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      Composition of Glycosaminoglycans in Elasmobranchs including Several Deep-Sea Sharks: Identification of Chondroitin/Dermatan Sulfate from the Dried Fins of Isurus oxyrinchus and Prionace glauca

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          Abstract

          Shark fin, used as a food, is a rich source of glycosaminoglyans (GAGs), acidic polysaccharides having important biological activities, suggesting their nutraceutical and pharmaceutical application. A comprehensive survey of GAGs derived from the fin was performed on 11 elasmobranchs, including several deep sea sharks. Chondroitin sulfate (CS) and hyaluronic acid (HA) were found in Isurus oxyrinchus, Prionace glauca, Scyliorhinus torazame, Deania calcea, Chlamydoselachus anguineus, Mitsukurina owatoni, Mustelus griseus and Dasyatis akajei, respectively. CS was only found from Chimaera phantasma, Dalatias licha, and Odontaspis ferox, respectively. Characteristic disaccharide units of most of the CS were comprised of C- and D-type units. Interestingly, substantial amount of CS/dermatan sulfate (DS) was found in the dried fin (without skin and cartilage) of Isurus oxyrinchus and Prionace glauca. 1H-NMR analysis showed that the composition of glucuronic acid (GlcA) and iduronic acid (IdoA) in shark CS/DS was 41.2% and 58.8% ( Isurus oxyrinchus), 36.1% and 63.9% ( Prionace glauca), respectively. Furthermore, a substantial proportion of this CS/DS consisted of E-, B- and D-type units. Shark CS/DS stimulated neurite outgrowth of hippocampal neurons at a similar level as DS derived from invertebrate species. Midkine and pleiotrophin interact strongly with CS/DS from Isurus oxyrinchus and Prionace glauca, affording K d values of 1.07 nM, 6.25 nM and 1.70 nM, 1.88 nM, respectively. These results strongly suggest that the IdoA-rich domain of CS/DS is required for neurite outgrowth activity. A detailed examination of oligosaccharide residues, produced by chondroitinase ACII digestion, suggested that the IdoA and B-type units as well as A- and C-type units were found in clusters in shark CS/DS. In addition, it was discovered that the contents of B-type units in these IdoA-rich domain increased in a length dependent manner, while C- and D-type units were located particularly in the immediate vicinity of the IdoA-rich domain.

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          Most cited references32

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          Recent advances in the structural biology of chondroitin sulfate and dermatan sulfate.

          Recent glycobiology studies have suggested fundamental biological functions for chondroitin, chondroitin sulfate and dermatan sulfate, which are widely distributed as glycosaminoglycan sidechains of proteoglycans in the extracellular matrix and at cell surfaces. They have been implicated in the signaling functions of various heparin-binding growth factors and chemokines, and play critical roles in the development of the central nervous system. They also function as receptors for various pathogens. These functions are closely associated with the sulfation patterns of the glycosaminoglycan chains. Surprisingly, nonsulfated chondroitin is indispensable in the morphogenesis and cell division of Caenorhabditis elegans, as revealed by RNA interference experiments of the recently cloned chondroitin synthase gene and by the analysis of mutants of squashed vulva genes.
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            Recent advances in the study of the biosynthesis and functions of sulfated glycosaminoglycans.

            Recent cDNA cloning of the glycosyltransferases involved in the synthesis of the sulfated glycosaminoglycan sidechains of proteoglycans has provided important clues to answering long-standing questions concerning the mechanisms of both chain polymerization and the biosynthetic sorting of glucosaminoglycans (heparin/heparan sulfate) and galactosaminoglycans (chondroitin/dermatan sulfate). These biosynthetic mechanisms are crucial to the expression and regulation of the biological functions of glycosaminoglycans in development and pathophysiology.
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              Chondroitin/dermatan sulfate in the central nervous system.

              In the central nervous system (CNS) chondroitin sulfate proteoglycans, as one of the major barrier-forming molecules, influence cell migration patterns and axon pathfinding. By contrast, chondroitin sulfate side chains often form hybrid chains with dermatan sulfate and serve as a neural stem cell marker and neurogenic/neuritogenic molecules involved in neural stem cell proliferation. Hybrid chondroitin/dermatan sulfate chains are also involved in formation of the neural network by capturing and presenting heparin-binding growth factors like basic fibroblast growth factor, pleiotrophin, and hepatocyte growth factor to stem cells or neuronal cells. Research tools for structural glycobiology are emerging to perform a high-throughput screening of glycosaminoglycans for the binding to ligands, to decipher sulfation patterns of rare functional oligosaccharide sequences and to build structural models for the shape of such sulfated oligosaccharides.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                24 March 2015
                2015
                : 10
                : 3
                : e0120860
                Affiliations
                [1 ]Graduate School of Pharmaceutical Sciences, Chiba University, 1-8-1 Inohana, Chuo-ku, Chiba 260-8675, Japan
                [2 ]Faculty of Pharmacy, Chiba Institute of Science, 15-8 Shiomi-cho, Choshi, Chiba 288-0025, Japan
                [3 ]Natural History Museum and Institute, 955-2 Aoba-cho, Chuo-ku, Chiba 260-8682, Japan
                [4 ]Department of Biology, Center for Biotechnology and Interdisciplinary Studies, Rensselaer Polytechnic Institute, 110 8th Street, Troy, New York, United States of America
                University of Patras, GREECE
                Author notes

                Competing Interests: Dried fins (without skin and cartilage) of Isurus oxyrinchus and Prionace glauca and raw fin (without skin) of Prionace glauca were kindly provided by Mrs. T. Mano and T. Wada (Nihon Pharmaceutical Co. Ltd.). This does not alter the authors' adherence to PLOS ONE policies on sharing data and materials.

                Conceived and designed the experiments: KH MM TT. Performed the experiments: KH YT AM HT. Analyzed the data: KH MM RJL TT. Contributed reagents/materials/analysis tools: TT. Wrote the paper: KH MM RJL TT.

                Article
                PONE-D-14-37186
                10.1371/journal.pone.0120860
                4372294
                25803296
                d5914d16-8875-4251-a7ca-272cd914180b
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 1 September 2014
                : 27 January 2015
                Page count
                Figures: 7, Tables: 1, Pages: 15
                Funding
                The work was funded by 24590046 Grant-in-Aid for Scientific Research ( http://www-shinsei.jsps.go.jp/kaken/index.html) TT. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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