New 9-Hydroxybriarane Diterpenoids from a Gorgonian Coral Briareum Sp

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New 9-Hydroxybriarane Diterpenoids from a Gorgonian Coral Briareum Sp International Journal of Molecular Sciences Article New 9-Hydroxybriarane Diterpenoids from a Gorgonian Coral Briareum sp. (Briareidae) Yin-Di Su 1,2,†, Chun-Sung Sung 3,4,†, Zhi-Hong Wen 1,5, Yu-Hsin Chen 2,6, Yu-Chia Chang 2,5, Jih-Jung Chen 7, Lee-Shing Fang 8, Yang-Chang Wu 9,10,11,12,*, Jyh-Horng Sheu 1,5,* and Ping-Jyun Sung 1,2,10,12,13,* Received: 30 November 2015; Accepted: 5 January 2016; Published: 9 January 2016 Academic Editor: Vassilios Roussis 1 Department of Marine Biotechnology & Resources and Asia-Pacific Ocean Research Center, National Sun Yat-sen University, Kaohsiung 804, Taiwan; [email protected] (Y.-D.S.); [email protected] (Z.-H.W.) 2 National Museum of Marine Biology & Aquarium, Pingtung 944, Taiwan; [email protected] (Y.-H.C.); [email protected] (Y.-C.C.) 3 Department of Anesthesiology, Taipei Veterans General Hospital, Taipei 112, Taiwan; [email protected] 4 School of Medicine, National Yang-Ming University, Taipei 112, Taiwan 5 Doctoral Degree Program of Marine Biotechnology, National Sun Yat-sen University & Academia Sinica, Kaohsiung 804, Taiwan 6 Department of Life Science and Institute of Biotechnology, National Dong Hwa University, Hualien 974, Taiwan 7 Department of Pharmacy & Graduate Institute of Pharmaceutical Technology, Tajen University, Pingtung 907, Taiwan; [email protected] 8 Department of Sport, Health and Leisure, Cheng Shiu University, Kaohsiung 833, Taiwan; [email protected] 9 School of Pharmacy, College of Pharmacy, China Medical University, Taichung 404, Taiwan 10 Chinese Medicine Research and Development Center, China Medical University Hospital, Taichung 404, Taiwan 11 Center for Molecular Medicine, China Medical University Hospital, Taichung 404, Taiwan 12 Graduate Institute of Natural Products, Kaohsiung Medical University, Kaohsiung 807, Taiwan 13 Graduate Institute of Marine Biology, National Dong Hwa University, Pingtung 944, Taiwan * Correspondence: [email protected] (Y.-C.W.); [email protected] (J.-H.S.); [email protected] (P.-J.S.); Tel.: +886-4-2205-7513 (Y.-C.W.); +886-7-5252-000 (ext. 5030) (J.-H.S.); +886-8-882-5037 (P.-J.S.); Fax: +886-4-2206-0248 (Y.-C.W.); +886-7-5255-020 (J.-H.S.); +886-8-882-5087 (P.-J.S.) † These authors contributed equally to this work. Abstract: Six new 9-hydroxybriarane diterpenoids, briarenolides ZI–ZVI (1–6), were isolated from a gorgonian coral Briareum sp. The structures of briaranes 1–6 were elucidated by spectroscopic methods and by comparison of their spectroscopic data with those of related analogues. Briarenolides ZII (2) and ZVI (6) were found to significantly inhibit the expression of the pro-inflammatory inducible nitric oxide synthase (iNOS) protein of lipopolysaccharide (LPS)-stimulated RAW264.7 macrophage cells. Keywords: Briareum; briarenolide; briarane; gorgonian; anti-inflammatory; iNOS 1. Introduction The briarane-type diterpenoid (3,8-cyclized cembranoid), 2β-acetoxy-2-(debutyryloxy)-stecholide E, was first isolated from the gorgonian coral Briareum sp. in 1996 [1]. Since then, hundreds of compounds of this type have been obtained from various Taiwanese gorgonian corals, such as Briareum, Junceella and Ellisella spp. [2–6], that have been located off the coast of Taiwan. Recently, in a sample collected at the southern tip of Taiwan, as Briareum sp. (family Briareidae), we identified six new Int. J. Mol. Sci. 2016, 17, 79; doi:10.3390/ijms17010079 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2016, 17, 79 2 of 13 Int. J. Mol. Sci. 2016, 17, 79 2 of 13 Recently, in a sample collected at the southern tip of Taiwan, as Briareum sp. (family Briareidae), we identified six new briaranes, briarenolides ZI–ZVI (1–6) (Figure 1). In this report, we isolate and briaranes,determine briarenolides the structures ZI–ZVI of (1these–6) (Figure briaranes,1). In in this addition report, weto isolatestudying and their determine anti-inflammatory the structures of theseproperties. briaranes, in addition to studying their anti-inflammatory properties. OAc OH OAc OAc R AcO AcO AcO 15 3 4 2 16 14 5 13 1 O 12 10 6 11 7 Cl CH (CH ) CO HO H 9 3 2 2 H H 8 O O HO 20 O O O O O HO 17 R HO 19 18 O O O 1 2: R = OH, 7: R = OAc 3: R = OH, 8: R = H OAc R1 AcO 4: R1 = OH, R2 = α-H, R3 = α-OC(O)(CH2)2CH3 5: R1 = H, R2 = β-OH, R3 = α-OH 6: R1 = OAc, R2 = α-H, R3 = β-OH R 3 H 9: R1 = H, R2 = β-OH, R3 = α-OC(O)(CH2)2CH3 R2 O O 10: R1 = H, R2 = α-H, R3 = β-OH HO O FigureFigure 1. The 1. structuresThe structures of briarenolidesof briarenolides ZI–ZVI ZI–ZVI ( 1–(16–),6), excavatolide excavatolide F ((77),), 22ββ-acetoxy-2--acetoxy-2- (debutyryloxy)-stecholideE(debutyryloxy)-stecholide E (8), ( excavatolide8), excavatolide Z (9 Z) and (9) andexcavatolide excavatolide E (10 E). (10). 