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Echinoderms Metabolites: Structure, Functions and Biomedical Perspectives

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A special issue of Marine Drugs (ISSN 1660-3397).

Deadline for manuscript submissions: closed (23 January 2021) | Viewed by 22595

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Dr. Vladimir I. Kalinin

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G.B. Elyakov Pacific Institute of Bioorganic Chemistry of the Far East Branch of the Russian Academy of Sciences, Pr. 100-letya Vladivostoka 159, 690022 Vladivostok, Russia
Interests: marine natural product chemistry; secondary metabolites; sea cucumber triterpene glycosides; biological activities; evolution of biosynthesis; chemotaxonomy
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Dear Colleagues,

Echinoderms are marine invertebrates belonging to the phylum Echinodermata (from the Ancient Greek words “echinos” (hedgehog) and “derma” (skin)). They have radial symmetry, a unique water vascular (ambulacral) system, and a limestone skeleton and include the classes Asteroidea (starfish), Ophiuroidea (brittle stars), Echinoidea (sea urchins), Holothuroidea (sea cucumbers), and Crinoidea (sea lilies). The skeleton of sea cucumbers is reduced by ossicles. Echinoderms have no freshwater or terrestrial representatives and are habitants of every ocean depth. The phylum contains more than 7000 living species. Echinoderms are unique sources of different metabolites having a wide spectrum of biological activities. All echinoderms possess a unique mechanism of decreasing the lever of free 5,6-unsaturated sterols in their cell membranes—sulfation of these food sterols. Moreover, sea cucumbers and starfish transform these 5,6-unsaturated sterols to stanols or 7,8-unsaturated sterols that allow them to synthesize and keep their own 5,6-sterol-depending membranolytic toxins, namely triterpene oligoglycosides for sea cucumbers and steroid olygoglycosides for starfish, which have protective significance for the producers. Starfish and brittle stars have numerous polyhydoxysteroids and their sulfated and glycosylated derivatives, using them as food emulgators. All echinoderms contain carotenoids and naphthoquinone pigments. The latter are widely presented in sea urchins. The lipid composition of echinoderms is also uncommon and very interesting. For example, they contain cerebrosides and gangliosides characteristic of other deuterostomes including Chordata, Hemichordata, and Tunicata, relatives of echinoderms. Echinoderms contain lectins, glycan-specific glycoproteins having immunity functions for the producers, and glycoseaminoglycans. Microorganisms associated with some echninoderms and adopted to their toxins may also produce very uncommon metabolites, such as diterpene glycosides synthesized by some fungi associated with sea cucumbers. All the listed as well as other classes of echinoderm metabolites possess significant biomedical potential revealing cytotoxic, antitumor, antifungal, immunomodulatory, antioxidant activity, anti-arthritic, and anti-diabetic action and may be also used as a food supplement for nutrition. The main goal of this Special Issue “Echinoderm Metabolites: Structure, Functions, and Biomedical Perspectives” is to provide a convenient platform for discussion of all possible scientific aspects concerning low molecular weight and biopolymer metabolites from echinoderms and the microorganisms associated with them, including their isolation and chemical structures, taxonomical distribution and participation in food chains, methods of analysis, biological activities, biosynthesis and evolution, biological functions, and chemical syntheses, including the obtaining of semi-synthetic derivatives of biologically active natural products.

Dr. Vladimir I. Kalinin
Guest Editor

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Keywords

echinoderms
sea cucumbers
starfish
sea urchins
steroids
terpenoids
glycosides
naphtoquinones
glycolipids
polysaccharides
chemical structures
synthesis
biological activity

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Published Papers (9 papers)

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Editorial

Jump to: Research

4 pages, 198 KiB

Open AccessEditorial

Echinoderms Metabolites: Structure, Functions, and Biomedical Perspectives

by Vladimir I. Kalinin

Mar. Drugs 2021, 19(3), 125; https://doi.org/10.3390/md19030125 - 26 Feb 2021

Cited by 10 | Viewed by 2257

Abstract

Echinoderms are marine invertebrates belonging to the phylum Echinodermata (from the Ancient Greek words “echinos” (hedgehog) and “derma” (skin)) [...] Full article

