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Antiprotozoal Steroidal Saponins from the Marine Sponge Pandaros Acanthifolium

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Antiprotozoal Steroidal Saponins from the Marine Sponge Pandaros Acanthifolium Antiprotozoal steroidal saponins from the marine sponge Pandaros acanthifolium Item Type Journal Contribution Authors Regalado, E.L.; Tasdemir, D.; Kaiser, M.; Cachet, N.; Amade, P.; Thomas, O.P. Citation Journal of Natural Products, 73. p. 1404-1410 Download date 27/09/2021 02:08:16 Link to Item http://hdl.handle.net/1834/3863 Antiprotozoal Steroidal Saponins from the Marine Sponge Pandaros acanthifolium Erik L. Regalado,*,† Deniz Tasdemir,‡ Marcel Kaiser,§ Nadja Cachet,┴ Philippe Amade,┴ Olivier P. Thomas*,┴ Department of Chemistry, Center of Marine Bioproducts (CEBIMAR), Loma y 37 Alturas del Vedado, C.P. 10400 Havana, Cuba, University of London, School of Pharmacy Department of Pharmaceutical and Biological Chemistry Centre for Pharmacognosy and Phytotherapy, 29-39 Brunswick Square London WC1N 1AX, United Kingdom, Department of Medical Parasitology and Infection Biology, Swiss Tropical Institute, 4002, Basel, Switzerland and University of Nice-Sophia Antipolis, Laboratoire de Chimie des Molécules Bioactives et des Arômes UMR 6001 CNRS, Institut de Chimie de Nice, Faculté des Sciences Parc Valrose, 06108 Nice Cedex 2, France. RECEIVED DATE * To whom correspondence should be addressed. O.P.T.: [email protected]; phone +33-4- 92076134; fax: +33-4-92076599 † CEBIMAR Cuba ‡ University of London § Swiss Tropical Institute ┴ University of Nice-Sophia Antipolis IMPORTANT: This is an uncorrected proof. Please, access to the published version: http://pubs.acs.org/doi/abs/10.1021/np100348x 1 The chemical composition of the Caribbean sponge Pandaros acanthifolium was reinvestigated and led to the isolation of 12 new steroidal glycosides, namely pandarosides E–J (1–6) and their methyl esters (7–12). Their structures were determined on the basis of extensive spectroscopic analyses, including two-dimensional NMR and HRESIMS data. As the previously isolated pandarosides A–D (13–16), the new compounds 1–12 share an unusual oxidized D-ring and a cis C/D ring junction. The absolute configurations of the aglycones were assigned by interpretation of CD spectra, whereas the absolute configurations of the monosaccharide units were determined by chiral GC analyses of the acid methanolysates. The majority of the metabolites showed in vitro activity against three or four parasitic protozoa. Particularly active were the compounds 3 (pandaroside G) and its methyl ester (9), which potently inhibited the growth of Trypanosoma brucei rhodesiense (IC50 values 0.78 and 0.038 µM, respectively) and Leishmania donovani (IC50s 1.3 and 0.051 µM, respectively). 2 Tropical diseases (TDs) are a group of chronic infections affecting about 1 billion people worldwide, mainly in Africa, South America and Southeast Asia. Besides their massive negative impact on global health, TDs such as malaria, African trypanosomiasis (sleeping sickness), American trypanosomiasis (Chagas disease) and visceral leishmaniasis (kala azar) result in billions of dollars of lost productivity, an ongoing cycle of poverty and social isolation.1 Medicinal plants have provided excellent drug and drug templates for the treatment and control of parasitic diseases, especially malaria. During the last four decades marine invertebrates have been shown to produce highly active natural