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8-Hydroxybriaranes from Octocoral Briareum Stechei (Briareidae) (Kükenthal, 1908)

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8-Hydroxybriaranes from Octocoral Briareum Stechei (Briareidae) (Kükenthal, 1908) marine drugs Article 8-Hydroxybriaranes from Octocoral Briareum stechei (Briareidae) (Kükenthal, 1908) Thanh-Hao Huynh 1,2, Su-Ying Chien 3, Junichi Tanaka 4 , Zhi-Hong Wen 1,5 , Yang-Chang Wu 6,7, Tung-Ying Wu 8,9,* and Ping-Jyun Sung 1,2,7,10,11,* 1 Department of Marine Biotechnology and Resources, National Sun Yat-sen University, Kaohsiung 804201, Taiwan; [email protected] (T.-H.H.); [email protected] (Z.-H.W.) 2 National Museum of Marine Biology and Aquarium, Pingtung 944401, Taiwan 3 Instrumentation Center, National Taiwan University, Taipei 106319, Taiwan; [email protected] 4 Department of Chemistry, Biology and Marine Science, University of the Ryukyus, Nishihara, Okinawa 9030213, Japan; [email protected] 5 Institute of BioPharmaceutical Sciences, National Sun Yat-sen University, Kaohsiung 804201, Taiwan 6 Graduate Institute of Integrated Medicine, College of Chinese Medicine, China Medical University, Taichung 404333, Taiwan; [email protected] 7 Chinese Medicine Research and Development Center, China Medical University Hospital, Taichung 404394, Taiwan 8 Department of Biological Science & Technology, Meiho University, Pingtung 912009, Taiwan 9 Department of Food Science and Nutrition, Meiho University, Pingtung 912009, Taiwan 10 Graduate Institute of Marine Biology, National Dong Hwa University, Pingtung 944401, Taiwan 11 Graduate Institute of Natural Products, Kaohsiung Medical University, Kaohsiung 807378, Taiwan * Correspondence: [email protected] (T.-Y.W.); [email protected] (P.-J.S.); Tel.: +886-8-779-9821 (ext. 8754) (T.-Y.W.); +886-8-882-5037 (P.-J.S.); Fax: +886-8-779-3281 (T.-Y.W.); +886-8-882-5087 (P.-J.S.) Abstract: Chemical investigation of the octocoral Briareum stechei, collected in the Ie Island, Okinawa, Citation: Huynh, T.-H.; Chien, S.-Y.; Japan, resulted in the isolation of a new briarane-type diterpenoid, briastecholide A (1), as well Tanaka, J.; Wen, Z.-H.; Wu, Y.-C.; Wu, as the previously reported metabolites, solenolide C (2) and briarenolide S (3). The structures of T.-Y.; Sung, P.-J. 8-Hydroxybriaranes briaranes 1–3 were characterized through spectroscopic analysis, and the absolute configuration of from Octocoral Briareum stechei 2 was corroborated by a single-crystal X-ray diffraction analysis. Briarane 3 exhibited bioactivity (Briareidae) (Kükenthal, 1908). Mar. against the protein expression of inducible nitric oxide synthase (iNOS). Drugs 2021, 19, 136. https://doi.org/ 10.3390/md19030136 Keywords: Briareum stechei; briarane; briastecholide; solenolide; anti-inflammation; iNOS Academic Editor: Vassilios Roussis Received: 9 February 2021 1. Introduction Accepted: 26 February 2021 Briareum Published: 28 February 2021 Octocorals of the genus (family Briareidae), flourishing in the tropical and subtropical Indo-Pacific Ocean, are proven to be the most important sources to yield the 3,8-cyclized cembranoids (briarane), and compounds of this type were found to possess Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in complex structures and extensive bioactivities, especially in anti-inflammatory activity [1,2]. published maps and institutional affil- Briareum stechei (Kükenthal, 1908) [3], one of the widely studied species of octocoral, iations. is considered a rich source of briarane-type compound. In continuation of our interest in the comparative chemistry of Briareum species collected at diverse geographical locations, we obtained a specimen of B. stechei from Ie Island, Okinawa, Japan [3,4]. We report herein the isolation, structure determination and antiinflammatory activity of one new (briastecholide A (1)), one revised (solenolide C (2)) [5,6] and one known (briarenolide S Copyright: © 2021 by the authors. (3)) [7] briarane (Figure1). Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Mar. Drugs 2021, 19, 136. https://doi.org/10.3390/md19030136 https://www.mdpi.com/journal/marinedrugs Mar. Drugs 2021, 19, x 2 of 8 Mar. Drugs 2021, 19, 136 EtOAc layer was collected and loaded onto a column chromatograph with silica gel,2 and of 8 separated using high performance liquid chromatography (HPLC), yielding briaranes 1– 3. Mar. Drugs 2021, 19, x 2 of 8 EtOAc layer was collected and loaded onto a column chromatograph with silica gel, and separated using high performance liquid chromatography (HPLC), yielding briaranes 1– 3. 1: R = OAc, 3: R = Cl 2 FigureFigure 1.1. StructuresStructures ofof briastecholidebriastecholide AA ((11),), solenolidesolenolide CC ((22)) andand briarenolidebriarenolide S S ( 3(3).). 