 17, Words: 13535
                Funding
                Funded by: Queen Mary University of London
                Funded by: Engineering & Physical Sciences Research Council
                Award ID: EP/J501360/1
                Funded by: Biotechnology and Biological Sciences Research Council
                Award ID: BBSRC;BB/M001644/1
                Funded by: Royal Society through the Equipment Grant scheme
                Award ID: SEMF1A6R
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                joa12646
                September 2017
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.1.7 mode:remove_FC converted:14.08.2017

                Anatomy & Physiology
                body wall,collagen,echinoderm,ossicle,scanning synchrotron small‐angle x‐ray diffraction,starfish,x‐ray microtomography

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