products with complex structural features. Despite their short history, marine natural products have found applications in therapeutic fields, particularly in cancer,2–3 however their potential in antiprotozoal drug discovery has remained largely unexplored. During our first investigation of the little-studied Caribbean marine sponge Pandaros acanthifolium (Poecilosclerida, Microcionidae) collected at the Canyon rock off the Martinique coast, steroidal saponins named pandarosides A–D (13–16), as well as their methyl esters (17–19), were identified as the major constituents of the sponge extract.4 Before that, saponins have mostly been isolated from marine sponge of the genera Asteropus and Erylus.5 This result was unexpected as the order Poecilosclerida is best known to produce a large diversity of complex bioactive guanidine alkaloids.6 The polyether acanthifolicin was the unique secondary metabolite reported from Pandaros genus to date.7 Acanthifolicin is an episulfur derivative of okadaic acid, a toxin identified as a major cause of diarrhetic shellfish poisoning. Because polyether toxins of this family were isolated from dinoflagellates a microbial origin was also assumed for acanthifolicin.8 We decided to reinvestigate the chemical composition of the extract in the search for bioactive constituents. We were not able to isolate the known acanthifolicin and we report herein the isolation of 6 new additional steroidal glycosides named pandarosides E–J (1–6) and their methyl esters (7–12) as constituents of the sponge P. acanthifolium. Their structures were elucidated by spectroscopic studies including 1D- and 2D-NMR experiments (COSY, HSQC, HMBC, and NOESY), as well as HRESIMS analyses. All of these metabolites 1–12 share a rare 2-hydroxycyclopent-2-enone D ring with a β configuration at C-14. Differences with the 3 previously isolated pandarosides A–D reside in the B and C rings, in the alkyl side chain of the aglycone moiety, as well as in the sugar residues, where for the first time in this family xylose and rhamnose were identified. Only a few saponins have been found to exhibit antiprotozoal bioactivity,9 however we decided to evaluate the potential of this new family of compounds. To this end, in vitro inhibitory activity of the new metabolites 1–12 and the previously isolated pandarosides 13, 15, 16 and their methyl esters 17, 18 and 19 were evaluated against a small panel of parasitic protozoa, i.e. Trypanosoma brucei rhodesiense (bloodstream forms), Trypanosoma cruzi (intracellular amastigotes in L6 rat skeletal myoblasts), Leishmania donovani (axenic amastigotes), and Plasmodium falciparum (blood stage forms of K1 strain resistant to chloroquine and pyrimethamine). The compounds were also tested against recombinant P. falciparum fatty acid biosynthesis enzymes (PfFabG, PfFabI, PfFabZ) in order to assess their potential in malaria prophylaxis.10,11 The selectivity of the compounds toward L6 cells (a primary cell line derived from rat skeletal myoblasts) was also assessed. Results and Discussion 4 The CH2Cl2/MeOH (1:1) extract of the Caribbean marine sponge P. acanthifolium was fractionated by RP-C18 flash chromatography and a complex polar fraction was further purified by successive semi- preparative RP-C18 HPLC and analytical C6-phenyl HPLC to yield 12 new compounds, 1–6 together with their methyl esters 7–12. Compound 1 had a molecular formula of C39H56O14 as established by the HRESIMS analysis. The bands at 3496, 1692, and 1640 cm-1 in the IR spectrum suggested