2. ResultsSolenolide and Discussion C (2) was first isolated from octocoral Solenopodium sp. [5], and the stere- ochemistryFreshly of collected C-12 in B.this stechei compoundwas frozen was andrevised subsequently in a later study freeze-dried, by NMR powdered data analysis and extracted with a mixture of methanol/dichloromethane (MeOH/CH Cl ) at a 1:1 ratio [6]. The structure of 2 was determined directly in this study for the first2 time2 by a single- tocrystal produce X-ray an analysis, extract thatand the was Oak separated Ridge Thermal by ethyl Ellipsoid acetate (EtOAc)–water Plot (ORTEP) diagram partitioning. (Fig- 1: R = OAc, 3: R = Cl 2 Theure EtOAc2) showed layer wasthat collected the absolute and loaded configurations onto a column of stereogenic chromatograph carbons with silicaof 2 gel,are and1FigureR,2 separatedR,3 1.R Structures,4R,6S using,7R of,8 highRbria,9Sstecholide, performance10S,11R, 1A2 R(1,)1 liquid, 3solenolideS,14R chromatography and C 17(2)R and. Analyzing briarenolide (HPLC), the Syielding X(3-).ray structure briaranes of 12– 3confirmed. the β-orientation of the 12-hydroxy group, rather than an α-orientation, as statedSolenolideSolenolide in a previous CC ((22) )study waswas first first[5] (Supplem isolatedisolated fromfromentary octocoraloctocoral Materials, SolenopodiumSolenopodium Figures S12 sp.sp.–S16 [[5]5],)., andand thethe stere-stere- ochemistryochemistry ofof C-12C-12 in this this c compoundompound was was revised revised in in a alater later study study by by NMR NMR data data analysis anal- ysis[6]. The [6]. structure The structure of 2 was of 2 determinedwas determined directly directly in this instudy this for study the first for thetime first by timea single by- acrystal single-crystal X-ray analysis, X-ray analysis, and the Oak and theRidge Oak Thermal Ridge ThermalEllipsoid EllipsoidPlot (ORTEP) Plot (ORTEP)diagram (Fig- dia- gramure 2 (Figure) showed2) showed that the that absolute the absolute configurations configurations of ofstereogenic stereogenic carbons carbons of of 2 areare 11RR,2,2RR,3,3RR,4,4RR,6,6SS,7,7RR,8,8RR,9,9SS,10,10SS,11,11RR,12,12RR,13,1S3S,14,1R4Rand and 17 17RR. Analyzing. Analyzing the the X-ray X-ray structure structure of of2 confirmed2 confirmed the theβ-orientation β-orientation of the of 12-hydroxythe 12-hydroxy group, group, rather rather than an thanα-orientation, an α-orientation, as stated as instated a previous in a previous study [ 5study] (Supplementary [5] (Supplem Materials,entary Materials, Figures Figures S12–S16). S12–S16). Figure 2. Crystal structure and absolute configuration of solenolide C (2) by X-ray diffraction. Briastecholide A (1) was obtained as an amorphous powder. The positive mode high resolution electrospray ionization mass spectrum [(+)-HRESIMS] showed a peak at m/z 487.19356, suggesting a molecular formula C24H32O9 (calcd. for C24H32O9 + Na, 487.19385) (nine degrees of unsaturation). The IR spectrum indicated the presence of hydroxy (νmax 3462 cm–1), γ-lactone (νmax 1771 cm–1), ester carbonyl (νmax 1740 cm–1) and α,β-unsaturated FigureketonicFigure 2.2. (ν CrystalCrystalmax 1675 structurestructure cm–1) and groups.andabsolute absolute The configuration configuration13C NMR spectrum of of solenolide solenolide of 1 C C(Table ( 2(2)) by by X-ray1) X -showedray diffraction. diffraction signals. of 24 carbons. The multiplicity of carbon signals was determined from distortionless en- Briastecholide A (1) was obtained as an amorphous powder. The positive mode hancementBriastecholide by polarization A (1) was transfer obtained (DEPT) as an and amorphous heteronuclear powder. single The quantum positive modecoherence high high resolution electrospray ionization mass spectrum [(+)-HRESIMS] showed a peak (HSQC)resolution spectr electrospraya: five methyls, ionization three massmethylenes spectrum (one [(+) bearing-HRESIMS] a heteroatom), showed ninea peak methines at m/z at m/z 487.19356, suggesting a molecular formula C H O (calcd. for C H O + Na, (three487.19356 bearing, suggest a heteroatoming a molecular and three formula olefins) C24H and32O 924 seven(calcd.32 non9 for -Cprotonated24H32O9 + 24Na, carbons32 487.19385)9 (four 487.19385)(nine degrees (nine of degrees unsaturation of unsaturation).). The IR spectrum The IR spectrum indicated indicated the presence the presence of hydroxy of hydroxy (νmax ν −1 γ ν −1 ν −1 α β (34max62 cm3462–1),cm γ-lactone), -lactone (νmax 17 (71max cm1771–1), ester cm carbonyl), ester carbonyl(νmax 1740 ( cmmax–1)1740 and α,β cm-unsaturated) and , - ν −1 13 unsaturatedketonic (νmax ketonic 1675 cm ( max–1) groups.1675 cm The) groups.13C NMR The spectrumC NMR of spectrum 1 (Table of1) 1showed(Table1 )signals showed of signals24 carbons. of 24 carbons.The multiplicity The multiplicity of carbon of carbon signals signals was determined was
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