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RSC Advances REVIEW View Article Online View Journal | View Issue Naphthoquinones of the spinochrome class: occurrence, isolation, biosynthesis and biomedical Cite this: RSC Adv.,2018,8,32637 applications Yakun Hou, a Elena A. Vasileva,b Alan Carne,c Michelle McConnell,d Alaa El-Din A. Bekhit a and Natalia P. Mishchenko*b Quinones are widespread in nature and have been found in plants, fungi and bacteria, as well as in members of the animal kingdom. More than forty closely related naphthoquinones have been found in echinoderms, mainly in sea urchins but occasionally in brittle stars, sea stars and starfish. This review aims to examine controversial issues on the chemistry, biosynthesis, functions, stability and application aspects of the spinochrome class, a prominent group of secondary metabolites found in sea urchins. The emphasis of this review is on the isolation and structure of these compounds, together with evaluation of their Received 5th June 2018 relevant biological activities, source organisms, the location of origin and methods used for isolation and Accepted 17th August 2018 Creative Commons Attribution-NonCommercial 3.0 Unported Licence. identification. In addition, the studies of their biosynthesis and ecological function, stability and chemical DOI: 10.1039/c8ra04777d synthesis have been highlighted. This review aims to establish a focus for future spinochrome research rsc.li/rsc-advances and its potential for benefiting human health and well-being. 1. Introduction biosynthesis, distribution, isolation and identication tech- niques, stability, synthesis and biomedical applications is Rational use of biological resources of the aquatic environment presented. is a realistic scientic and practical goal since they represent This article is licensed under a 70% of the organisms on earth. Marine hydrobionts, such as sea urchins, and specically their gonads, are a valuable renewable 2. The structure and nomenclature of food resource. At the same time, they can serve as a unique spinochromes source of various natural compounds, which can be the basis Open Access Article. Published on 21 September 2018. Downloaded 9/28/2021 5:31:31 PM. for the creation of various biomaterials,1,2 effective medicinal Spinochromes are polyhydroxylated derivatives of either juglone and parapharmaceutical preparations,3 as well as functional (5-hydroxy-1,4-naphthoquinone) or naphthazarin (5,8- food products.3–5 Many species of regular sea urchins are dihydroxy-1,4-naphthoquinone) that are substituted with commercially harvested because their gonads are consumed in various functional groups such as ethyl, acetyl, methoxyl, and many countries of Asia, the Mediterranean and North America. amino groups. The rst discovered compound of this class, Aer the removal of the gonads, large amounts of sea urchin a red pigment in the perivisceral (coelomic) uid of Echinus shells are le as waste. This shell material is rich in bioactive esculentus was called ‘echinochrome’, without knowing its quinonoid pigments, principally spinochromes.4–6 Although chemical composition.9 The structure of this ‘echinochrome’ this class of compounds has been known for over 100 years,7,8 was established later by Kuhn and Wallenfels (1940)10 as 6-ethyl- there is still some controversy in relation to their structures, 2,3,7-trihydroxynaphthazarin and it was named echinochrome stability, biosynthesis and ecological functions. In this review, A (Table 1, structure 1). Subsequently, a number of pigment a critical evaluation of existing data on spinochrome structures, compounds were isolated from the shells and spines of various sea urchin species, which were named spinochromes to aDepartment of Food Science, University of Otago, PO Box 56, Dunedin 9054, New distinguish them from the echinochrome A found in the 7 Zealand coelomic uid, ovaries and internal organs of sea urchins. bLaboratory of the Chemistry of Natural Quinonoid Compounds, G.B. Elyakov Pacic However, it was found later that echinochrome A is also a major Institute of Bioorganic Chemistry, Far Eastern Branch of Russian Academy of Sciences, pigment component of the shells and spines of many sea Prospect 100 let Vladivostoku 159/2, 690022, Vladivostok, Russia. E-mail: urchins, so it was assigned to the class of spinochromes, but the [email protected] 18 c original name echinochrome has remained. Department of Biochemistry, University of Otago, PO Box 56, Dunedin 9054, New Zealand New spinochromes were named based on the rst letter of dDepartment of Microbiology and Immunology, University of Otago, PO Box 56, the name of the sea