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A New Anti-HIV Ent-Kaurane Diterpene from Pteris Henryi

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A New Anti-HIV Ent-Kaurane Diterpene from Pteris Henryi Article Henrin A: A New Anti-HIV Ent-Kaurane Diterpene from Pteris henryi Wan-Fei Li 1,†, Juan Wang 2,3,†, Jing-Jie Zhang 1, Xun Song 2, Chuen-Fai Ku 2, Juan Zou 1, Ji-Xin Li 1, Li-Jun Rong 4, Lu-Tai Pan 1,* and Hong-Jie Zhang 2,* Received: 17 September 2015; Accepted: 13 November 2015; Published: 24 November 2015 Academic Editor: Ge Zhang 1 Guiyang College of Traditional Chinese Medicine, Guiyang 550002, China; [email protected] (W.-F.L.); [email protected] (J.-J.Z.); [email protected] (J.Z.); [email protected] (J.-X.L.) 2 School of Chinese Medicine, Hong Kong Baptist University, 7 Baptist University Road, Kowloon Tong, Kowloon, Hong Kong, China; [email protected] (J.W.); [email protected] (X.S.); [email protected] (C.-F.K.) 3 School of Public Health, Jilin University, Changchun 130021, China 4 Department of Microbiology and Immunology, College of Medicine, University of Illinois at Chicago, 833 South Wood Street, Chicago, IL 60612, USA; [email protected] * Correspondences: [email protected] (L.-T.P.); [email protected] (H.-J.Z.); Tel./Fax: +86-852-8823-3016 (L.-T.P.); Tel.: +852-3411-2956 (H.-J.Z.); Fax: +852-3411-2461 (H.-J.Z.) † These authors contributed equally to this work. Abstract: Henrin A (1), a new ent-kaurane diterpene, was isolated from the leaves of Pteris henryi. The chemical structure was elucidated by analysis of the spectroscopic data including one-dimensional (1D) and two-dimensional (2D) NMR spectra, and was further confirmed by X-ray crystallographic analysis. The compound was evaluated for its biological activities against a panel of cancer cell lines, dental bacterial biofilm formation, and HIV. It displayed anti-HIV potential with an IC50 value of 9.1 µM (SI = 12.2). Keywords: Pteris henryi; ent-kaurane diterpene; henrin A; bioactivity evaluation; anti-HIV activity 1. Introduction Ent-kaurane compounds are members of a class of diterpenes with a four-membered ring system, which are richly found in the Isodon genus (Lamiaceae) [1–3]. They have been known for having a variety of biological activities, including anticancer and antibacterial activities [4–6]. Tetracyclic ent-kauranes have also been found in the fern plants of the genus Pteris (Pteridaceae family), and some of them have demonstrated biological activities [7–13]. Phytochemical and biological investigation of the plants in the genus Pteris may produce potentially novel bioactive diterpenes [14,15]. The genus Pteris comprises more than 300 species, 66 of which are distributed in China [16]. Few phytochemical studies have been reported for the chemical constituents of the plants in this genus [17]. Our present study focused on the plant species P. henryi Chirst, a perennial herb that has been used as an herbal medicine for the treatment of burns and scalds, lyssodexis, traumatic hemorrhages, leucorrhea, and difficulty and pain in micturition [18]. The plant is mainly distributed in the Guizhou and Yunnan provinces, People’s Republic of China [19]. In this study, we report the isolation, structural determination, and biological activity evaluation of henrin A (1), a new ent-kaurane diterpene (Figure1). Int. J. Mol. Sci. 2015, 16, 27978–27987; doi:10.3390/ijms161126071 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2015, 16, 27978–27987 Int. J. Mol. Sci. 2015, 16, page–page OH 12 OH 20 11 13 HO 9 14 16 1 17 2 10 H 8 3 5 7 15 4 6 H 18 19 Figure 1. Structure of compound henrin A (1). 2. Results Results and and Discussion Discussion 2.1. Compound IdentificationIdentification The dried leaves of P. henryi were extracted with MeOH to affordafford a MeOH extract, which was separated through silica gelgel chromatographychromatography toto yieldyield henrinhenrin AA ((11).). Henrin A (1) was obtained as colorless crystals with UV (MeOH) λmax (log ") at 204 (1.60) nm (Figure S1). In the IR spectrum,Table 1. 