Ponasterone a and F, Ecdysteroids from the Arctic Bryozoan Alcyonidium Gelatinosum

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Ponasterone a and F, Ecdysteroids from the Arctic Bryozoan Alcyonidium Gelatinosum molecules Article Ponasterone A and F, Ecdysteroids from the Arctic Bryozoan Alcyonidium gelatinosum Kine Østnes Hansen 1,* ID , Johan Isaksson 2, Eirin Glomsaker 1, Jeanette Hammer Andersen 1 ID and Espen Hansen 1 ID 1 Marbio, UiT—The Arctic University of Norway, Breivika, N-9037 Tromsø, Norway; [email protected] (E.G.); [email protected] (J.H.A.); [email protected] (E.H.) 2 Department of Chemistry, UiT—The Arctic University of Norway, Breivika, N-9037 Tromsø, Norway; [email protected] * Correspondence: [email protected]; Tel.: +47-77649272 Received: 18 May 2018; Accepted: 12 June 2018; Published: 19 June 2018 Abstract: A new ecdysteroid, ponasterone F (1) and the previously reported compound ponasterone A(2) were isolated from specimens of the Arctic marine bryozoan Alcyonidium gelatinosum collected at Hopenbanken, off the coast of Edgeøya, Svalbard. The structure of 1 was elucidated, and the structure of 2 confirmed by spectroscopic methods including 1D and 2D NMR and analysis of HR-MS data. The compounds were evaluated for their ability to affect bacterial survival and cell viability, as well as their agonistic activities towards the estrogen receptors α and β. The compounds were not active in these assays. Compound 2 is an arthropod hormone controlling molting and are known to act as an allelochemical when produced by plants. Even though its structure has been previously reported, this is the first time a ponasterone has been isolated from a bryozoan. A. gelatinosum produced 1 and 2 in concentrations surpassing those expected of hormonal molecules, indicating their function as defence molecules against molting predators. This work adds to the chemical diversity reported from marine bryozoans and expanded our knowledge of the chemical modifications of the ponasterones. Keywords: marine bryozoan; Alcyonidium gelatinosum; ponasterone; ecdysteroids; marine bioprospecting; allelochemicals 1. Introduction Ecdysteriods are arthropod steroid hormones controlling molting (ecdysis), development and reproduction through interaction with the ecdysteroid receptors [1]. To date, more than 500 ecdysteroids have been characterized [2]. Compared to human steroidal hormones, ecdysteroids are more hydrophilic due to polyhydroxylation, they have C-27 to C-29 steroidal cores and different shapes due to an A/B-cis-ring conjugation [3]. Their structural variations lie in the side chains liked to C-17 of the steroidal D-ring, methylation patterns and conjugation moieties linked through the hydroxyl groups [4,5]. Ecdysteroids are also found in a wide variety of plants [6,7]. Phytoecdysteroids are often present in concentrations surpassing those expected of hormonal molecules [8], and they are widely recognized to serve as anti-feeding agents against insect herbivores [9–11]. Ecdysteroids demonstrate several beneficial effects in mammals, including promotion of wound healing, reduction in blood cholesterol and glucose levels and neuroprotective properties [12,13]. In addition, ecdysteroids have the capacity to act as anabolic agents by increasing protein synthesis in skeletal muscle [14]. Ecdysteroids are not prohibited in sports, and a large number of ecdysteroid-based preparations are freely available on the market [15]. Interestingly, this anabolic effect is not associated with the androgenic (masculinization) effects observed for human anabolic-androgenic steroids, like testosterone, as ecdysteroids show no significant binding affinity to the androgen receptor [16]. Molecules 2018, 23, 1481; doi:10.3390/molecules23061481 www.mdpi.com/journal/molecules Molecules 2018, 23, 1481 2 of 9 Molecules 2018, 23, x 2 of 9 Humans have no receptor equivalent to the ecdysteroid receptors, and the exact mechanism behind steroids, like testosterone, as ecdysteroids show no significant binding affinity to the androgen this observed effect is unknown [15]. However, it has been shown that 20-hydroxyecdysone (3), the receptor [16]. Humans have no receptor equivalent to the ecdysteroid receptors, and the exact ecdysteroid most commonly administered to humans either naturally through food or as a supplement, mechanism behind this observed effect is unknown [15]. However, it has been shown that 20- mediates its anabolic activity through interaction with the estrogen receptor β [17]. Furthermore, hydroxyecdysone (3), the ecdysteroid most commonly administered to humans either naturally ecdysteroidsthrough food appear or as toxicologicallya supplement, mediates benign, with its anabolic reported activity LD50 >through 6 g/kg interaction in mammals with [12 the]. This estrogen unique mode-of-action indicates the potential of ecdysteroids as orphan drugs to treat