(This article belongs to the Special Issue Echinoderms Metabolites: Structure, Functions and Biomedical Perspectives)

Research

Jump to: Editorial

29 pages, 6077 KiB

Open AccessArticle

Synthesis, Cytotoxic Activity Evaluation and Quantitative Structure-ActivityAnalysis of Substituted 5,8-Dihydroxy-1,4-naphthoquinones and Their O- and S-Glycoside Derivatives Tested against Neuro-2a Cancer Cells

by Sergey Polonik, Galina Likhatskaya, Yuri Sabutski, Dmitry Pelageev, Vladimir Denisenko, Evgeny Pislyagin, Ekaterina Chingizova, Ekaterina Menchinskaya and Dmitry Aminin

Mar. Drugs 2020, 18(12), 602; https://doi.org/10.3390/md18120602 - 29 Nov 2020

Cited by 8 | Viewed by 2713

Abstract

Based on 6,7-substituted 2,5,8-trihydroxy-1,4-naphtoquinones (1,4-NQs) derived from sea urchins, five new acetyl-O-glucosides of NQs were prepared. A new method of conjugation of per-O-acetylated 1-mercaptosaccharides with 2-hydroxy-1,4-NQs through a methylene spacer was developed. Methylation of 2-hydroxy group of quinone core of acetylthiomethylglycosides by diazomethane and deacetylation of sugar moiety led to 28 new thiomethylglycosidesof 2-hydroxy- and 2-methoxy-1,4-NQs. The cytotoxic activity of starting 1,4-NQs (13 compounds) and their O- and S-glycoside derivatives (37 compounds) was determined by the MTT method against Neuro-2a mouse neuroblastoma cells. Cytotoxic compounds with EC₅₀ = 2.7–87.0 μM and nontoxic compounds with EC₅₀ > 100 μM were found. Acetylated O- and S-glycosides 1,4-NQs were the most potent, with EC₅₀ = 2.7–16.4 μM. Methylation of the 2-OH group innaphthoquinone core led to a sharp increase in the cytotoxic activity of acetylated thioglycosidesof NQs, which was partially retained for their deacetylated derivatives. Thiomethylglycosides of 2-hydroxy-1,4-NQs with OH and MeO groups in quinone core at positions 6 and 7, resprectively formed a nontoxic set of compounds with EC₅₀ > 100 μM. A quantitative structure-activity relationship (QSAR) model of cytotoxic activity of 22 1,4-NQ derivatives was constructed and tested. Descriptors related to the cytotoxic activity of new 1,4-NQ derivatives were determined. The QSAR model is good at predicting the activity of 1,4-NQ derivatives which are unused for QSAR models and nontoxic derivatives. Full article

(This article belongs to the Special Issue Echinoderms Metabolites: Structure, Functions and Biomedical Perspectives)

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20 pages, 6807 KiB

Open AccessArticle

Sterol Composition of Sponges, Cnidarians, Arthropods, Mollusks, and Echinoderms from the Deep Northwest Atlantic: A Comparison with Shallow Coastal Gulf of Mexico

by Laura Carreón-Palau, Nurgül Şen Özdemir, Christopher C. Parrish and Camilla Parzanini

