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Eunicellin-Based Diterpenoids, Hirsutalins S–V, from the Formosan Soft Coral Cladiella Hirsuta

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Eunicellin-Based Diterpenoids, Hirsutalins S–V, from the Formosan Soft Coral Cladiella Hirsuta Mar. Drugs 2015, 13, 2757-2769; doi:10.3390/md13052757 OPEN ACCESS marine drugs ISSN 1660-3397 www.mdpi.com/journal/marinedrugs Article Eunicellin-Based Diterpenoids, Hirsutalins S–V, from the Formosan Soft Coral Cladiella hirsuta Tzu-Zin Huang 1,†, Bo-Wei Chen 1,†, Chiung-Yao Huang 1, Tsong-Long Hwang 2,3, Chokkalingam Uvarani 1,4, Chang-Feng Dai 5, Ping-Jyun Sung 4,6, Jui-Hsin Su 4,6 and Jyh-Horng Sheu 1,7,8,9,10,* 1 Department of Marine Biotechnology and Resources, National Sun Yat-sen University, Kaohsiung 804, Taiwan; E-Mails: [email protected] (T.-Z.H.); [email protected] (B.-W.C.); [email protected] (C.-Y.H.); [email protected] (C.U.) 2 Graduate Institute of Natural Products, School of Traditional Chinese Medicine, College of Medicine, and Chinese Herbal Medicine Research Team, Healthy Aging Research Center, Chang Gung University, Taoyuan 333, Taiwan; E-Mail: [email protected] 3 Department of Cosmetic Science and Research Center for Industry of Human Ecology, Chang Gung University of Science and Technology, Taoyuan 333, Taiwan 4 National Museum of Marine Biology and Aquarium, Pingtung 944, Taiwan; E-Mails: [email protected] (P.-J.S.); [email protected] (J.-H.S.) 5 Institute of Oceanography, National Taiwan University, Taipei 112, Taiwan; E-Mail: [email protected] 6 Department of Life Science and Institute of Biotechnology and Graduate Institute of Marine Biotechnology, National Dong Hwa University, Pingtung 944, Taiwan 7 Frontier Center for Ocean Science and Technology, National Sun Yat-sen University, Kaohsiung 804, Taiwan 8 Graduate Institute of Natural Products, Kaohsiung Medical University, Kaohsiung 807, Taiwan 9 Department of Medical Research, China Medical University Hospital, China Medical University, Taichung 404, Taiwan 10 Doctoral Degree Program in Marine Biotechnology, National Sun Yat-sen University and Academia Sinica, Kaohsiung 804, Taiwan † These authors contributed equally to this work. * Author to whom correspondence should be addressed; E-Mail: [email protected]; Tel.: +886-7-525-2000 (ext. 5030); Fax: +886-7-525-5020. Academic Editor: Vassilios Roussis Mar. Drugs 2015, 13 2758 Received: 24 March 2015 / Accepted: 20 April 2015 / Published: 30 April 2015 Abstract: Four new eunicellin-type hirsutalins S–V (1–4), along with a known compound (–)-6α-hydroxy polyanthellin A (5), were isolated from the soft coral Cladiella hirsuta. The structures of the metabolites were determined by extensive spectroscopic analysis. Cytotoxity of compounds 1–5 against the proliferation of a limited panel of cancer cell lines was measured. Anti-inflammatory activity of compounds 1–5 was evaluated by measuring their ability in suppressing superoxide anion generation and elastase release in fMLP/ CB-induced human neutrophils. Keywords: soft coral; Cladiella hirsuta; eunicellins; cytotoxic activity; anti-inflammatory activity 1. Introduction The chemical investigations on soft corals of the genus Cladiella and Klyxum [1–32] have afforded series of eunicellin-based diterpenoids, of which many have been shown to exhibit attracting biological activities [8,10–32]. We have previously isolated some bioactive eunicellins and steroids from a Taiwanese soft coral Cladiella hirsuta. Our recent studies of C. hirsuta have led to the discovery of 18 eunicellin-based diterpenoids, hirsutalins A–R [29–31], some of which have been found to possess cytotoxic [29,31] and anti-inflammatory activities [29–31]. In this paper, we further report the isolation of four new eunicellin-based compounds, hirsutalins S–V along with a known compound (–)-6α-hydroxy polyanthellin A (5) [32] from C. hirsuta (Chart 1). The structures of new compounds were determined by extensive spectroscopic analysis. Cytotoxicity of 1–5 against a limited panel of cancer cell lines and their anti-inflammatory activity, determined by their ability to inhibit the generation of superoxide anion and elastase release in N-formyl-methionyl-leucyl-phenylalanine/ cytochalasin B (fMLP/CB)-induced human neutrophils, were studied in order to discover bioactive compounds from marine environment. 