2. Results2. Results and and Discussion Discussion The molecular formula of a new briarane, briarenolide ZI (1), was determined as C24H33ClO11 The molecular formula of a new briarane, briarenolide ZI (1), was determined as C24H33ClO11 (eight(eight degrees degrees of unsaturation) of unsaturation) by high-resolution by high-resol electrosprayution electrospray ionization ionization mass spectrum mass (HRESIMS)spectrum (HRESIMS) at m/z 555.16025 (calcd. for C24H33ClO11 + Na, 555.16036). The IR of 1 showed absorptions at m/z 555.16025 (calcd. for C24H33ClO11 + Na, 555.16036). The IR of 1 showed absorptions at 1715, at 1715, 1769 and 3382 cm−1, which were consistent with the presence of ester, γ-lactone and hydroxy 1769 and 3382 cm´1, which were consistent with the presence of ester, γ-lactone and hydroxy groups. groups. The 13C NMR spectrum (Table 1) suggested that 1 possessed an exocyclic carbon-carbon The 13C NMR spectrum (Table1) suggested that 1 possessed an exocyclic carbon-carbon double bond 1 double bond based on signals at δC 138.6 (C-5) and 116.9 (CH2-16), which was confirmed1 by the H based on signals at δC 138.6 (C-5) and 116.9 (CH2-16), which was confirmed by the H NMR spectrum NMR spectrum of 1 (Table 1), which showed two olefin proton signals at δH 5.88 (1H, dd, J = 2.4, of 1 (Table1), which showed two olefin proton signals at δH 5.88 (1H, dd, J = 2.4, 1.2 Hz, H-16a) and 1.2 Hz, H-16a) and 5.64 (1H, dd, J = 2.4, 1.2 Hz, H-16b). Three carbonyl resonances at δC 175.3 (C-19), δ 5.64173.4 (1H, and dd, 169.3J = 2.4, (2 × 1.2ester Hz, carbonyl H-16b).s) revealed Three carbonyl the presence resonances of one γ at-lactoneC 175.3 and (C-19), two ester 173.4 groups and in 169.3 1; (2ˆ ester carbonyls) revealed the presence of one γ-lactone and two ester groups in 1; two acetyl two acetyl methyls (δH 2.06, s, 2 × 3H) were also observed. According to the overall unsaturation methylsdata, it (δ wasH 2.06, concluded s, 2 ˆ 3H) that were 1 was also a diterpenoid observed. molecule According possessing to the overall four rings. unsaturation data, it was concluded1H thatNMR1 wascoupling a diterpenoid information molecule in the possessing1H–1H correlation four rings. spectroscopy (COSY) spectrum of 1 1 1 1 enabledH NMR identification coupling informationof the H-2/H in2-3, the H-6/H-7,H– H H-12/H correlation2-13/H-14, spectroscopy H-6/H2-16 (COSY) (by allylic spectrum coupling) of 1 enabledand H-17/H identification3-18 units of (Table the H-2/H 1). The2-3, heteronuclear H-6/H-7, H-12/H mult2iple-13/H-14, bond coherence H-6/H2-16 (HMBC) (by allylic correlations coupling) andbetween H-17/H protons3-18 units and (Table quaternary1). The carbons heteronuclear of 1 (H-2, multiple H2-3, H-10, bond H2 coherence-13, H3-15/C-1; (HMBC) H-2, H correlations2-3, H2-16, betweenOH-4/C-4; protons H-16b, and OH-4/C-5; quaternary H-10, carbons H3-18, of OH-9/C-8;1 (H-2, H2 -3,H3-20/C-11 H-10, H 2and-13, H-17, H3-15/C-1; H3-18/C-19) H-2, Hpermitted2-3, H2-16, OH-4/C-4;elucidation H-16b, of the OH-4/C-5; carbon skeleton H-10, H 3(Table-18, OH-9/C-8; 1). HMBC H 3correlations-20/C-11 and between H-17, HH32-18/C-19)-16/C-4, -5 permitted and -6 elucidationindicated ofanthe exocyclic carbon double skeleton bond (Table at C-5,1). wh HMBCich was correlations further confirmed between by H the2-16/C-4, allylic coupling -5 and -6 indicatedbetween an H exocyclic2-16/H-6. HMBC double correlations bond at C-5, between which H3 was-15/C-1, further -2, -10 confirmed and -14 and by H-2 the and allylic H-10/C-15, coupling revealed that the ring junction C-15 methyl group was located at C-1. Furthermore, an HMBC between H2-16/H-6. HMBC correlations between H3-15/C-1, -2, -10 and -14 and H-2 and H-10/C-15, revealedcorrelation that between the ring H-2 junction (δH 5.09) C-15 and methyl the acetate group carbonyl was located (δC 173.4) at C-1. revealed Furthermore, the presence an HMBCof an acetate ester at C-2; and an HMBC correlation between a hydroxy proton (δH 6.50) and C-4 correlation between H-2 (δH 5.09) and the acetate carbonyl (δC 173.4) revealed the presence of an oxygenated quaternary carbon suggested the presence of a hydroxy group at C-4.
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