Mar. Drugs 2020, 18(12), 598; https://doi.org/10.3390/md18120598 - 27 Nov 2020

Cited by 8 | Viewed by 3672

Abstract

Triterpenoid biosynthesis is generally anaerobic in bacteria and aerobic in Eukarya. The major class of triterpenoids in bacteria, the hopanoids, is different to that in Eukarya, the lanostanoids, and their 4,4,14-demethylated derivatives, sterols. In the deep sea, the prokaryotic contribution to primary productivity has been suggested to be higher because local environmental conditions prevent classic photosynthetic processes from occurring. Sterols have been used as trophic biomarkers because primary producers have different compositions, and they are incorporated in primary consumer tissues. In the present study, we inferred food supply to deep sea, sponges, cnidarians, mollusks, crustaceans, and echinoderms from euphotic zone production which is driven by phytoplankton eukaryotic autotrophy. Sterol composition was obtained by gas chromatography and mass spectrometry. Moreover, we compared the sterol composition of three phyla (i.e., Porifera, Cnidaria, and Echinodermata) collected between a deep and cold-water region and a shallow tropical area. We hypothesized that the sterol composition of shallow tropical benthic organisms would better reflect their photoautotrophic sources independently of the taxonomy. Shallow tropical sponges and cnidarians from environments showed plant and zooxanthellae sterols in their tissues, while their deep-sea counterparts showed phytoplankton and zooplankton sterols. In contrast, echinoids, a class of echinoderms, the most complex phylum along with hemichordates and chordates (deuterostomes), did not show significant differences in their sterol profile, suggesting that cholesterol synthesis is present in deuterostomes other than chordates. Full article

(This article belongs to the Special Issue Echinoderms Metabolites: Structure, Functions and Biomedical Perspectives)

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21 pages, 752 KiB

Open AccessArticle

Kurilosides A₁, A₂, C₁, D, E and F—Triterpene Glycosides from the Far Eastern Sea Cucumber Thyonidium (= Duasmodactyla) kurilensis (Levin): Structures with Unusual Non-Holostane Aglycones and Cytotoxicities

by Alexandra S. Silchenko, Anatoly I. Kalinovsky, Sergey A. Avilov, Pelageya V. Andrijaschenko, Roman S. Popov, Pavel S. Dmitrenok, Ekaterina A. Chingizova and Vladimir I. Kalinin

Mar. Drugs 2020, 18(11), 551; https://doi.org/10.3390/md18110551 - 6 Nov 2020

Cited by 11 | Viewed by 1945

Abstract

Six new monosulfated triterpene tetra-, penta- and hexaosides, namely, the kurilosides A₁ (1), A₂ (2), C₁ (3), D (4), E (5) and F (6), as well as the [...] Read more.

Six new monosulfated triterpene tetra-, penta- and hexaosides, namely, the kurilosides A₁ (1), A₂ (2), C₁ (3), D (4), E (5) and F (6), as well as the known earlier kuriloside A (7), having unusual non-holostane aglycones without lactone, have been isolated from the sea cucumber Thyonidium (= Duasmodactyla) kurilensis (Levin) (Cucumariidae, Dendrochirotida), collected in the Sea of Okhotsk near Onekotan Island from a depth of 100 m. Structures of the glycosides were established by 2D NMR spectroscopy and HR-ESI mass spectrometry. Kurilosides of the groups A and E contain carbohydrate moieties with a rare architecture (a pentasaccharide branched by C(4) Xyl1), differing from each other in the second monosaccharide residue (quinovose or glucose, correspondingly); kurilosides of the group C are characterized by a unique tetrasaccharide branched by a C(4) Xyl1 sugar chain; and kurilosides of the groups D and F are hexaosides differing from each other in the presence of an O-methyl group in the fourth (terminal) sugar unit. All these glycosides contain a sulfate group at C-6 of the glucose residue attached to C-4 Xyl1 and the non-holostane aglycones have a 9(11) double bond and lack γ-lactone. The cytotoxic activities of compounds 1–7 against mouse neuroblastoma Neuro 2a, normal epithelial JB-6 cells and erythrocytes were studied. Kuriloside A₁ (1) was the most active compound in the series, demonstrating strong cytotoxicity against the erythrocytes and JB-6 cells and a moderate effect against Neuro 2a cells. Full article

(This article belongs to the Special Issue Echinoderms Metabolites: Structure, Functions and Biomedical Perspectives)