16 17 H H H 7 H OH 12 9 6 1 O O 14 O 3 O H HH H HH O 1 2 20 18 15 19 O 1 OH O OH O 1 O 1 1 12O O O Chart 1. Cont. Mar. Drugs 2015, 13 2759 OH AcO H H H H H H OH OH OH O O O O O O H HH O 1 H HH HH 2 OH O 1 2 O O 1 34OH O 5 S 1 O O Chart 1. Structures of metabolites 1–5. 2. Results and Discussion Hirsutalin S (1) was isolated as a colorless oil. The HRESIMS (m/z 485.2512) of 1 established a molecular formula of C26H38O7. The IR spectrum of 1 showed the presence of hydroxy and carbonyl groups from absorptions at 3463 and 1740 cm−1, respectively. The 1H and 13C NMR data of 1 (Table 1) were found to be closely resembled to those of known metabolite hirsutalin R [32]. The only difference was the presence of 2-acetoxybutanoate (δC 169.0 (C), 73.9 (CH), 24.5 (CH2), and 9.7 (CH3); 171.0 (C) and 20.6 (CH3)) in 1, instead of 2-butyryloxy butanoate at C-3 of hirsutalin R [32]. This was supported by the HMBC interaction of H-2′′ (δ 2.16) with carbonyl carbon resonating at δ 171.0. Moreover, the 13C NMR spectroscopic data (Table 1) of 1 showed the presence of two 1,1-disubstituted carbon-carbon double bonds (δC 147.6 (C) and 118.3 (CH2); 145.2 (C) and 111.6 (CH2)). The molecular framework of 1 was established by the complete analysis of its COSY and HMBC correlations (Figure 1). In the NOESY spectrum of 1, the correlations between H-10 with H-1; H-1 with H3-19, suggested that H-1, H-10 and H3-19 are β-oriented. Besides, correlations of H-2 with H3-15 and H-14; H-9 with H-14, suggested that H-2, H-9, H-14 and H3-15 are α-oriented. Furthermore, the asymmetric center at C-18 was suggested to be R-configured on the basis of NOE correlations between the β-oriented H-1 and H3-19 and between the α-oriented H-2 and H-18. As the absolute configuration of hirsutalin A [29] and that of hirsutalin J except C-2′ configuration [30] have been completely assigned based on Mosher’s method, thus, the absolute configuration of 1, except that of C-2′, should be revealed as depicted. Mar. Drugs 2015, 13 2760 Table 1. NMR spectroscopic data for hirsutalins S (1) and T (2). 1 2 a,b c b,d e Position δC δH (J in Hz) δC δH (J in Hz) 1 45.1, CH b 2.24, m 39.8; 39.7,f CH 2.69, m 2 90.7, CH 3.70, s 87.64; 87.61, CH 3.86, d (6.0) 3 86.0, C 74.3, C 4 32.4, CH2 2.13, m; 74.2, CH 5.08, dd (8.5, 3.5) 5 37.2, CH2 2.84, t (10.4); 2.35, m 37.9; 37.8, CH2 2.90, dq (15.5, 5.0); 1.78, m 6 206.5, C 72.6, CH 4.23, br s 7 147.6, C 147.7, C 8 37.2, CH2 3.22, dd (13.2, 5.2); 2.40, m 40.1, CH2 2.42, m; 2.34, m 9 78.3, CH 4.07, m 81.80; 81.76, CH 4.15, m 10 48.7, CH 3.07, dd (9.6, 7.6) 44.5, CH 2.69, m 11 145.2, C 132.1; 132.0, C 12 31.1, CH2 2.30, m; 2.11, m 122.02; 121.97, CH 5.46, s 13 25.8, CH2 1.68, m; 1.13, m 22.8; 22.8, CH2 2.09, m; 1.91, m 14 37.3, CH 1.68, m 34.4; 34.3, CH 1.84, m 15 22.7, CH3 1.48, s 22.6, CH3 1.38, s 16 118.3, CH2 5.62, s; 5.27, s 115.9; 115.8, CH2 5.62, s; 5.24, s 17 111.6, CH2 4.85, s; 4.72, s 22.3; 22.2, CH3 1.70, s 18 36.4, CH 1.79, m 33.8; 33.7, CH 1.84, m 19 16.3, CH3 1.03, d (7.2) 14.5; 14.3, CH3 0.86, d (6.5) 20 66.4, CH2 3.52, d (7.2) 67.8; 67.6, CH2 4.11, dd (9.5, 4.0); 3.89, m 1′ 169.0, C 171.4;171.2, C 2′ 73.9, CH 4.76, t (6.8) 74.1, CH 4.84, dd (13.0, 6.0) 3′ 24.5, CH2 1.87, m 24.4; 24.3, CH2 1.90, m 4′ 9.7, CH3 1.03, t (7.6) 9.4; 9.3, CH3 1.03, t (7.5) 1′′ 171.0, C 171.1; 171.0, C 2′′ 20.6, CH3 2.16, s 20.9; 20.5, CH3 2.13, s; 2.02, s 20-OCOPr 173.9; 173.7, C 36.2; 35.7, CH2 2.27, m; 18.5; 18.3, CH2 1.64, m; 13.7; 13.6, CH3 0.96, t (7.5); 0.94, t (7.5) a b c Spectra recorded at 100 MHz in CDCl3; Attached protons were deduced by DEPT experiments; Spectra recorded at d e f 400 MHz in CDCl3; Spectra recorded at 125 MHz in CDCl3; Spectra recorded at 500 MHz in CDCl3; Paired signals due to C-2′ epimeric mixture.
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