the presence of hydroxy and carbonyl functions. The NMR data were closely related to the previously isolated pandarosides A–D (13–16) (Tables 1 and 2).5 5 1 Table 1. H NMR data (500 MHz, CD3OD) for Pandarosides 1–6: δ in ppm, multiplicity (J in Hz). No. 1 2 3 4 5 6 1β 1.72, m 1.73, m 1.79, m 1.68, m 1.64, m 1.68, m 1α 1.02, m 0.90, m 0.95, m 0.86, m 0.86, m 0.86, m 2α 1.90, m 1.90, m 1.85, m 1.85, m 1.85, m 1.86, m 2β 1.55, m 1.56, m 1.61, m 1.50, m 1.50, m 1.50, m 3 3.74, tt (10.5, 5.0) 3.67, m 3.49, m 3.64, tt (10.5, 5.0) 3.64, m 3.64, m 4α 1.78, m 1.78, m 2.42, m 1.70, m 1.72, m 1.72, m 4β 1.31, m 1.33, m 2.20, m 1.28, m 1.28, m 1.28, m 5 1.26, m 1.26, m 1.23, m 1.04, m 1.04, m 1.04, m 6α 1.58, m 1.58, m 2.99, m 1.35, m 1.35, m 1.35, m 6β 1.42, m 1.42, m 1.95, m 1.30, m 1.30, m 1.30, m 7α 2.67, m 2.67, m 2.17, m 2.16, m 2.17, m 5.42, dd (5.0, 2.0) 7β 1.89, m 1.90, m 1.66, m 1.66, m 1.65, m 8 1.94, m 1.94, m 1.94, m 9 2.02, dd (8.5, 5.5) 0.88, m 0.87, m 0.88, m 11β 2.00, m 2.00, m 1.43, m 1.39, m 1.38, m 1.39, m 11α 1.56, m 1.56, m 1.14, m 1.17, m 1.17, m 1.16, m 12β 1.92, m 1.93, m 1.59, m 1.55, m 1.55, m 1.55, m 12α 1.16, m 1.16, m 1.42, m 1.47, m 1.46, m 1.47, m 14 2.34, s 2.34, s 1.90, br s 1.84, d (4.5) 1.83, d (4.5) 1.85, d (4.5) 18 1.14, s 1.17, s 1.21, s 1.17, s 1.16, s 1.20, s 19 0.94, s 0.95, s 1.04, s 0.81, s 0.81, s 0.81, s 20 2.91, m 2.90, m 2.90, m 2.88, m 2.88, m 2.94, m 21 1.21, d (6.5) 1.18, d (7.0) 1.15, d (6.5) 1.15, d (7.0) 1.15, d (7.0) 1.19, d (6.5) 3.19, dd (16.5, 3.05, dd (18.0, 2.97, dd (17.5, 2.96, dd (17.5, 2.97, dd (18.0, 3.06, dd (16.5, 22a 8.5) 9.0) 9.0) 8.5) 8.5) 9.0) 3.02, dd (16.5, 2.79, dd (18.0, 2.81, dd (17.5, 2.79, dd (17.5, 2.80, dd (18.0, 2.94, dd (16.0, 22b 5.5) 4.5) 4.5) 4.5) 4.5) 4.5) 2.23, ddd (10.5, 2.23, ddd (10.0, 2.23, ddd (10.0, 24 2.34, m 7.5, 4.0) 7.5, 4.0) 7.5, 4.0) 241a 6.12, s 1.58, m 1.57, m 1.57, m 1.01, d (7.0) 5.57, q (7.0) 241b 5.80, br s 1.53, m 1.51, m 1.52, m 242 0.76, t (7.5) 0.76, t (7.5) 0.76, t (7.5) 1.67, d (7.0) 25 2.88, m 1.90, m 1.88, m 1.88, m 1.88, m 2.59, m 26/2 1.02, d (7.0) 0.88, d (6.5) 0.89, d (6.5) 0.89, d (6.5) 0.89, d (6.5) 1.02, d (6.5) 7 1.04, d (7.0) 0.85, d (7.0) 0.90, d (6.5) 0.90, d (6.5) 0.90, d (6.5) 1.03, d (6.5) 1' 4.46, d (8.0) 4.50, d (8.0) 4.45, d (7.5) 4.48, d (8.0) 4.53, d (7.5) 4.57, d (7.5) 2' 3.37, t (8.0) 3.37, d (8.0) 3.37, t (8.0) 3.37, t (8.0) 3.38, t (9.5) 3.44, dd (9.0, 8.0) 3' 3.57, t (8.5) 3.56, m 3.56, t (8.5) 3.55, t (8.5) 3.51, m 3.60, t (9.0) 4' 3.55, t (8.5) 3.57, m 3.57, t (9.0) 3.56, t (8.5) 3.49, m 3.59, t (9.0) 5' 3.76, d (8.5) 3.77, d (8.5) 3.77, d (7.0) 3.81, d (9.5) 3.77, d (8.5) 3.78, d (8.0) 1" 4.55, d (7.5) 4.53, d (7.5) 4.55, d (7.5) 4.52, d (7.5) 5.17, d (1.5) 4.57, d (8.0) 2" 3.27, t (9.0) 3.27, t (8.5) 3.26, t (8.0) 3.27, t (9.0) 3.90, dd (3.0, 1.5) 3.24, t (8.0) 3" 3.33, t (9.0) 3.33, t (8.5) 3.33, t (9.0) 3.34, t (9.0) 3.64, dd (9.5, 3.5) 3.37, t (8.5) 4" 3.51, m 3.50, m 3.50, m 3.51, m 3.38, t (9.5) 3.33, m 3.91, dd (11.5, 3.91, dd (11.5, 3.90, dd (11.5, 3.90, dd (11.5, 5"a 5.0) 5.5) 5.0) 5.0) 3.27, ddd (12.0, 4.11, tt (9.5, 6.5) 3.22, dd (11.5, 3.23, dd (11.5, 3.23, dd (11.5, 3.23, dd (11.5, 5.0, 2.5) 5"b 9.0) 9.0) 9.0) 9.0) 3.84, dd (11.5, 6"a 2.5) 1.22, d (6.5) 3.71, dd (11.5, 6"b 5.0) The 2-hydroxycyclopent-2-enone D-ring of the previously described pandarosides was present in 1 13 due to the signals at δC 58.8 (C-14), 201.0 (C-15), 151.5 (C-16) and 154.5 (C-17) in the C NMR 4 spectrum.
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