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15 pages, 5998 KiB

Open AccessArticle

Antiviral Potential of Sea Urchin Aminated Spinochromes against Herpes Simplex Virus Type 1

by Natalia P. Mishchenko, Natalia V. Krylova, Olga V. Iunikhina, Elena A. Vasileva, Galina N. Likhatskaya, Evgeny A. Pislyagin, Darya V. Tarbeeva, Pavel S. Dmitrenok and Sergey A. Fedoreyev

Mar. Drugs 2020, 18(11), 550; https://doi.org/10.3390/md18110550 - 5 Nov 2020

Cited by 20 | Viewed by 2786

Abstract

Herpes simplex virus type 1 (HSV-1) is one of the most prevalent pathogens worldwide requiring the search for new candidates for the creation of antiherpetic drugs. The ability of sea urchin spinochromes—echinochrome A (EchA) and its aminated analogues, echinamines A (EamA) and B (EamB)—to inhibit different stages of HSV-1 infection in Vero cells and to reduce the virus-induced production of reactive oxygen species (ROS) was studied. We found that spinochromes exhibited maximum antiviral activity when HSV-1 was pretreated with these compounds, which indicated the direct effect of spinochromes on HSV-1 particles. EamB and EamA both showed the highest virucidal activity by inhibiting the HSV-1 plaque formation, with a selectivity index (SI) of 80.6 and 50.3, respectively, and a reduction in HSV-1 attachment to cells (SI of 8.5 and 5.8, respectively). EamA and EamB considerably suppressed the early induction of ROS due to the virus infection. The ability of the tested compounds to directly bind to the surface glycoprotein, gD, of HSV-1 was established in silico. The dock score of EchA, EamA, and EamB was −4.75, −5.09, and −5.19 kcal/mol, respectively, which correlated with the SI of the virucidal action of these compounds and explained their ability to suppress the attachment and penetration of the virus into the cells. Full article

(This article belongs to the Special Issue Echinoderms Metabolites: Structure, Functions and Biomedical Perspectives)

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10 pages, 1409 KiB

Open AccessArticle

Fucosylated Chondroitin Sulfates from the Sea Cucumbers Paracaudina chilensis and Holothuria hilla: Structures and Anticoagulant Activity

by Nadezhda E. Ustyuzhanina, Maria I. Bilan, Andrey S. Dmitrenok, Alexandra S. Silchenko, Boris B. Grebnev, Valentin A. Stonik, Nikolay E. Nifantiev and Anatolii I. Usov

Mar. Drugs 2020, 18(11), 540; https://doi.org/10.3390/md18110540 - 28 Oct 2020

Cited by 30 | Viewed by 2889

Abstract

Fucosylated chondroitin sulfates (FCSs) PC and HH were isolated from the sea cucumbers Paracaudina chilensis and Holothuria hilla, respectively. The purification of the polysaccharides was carried out by anion-exchange chromatography on a DEAE-Sephacel column. The structural characterization of the polysaccharides was performed in terms of monosaccharide and sulfate content, as well as using a series of nondestructive NMR spectroscopic methods. Both polysaccharides were shown to contain a chondroitin core [→3)-β-d-GalNAc (N-acethyl galactosamine)-(1→4)-β-d-GlcA (glucuronic acid)-(1→]_n, bearing sulfated fucosyl branches at O-3 of every GlcA residue in the chain. These fucosyl residues were different in their pattern of sulfation: PC contained Fuc2S4S and Fuc4S in a ratio of 2:1, whereas HH included Fuc2S4S, Fuc3S4S, and Fuc4S in a ratio of 1.5:1:1. Moreover, some GalNAc residues in HH were found to contain an unusual disaccharide branch Fuc4S-(1→2)-Fuc3S4S-(1→ at O-6. Sulfated GalNAc4S6S and GalNAc4S units were found in a ratio of 3:2 in PC and 2:1 in HH. Both polysaccharides demonstrated significant anticoagulant activity in a clotting time assay, which is connected with the ability of these FCSs to potentiate the inhibition of thrombin and factor Xa in the presence of anti-thrombin III (ATIII) and with the direct inhibition of thrombin in the absence of any cofactors. Full article