conditions associated receptor β [17]. Furthermore, ecdysteroids appear toxicologically benign, with reported LD50 > 6 g/kg within mammals muscle atrophy [12]. This or unique injury. mode-of-action indicates the potential of ecdysteroids as orphan drugs to treatBryozoans conditions are sessile, associated marine with invertebrates muscle atrophy found or ininjury. benthic ecosystems throughout the world [18]. BryozoansBryozoans play relevant are sessile roles, marine in nutrient invertebrates cycles, representingfound in benthic a food ecosystems source for throughout many marine the world species, including[18]. Bryozoans nudibranchs, play relevant and molting roles invertebratesin nutrient cycles, like arthropodsrepresenting and a food crustaceans source for [19 many]. Their marine lack of anspecies, adaptive includin immuneg nudibranchs, system and and sessile molting nature invertebrates has necessitated like arthropods the production and crustaceans of a wealth [19] of. Th defenseeir moleculeslack of an [ 20adaptive,21]. Due immune to the system prominent and sessile bioactivities nature ofhas these necessitated compounds, the production many have of a proven wealth toof be importantdefense molecules lead structures [20,21]. for Due pharmaceutical to the prominent development bioactivities of [22 these]. Despite compounds the fact, many that have a number proven of compoundsto be important with medicallead structures potential for havepharmaceutical been isolated development from bryozoans [22]. Despite in recent the years,fact that the a number phylum is relativelyof compounds under-investigated with medical inpotential this context. have been In our isolated previous from studies bryozoans that focusedin recent on years, marine the bryozoans,phylum a monobrominatedis relatively under tyrosine-investigated derivative in this [23context.], and In five our variants previous of studies the securamines, that focused as on well marine as their bioactivitiesbryozoans, have a mono beenbrominated reported tyrosine [24]. derivative [23], and five variants of the securamines, as well as Duringtheir bioactivities the course have ofbeen our reported investigation [24]. towards the discovery of bioactive secondary metabolitesDuring from the course Arctic of marine our investigation bryozoans, towardsAlcyonidium the discovery gelatinosum of bioactivewas extracted secondary and metabolites fractionated. from Arctic marine bryozoans, Alcyonidium gelatinosum was extracted and fractionated. Preliminary Preliminary bioactivity experiments showed that one of the fractions significantly inhibited the viability bioactivity experiments showed that one of the fractions significantly inhibited the viability of a of a human melanomae cancer cell line. Further evaluation of the chemical constituents of the organic human melanomae cancer cell line. Further evaluation of the chemical constituents of the organic extract led to the isolation of a new ponasterone, ponasterone F (1), along with ponasterone A (2) extract led to the isolation of a new ponasterone, ponasterone F (1), along with ponasterone A (2) (Figure1), which has been isolated previously from several sources, including the leaves of the (Figure 1), which has been isolated previously from several sources, including the leaves of the terrestrialterrestrial plant plantPodocarpus Podocarpus nakaiinakaii [[25]25].. As As part part of of this this study, study, the the ponasterones ponasterones were were isolated isolated from from a a bryozoanbryozoan for the firstfirst time. Herein, Herein, we we report report the the isolation, isolation, structure structure elucidation elucidation and and bioactivity bioactivity profilingprofiling of of the the two two compounds, compounds, includingincluding theirtheir estrogen receptor receptor agonistic agonistic activities. activities. Moltin Moltingg in in bryozoansbryozoans is is an an almost almost unrecognized unrecognized phenomenon.phenomenon. The The free free-living-living bryozoan bryozoan species species CupuladriaCupuladria doma doma hashas been been shown shown to to molt molt frontal frontal andand basalbasal membranes under under conditions conditions of of heavy heavy fouling fouling colonies colonies [26] [26. ]. It hasIt has also also been been described described for forAlcyonidium Alcyonidium sanguineum,, a a species species closely closely related related to to A.A. gelatinosum gelatinosum (same(same family).family). We W thereforee therefore hypothesize hypothesize the the role role ofof thethe ponasterones to to be be part part of of a achemical chemical defense defense system system forforA. A. gelatinosum gelatinosum. FigureFigure 1. 1. TheThe structures of of the the herein herein isolated isolated compounds compounds ponasterone ponasterone F (1) Fand (1) A and (2) Aand (2 )20 and-
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