urchin species that they were isolated from, Dunedin 9054, New Zealand as for example, spinochrome P was rst isolated from This journal is © The Royal Society of Chemistry 2018 RSC Adv.,2018,8, 32637–32650 | 32637 View Article Online RSC Advances 32638 Table 1 Structures of known spinochromes | RSC Adv. ,2018, 8 , 32637 Creative Commons Attribution-NonCommercial 3.0 Unported Licence. – 32650 This article is licensed under a Open Access Article. Published on 21 September 2018. Downloaded 9/28/2021 5:31:31 PM. No. Structure elucidation R2 R3 R5 R6 R7 R8 Molecular formula Molecular mass Trivial name References 1 6-Ethyl-2,3,5,7,8-pentahydroxy-1,4-naphthoquinone OH OH OH C2H5 OH OH C12H9O7 265 Echinochrome A 7 2 2-Acetyl-3,5,6,8-tetrahydoxy-1,4-naphthoquinone COCH3 OH OH OH H OH C12H7O7 263 Spinochrome A 7 This journal is © The Royal Society of Chemistry 2018 3 2,3,5,7-Tetrahydroxy-1,4-naphthoquinone OH OH OH H OH H C10H6O6 221 Spinochrome B 7 4 2-Acetyl-3,5,6,7,8-pentahydroxy-1,4-naphthoquinone COCH3 OH OH OH OH OH C12H7O8 279 Spinochrome C 7 5 2,3,5,7,8-Pentahydroxy-1,4-naphthoquinone OH OH OH H OH OH C10H6O7 237 Spinochrome D 7 6 2,3,5,6,7,8-Hexahydroxy-1,4-naphthoquinone OH OH OH OH OH OH C10H6O8 252 Spinochrome E 7 7 6-Ethyl-2,5-dihydroxy-1,4-naphthoquinone OH H OH C2H5 HHC12H10O4 218 11 8 6-Acetyl-2,5,7-trihydroxy-1,4-naphthoquinone OH H OH COCH3 OH H C12H8O6 248 11 9 6-Ethyl-2,3,5,7-tetrahydroxy-1,4-naphthoquinone OH OH OH C2H5 OH H C12H10O6 250 11 10 6-Acetyl-2,3,5,7-tetrahydroxy-1,4-naphthoquinone OH OH OH COCH3 OH H C12H8O7 264 11 11 3-Acetyl-2,5,6,7-tetrahydroxy-1,4-naphthoquinone OH COCH3 OH OH OH H C12O7H8 264 11 12 2,5,8-Tryihydroxy-1,4-naphthoquinone OH H OH H H OH C10O5H6 206 Naphthopurpurin 11 13 3-Acetyl-2,5,8-trihydroxy-1,4-naphthoquinone OH COCH3 OH H H OH C12O6H8 248 11 14 6-Ethyl-2,5,8-trihydroxy-1,4-naphthoquinone OH H OH C2H5 HOHC12O5H10 234 11 15 6-Acetyl-2,5,8-trihydroxy-1,4-naphthoquinone OH H OH COCH3 HOHC12O6H8 248 11 16 3-Ethyl-2,5,7,8-tetrahydroxy-1,4-naphthoquinone OH C2H5 OH H OH OH C12H10O6 250 11 17 2,5,7,8-Tetrahydroxy-1,4-naphthoquinone OH H OH H OH OH C H O 222 Mompain 11 10 6 6 Review 0 0 18 2-Hydroxy-2 -methyl-2 H-pyrano[2,3-b]naphthazarin OH OH C4-unit OH 12 View Article Online Review This journal is © The Royal Society of Chemistry 2018 Table 1 (Contd.) Creative Commons Attribution-NonCommercial 3.0 Unported Licence. This article is licensed under a Open Access Article. Published on 21 September 2018. Downloaded 9/28/2021 5:31:31 PM. No. Structure elucidation R2 R3 R5 R6 R7 R8 Molecular formula Molecular mass Trivial name References 19 3-Acetyl-2,7-dihydroxy-6-methyl-1,4-naphthoquinone OH CH3CO OH CH3 OH OH C13H11O7 278 12 20 6-Ethyl-3,5,6,8-tetrahydroxy-2-methoxy-1,4-naphthoquinone OCH3 OH OH C2H5 OH OH C13H12O7 280 13 21 6-ethyl-2,5,6,8-tetrahydroxy-3-methoxy-1,4-naphthoquinone OH OCH3 OH C2H5 OH OH C13H12O7 280 13 22 3,5,6,7,8-Pentahydroxy-2-methoxy-1,4-naphthoquinone OCH3 OH OH OH OH OH C11H8O8 268 Namakochrome 14 RSC Adv. 28 2,3,5,8-Tetrahydroxy-1,4-naphthoquinone OH OH OH H H OH C10H6O6 222 Spinazarin 15 29 6-Ethyl-2,3,5,8-tetrahydroxy-1,4-naphthoquinone OH OH OH C2H5 HOHC12H10O6 250 Ethylspinazarin 15 30 3-Amino-6-ethyl-2,5,6,8-tetrahydroxy-1,4-naphthoquinone OH NH OH C H OH H C H NO 265 Echinamine A 16 ,2018, 2 2 5 12 11 6 31 2-Amino-6-ethyl-3,5,7,8-tetrahydroxy-1,4-naphthoquinone NH2 OH OH C2H5 OH OH C12H11NO6 265 Echinamine B 16 32 2-Amino-3,5,6,7,8-pentahydroxy-1,4-naphthoquinone NH2 OH OH OH OH OH C10H7NO7 253 Spinamine E 17 8 , 32637 – RSC Advances 32650 | 32639 View Article Online RSC Advances Review Paracentrotus lividus. Spinochromes extracted from several sea ones with characteristics similar to compounds 23 and 25 and its urchin species have been named as spinochromes A, F, C, M anhydrous derivative with characteristics similar to compounds 24 and H as well as others that can be found in the literature.18 It and 26 were isolated from the tropical sea urchin Astropyga radiata, was later shown that many quinones previously designated with and their structures were analysed using 2D-NMR procedures that different letters are in fact the same compound. Goodwin and were not available earlier.26 It was established that these Srisukh (1950)19 revised the nomenclature of all spinochromes compounds predominantly exist as ethylidene-3,30-bis(2,6,7- known at that time and proposed naming them in alphabetic trihydroxynaphthazarin) (23)and7,70-anhydroethylidene-6,60- order, as spinochromes A (2), B (3), C (4), D (5) and E (6), as bis(2,3,7-trihydroxynaphthazarin) (26), respectively.26 In addition indicated for the structures summarised in Table 1.