(This article belongs to the Special Issue Echinoderms Metabolites: Structure, Functions and Biomedical Perspectives)

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35 pages, 937 KiB

Open AccessArticle

Structures and Bioactivities of Quadrangularisosides A, A₁, B, B₁, B₂, C, C₁, D, D₁–D₄, and E from the Sea Cucumber Colochirus quadrangularis: The First Discovery of the Glycosides, Sulfated by C-4 of the Terminal 3-O-Methylglucose Residue. Synergetic Effect on Colony Formation of Tumor HT-29 Cells of these Glycosides with Radioactive Irradiation

Mar. Drugs 2020, 18(8), 394; https://doi.org/10.3390/md18080394 - 28 Jul 2020

Cited by 9 | Viewed by 2444

Abstract

Thirteen new mono-, di-, and trisulfated triterpene glycosides, quadrangularisosides A–D₄ (1−13) have been isolated from the sea cucumber Colochirus quadrangularis, which was collected in Vietnamese waters. The structures of these glycosides were established by 2D NMR spectroscopy and HR-ESI (High Resolution Electrospray Ionization) mass spectrometry. The novel carbohydrate moieties of quadrangularisosides D–D₄ (8−12), belonging to the group D, and quadrangularisoside E (13) contain three sulfate groups, with one of them occupying an unusual position—at C(4) of terminal 3-O-methylglucose residue. Quadrangularisosides A (1) and D₃ (11) as well as quadrangularisosides A₁ (2) and D₄ (12) are characterized by the new aglycones having 25-hydroperoxyl or 24-hydroperoxyl groups in their side chains, respectively. The cytotoxic activities of compounds 1–13 against mouse neuroblastoma Neuro 2a, normal epithelial JB-6 cells, erythrocytes, and human colorectal adenocarcinoma HT-29 cells were studied. All the compounds were rather strong hemolytics. The structural features that most affect the bioactivity of the glycosides are the presence of hydroperoxy groups in the side chains and the quantity of sulfate groups. The membranolytic activity of monosulfated quadrangularisosides of group A (1, 2) against Neuro 2a, JB-6 cells, and erythrocytes was relatively weak due to the availability of the hydroperoxyl group, whereas trisulfated quadrangularisosides D₃ (11) and D₄ (12) with the same aglycones as 1, 2 were the least active compounds in the series due to the combination of these two structural peculiarities. The erythrocytes were more sensitive to the action of the glycosides than Neuro 2a or JB-6 cells, but the structure–activity relationships observed for glycosides 1–13 were similar in the three cell lines investigated. The compounds 3−5, 8, and 9 effectively suppressed the cell viability of HT-29 cells. Quadrangularisosides A₁ (2), C (6), C₁ (7), and E (13) possessed strong inhibitory activity on colony formation in HT-29 cells. Due to the synergic effects of these glycosides (0.02 μM) and radioactive irradiation (1 Gy), a decreasing of number of colonies was detected. Glycosides 1, 3, and 9 enhanced the effect of radiation by about 30%. Full article

(This article belongs to the Special Issue Echinoderms Metabolites: Structure, Functions and Biomedical Perspectives)

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14 pages, 2209 KiB

Open AccessArticle

New Conjugates of Polyhydroxysteroids with Long-Chain Fatty Acids from the Deep-Water Far Eastern Starfish Ceramaster patagonicus and Their Anticancer Activity

by Timofey V. Malyarenko, Alla A. Kicha, Olesya S. Malyarenko, Viktor M. Zakharenko, Ivan P. Kotlyarov, Anatoly I. Kalinovsky, Roman S. Popov, Vasily I. Svetashev and Natalia V. Ivanchina

Mar. Drugs 2020, 18(5), 260; https://doi.org/10.3390/md18050260 - 15 May 2020

Cited by 3 | Viewed by 4626

Abstract

Four new conjugates, esters of polyhydroxysteroids with long-chain fatty acids (1–4), were isolated from the deep-water Far Eastern starfish Ceramaster patagonicus. The structures of 1–4 were established by NMR and ESIMS techniques as well as chemical transformations. Unusual compounds 1–4 contain the same 5α-cholestane-3β,6β,15α,16β,26-pentahydroxysteroidal moiety and differ from each other in the fatty acid units: 5′Z,11′Z-octadecadienoic (1), 11′Z-octadecenoic (2), 5′Z,11′Z-eicosadienoic (3), and 7′Z-eicosenoic (4) acids. Previously, only one such steroid conjugate with a fatty acid was known from starfish. After 72 h of cell incubation, using MTS assay it was found that the concentrations of compounds 1, 2, and 3 that caused 50% inhibition of growth (IC₅₀) of JB6 Cl41 cells were 81, 40, and 79 µM, respectively; for MDA-MB-231 cells, IC₅₀ of compounds 1, 2, and 3 were 74, 33, and 73 µM, respectively; for HCT 116 cells, IC₅₀ of compounds 1, 2, and 3 were 73, 31, and 71 µM, respectively. Compound 4 was non-toxic against tested cell lines even in three days of treatment. Compound 2 (20 µM) suppressed colony formation and migration of MDA-MB-231 and HCT 116 cells. Full article

(This article belongs to the Special Issue Echinoderms Metabolites: Structure, Functions and Biomedical Perspectives)

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31 pages, 8647 KiB

Open AccessArticle

Inspired by Sea Urchins: Warburg Effect Mediated Selectivity of Novel Synthetic Non-Glycoside 1,4-Naphthoquinone-6S-Glucose Conjugates in Prostate Cancer

by Sergey A. Dyshlovoy, Dmitry N. Pelageev, Jessica Hauschild, Yurii E. Sabutskii, Ekaterina A. Khmelevskaya, Christoph Krisp, Moritz Kaune, Simone Venz, Ksenia L. Borisova, Tobias Busenbender, Vladimir A. Denisenko, Hartmut Schlüter, Carsten Bokemeyer, Markus Graefen, Sergey G. Polonik, Victor Ph. Anufriev and Gunhild von Amsberg

Mar. Drugs 2020, 18(5), 251; https://doi.org/10.3390/md18050251 - 11 May 2020

Cited by 24 | Viewed by 4852

Abstract

The phenomenon of high sugar consumption by tumor cells is known as Warburg effect. It results from a high glycolysis rate, used by tumors as preferred metabolic pathway even in aerobic conditions. Targeting the Warburg effect to specifically deliver sugar conjugated cytotoxic compounds into tumor cells is a promising approach to create new selective drugs. We designed, synthesized, and analyzed a library of novel 6-S-(1,4-naphthoquinone-2-yl)-d-glucose chimera molecules (SABs)—novel sugar conjugates of 1,4-naphthoquinone analogs of the sea urchin pigments spinochromes, which have previously shown anticancer properties. A sulfur linker (thioether bond) was used to prevent potential hydrolysis by human glycoside-unspecific enzymes. The synthesized compounds exhibited a Warburg effect mediated selectivity to human prostate cancer cells (including highly drug-resistant cell lines). Mitochondria were identified as a primary cellular target of SABs. The mechanism of action included mitochondria membrane permeabilization, followed by ROS upregulation and release of cytotoxic mitochondrial proteins (AIF and cytochrome C) to the cytoplasm, which led to the consequent caspase-9 and -3 activation, PARP cleavage, and apoptosis-like cell death. These results enable us to further clinically develop these compounds for effective Warburg effect targeting. Full article

(This article belongs to the Special Issue Echinoderms Metabolites: Structure, Functions and Biomedical Perspectives)

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