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  • Metallothionein Gene Family in the Sea Urchin Paracentrotus Lividus: Gene Structure, Differential Expression and Phylogenetic Analysis

    Metallothionein Gene Family in the Sea Urchin Paracentrotus Lividus: Gene Structure, Differential Expression and Phylogenetic Analysis

    International Journal of Molecular Sciences Article Metallothionein Gene Family in the Sea Urchin Paracentrotus lividus: Gene Structure, Differential Expression and Phylogenetic Analysis Maria Antonietta Ragusa 1,*, Aldo Nicosia 2, Salvatore Costa 1, Angela Cuttitta 2 and Fabrizio Gianguzza 1 1 Department of Biological, Chemical, and Pharmaceutical Sciences and Technologies, University of Palermo, 90128 Palermo, Italy; [email protected] (S.C.); [email protected] (F.G.) 2 Laboratory of Molecular Ecology and Biotechnology, National Research Council-Institute for Marine and Coastal Environment (IAMC-CNR) Detached Unit of Capo Granitola, Torretta Granitola, 91021 Trapani, Italy; [email protected] (A.N.); [email protected] (A.C.) * Correspondence: [email protected]; Tel.: +39-091-238-97401 Academic Editor: Masatoshi Maki Received: 6 March 2017; Accepted: 5 April 2017; Published: 12 April 2017 Abstract: Metallothioneins (MT) are small and cysteine-rich proteins that bind metal ions such as zinc, copper, cadmium, and nickel. In order to shed some light on MT gene structure and evolution, we cloned seven Paracentrotus lividus MT genes, comparing them to Echinodermata and Chordata genes. Moreover, we performed a phylogenetic analysis of 32 MTs from different classes of echinoderms and 13 MTs from the most ancient chordates, highlighting the relationships between them. Since MTs have multiple roles in the cells, we performed RT-qPCR and in situ hybridization experiments to understand better MT functions in sea urchin embryos. Results showed that the expression of MTs is regulated throughout development in a cell type-specific manner and in response to various metals. The MT7 transcript is expressed in all tissues, especially in the stomach and in the intestine of the larva, but it is less metal-responsive.
  • Paleogenomics of Echinoids Reveals an Ancient Origin for the Double-Negative Specification of Micromeres in Sea Urchins

    Paleogenomics of Echinoids Reveals an Ancient Origin for the Double-Negative Specification of Micromeres in Sea Urchins

    Paleogenomics of echinoids reveals an ancient origin for the double-negative specification of micromeres in sea urchins Jeffrey R. Thompsona,1, Eric M. Erkenbrackb, Veronica F. Hinmanc, Brenna S. McCauleyc,d, Elizabeth Petsiosa, and David J. Bottjera aDepartment of Earth Sciences, University of Southern California, Los Angeles, CA 90089; bDepartment of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06511; cDepartment of Biological Sciences, Carnegie Mellon University, Pittsburgh, PA 15213; and dHuffington Center on Aging, Baylor College of Medicine, Houston, TX 77030 Edited by Douglas H. Erwin, Smithsonian National Museum of Natural History, Washington, DC, and accepted by Editorial Board Member Neil H. Shubin January 31, 2017 (received for review August 2, 2016) Establishing a timeline for the evolution of novelties is a common, methods thus provide a rigorous methodology in which to examine unifying goal at the intersection of evolutionary and developmental gene expression datasets, and ultimately animal body plan evolu- biology. Analyses of gene regulatory networks (GRNs) provide the tion (11), within the context of evolutionary time. After genomic ability to understand the underlying genetic and developmental novelties underlying differential body plan development have been mechanisms responsible for the origin of morphological structures identified, we can then consider the rates at which these novelties both in the development of an individual and across entire evolution- arise, and the rates at which GRNs evolve. Achieving this end ary lineages. Accurately dating GRN novelties, thereby establishing requires an explicit timeline in which to explore GRN evolution. a timeline for GRN evolution, is necessary to answer questions In a phylogenetically informed, comparative framework, it is about the rate at which GRNs and their subcircuits evolve, and to possible to infer where on a phylogenetic tree and when, in deep tie their evolution to paleoenvironmental and paleoecological time, GRN innovations are likely to have first arisen.