1H and1 showed 13C NMR absorption data of compound of hydroxyl 1 a. groups (3386, 1099, and 1049 cm´1) (Figure S2). Its molecular formula was determined to be C H O by means of analyzing No. δH (mult, J in Hz) b δC (mult) c No. δH (mult,20 J in34 Hz)3 b δC (mult) c its NMR1α spectroscopic 2.15 (brddd, data 12.0, (Table 3.8,1 1.9)), and further50.3 t verified11α by the1.65 HR-EIMS (overlap) data with20.7m/z t 345.2405 + [M + Na]1β (calcd 345.2400)0.67 (brt, (Figure11.7) S3). The- molecule11β of 1 has1.82 four(overlap) double-bond equivalences.- 1 However,2α no carbonyl3.87 (brtt, absorption 11.5, 4.3) was observed65.4 d in the12 IRα spectrum.1.68 (overlap) As evidenced from34.6 thet H and 13 C NMR3α spectral 1.72 data(brddd, (Table 12.5,1) (Figures4.3, 1.9) S4–S6)51.9 as t well as12β the HMQC1.64 (overlap) correlation data (Figure- S7), the δ 20 carbons3β of compound1.07 (brt,1 were12.0) characterized- as four13 methyl groups- ( H 0.87, 0.93,1.09,77.4 s and 1.18 δ δ (each 3H,4 s); C 19.4 (q), 21.3- (q), 22.8 (q), and35.7 34.2s (q)),14α an oxy-methine1.66 (overlap) group ( H44.03.87 t (1H, brtt, δ δ J = 11.5,5 4.3β Hz); 0.82C 65.4 (brd, (d)), 11.5) two oxy-tertiary57.0 d carbons 14β ( C 77.41.83 (s) (d, and 11.9) 81.1 (s)), eight- methylene δ carbons,6 twoα non-oxygenated1.34 (brqd, 12.1, methine 1.9) carbons21.2 (t H 0.8215α (1H, 1.50 brd, (dd,J = 14.5, 11.5 1.3) Hz), and56.7 0.96 t (1H, brd, δ J = 7.2 Hz);6β C 57.01.59 (d) (brd, and 57.112.3) (d)), and three- quaternary15β carbons.1.63 (d, No 14.7) signals were- observed in δ 1 δ 13 the range7α of H 5–71.60 ppm (overlap) of the H NMR spectrum43.2 t and16 in the range- of C 90–160 ppm81.1 sof the C NMR spectrum,7β 1.44 indicating (brtd, 11.9, that 3.4) there is no carbon-carbon- 17 double-bond1.18 (s) in 1. The21.3 lack q of olefinic signals in8 the molecule and- the calculation of42.2 four s double-bond18 equivalences0.93 (s) determined34.2 q that 1 has a tetracyclic-ring9β system.0.96 (brd, Compound 7.2) 1 was57.1 thus d suggested 19 to have0.87 a saturated (s) tetracyclic22.8 q diterpene having an10ent -kaurane skeleton.- 41.9 s 20 1.09 (s) 19.4 q Through analysis of the long-range correlation data observed in the HMBC (heteronuclear a Data were recorded in CD3OD; δ values are given in ppm with reference to the signal of CD3OD multiple-bond correlation spectroscopy) spectrum (Figure S8), together with the HMQC (δ 3.31 ppm) for 1H and to the center peak of the signal of CD3OD (δ 49.0 ppm) for 13C; b Multiplicities 1 1 (heteronuclearin parentheses multiple-quantum represent: s (singlet correlation), brs (broad spectroscopy) singlet), dd (doublet (Figure of S7) doublet), and H– brddH (broad COSY doublet (correlated spectroscopy)of doublet), (Figure brtd (broad S9) datatriplet (Figure of doublet),2), the brqd three (broad oxy-carbon quartet of groupsdoublet), (one ddd oxy-methine(doublet of doublet and two oxy-tertiaryof doublet), carbons) brddd (broad in 1 could doublet be of assigned doublet of accordingly. doublet), t (triplet), Starting brt (broad from triplet), the singlet and brtt signals (broad of the 13 methyltriplet protons of triplet); at C-18 c Multiplicities and C-19 represent: (δH 0.93 s (H (quaternary3-18), 0.87 carbon), (H3-19)), d (CH), the t (CHC NMR2), and atq (CHδC 351.9). (t) was assigned to C-3 due to the presence of its HMBC correlations to the two methyl protons, which in 1 1 turnHenrin suggested A ( the1) was oxy-methine obtained as group colorless at C-2 crystals due to with the presenceUV (MeOH) of the λmaxH– (logH ε COSY) at 204 correlations (1.60) nm between(Figure S1). H-2 (InδH the3.87) IR and spectrum, H2-3 (δH 11.07 showed and1.72). absorption The presence of hydrox of theyl HMBCgroups correlations(3386, 1099, of and the singlet1049 cm signals−1) (Figure of the S2). methyl Its molecular protons atformula C-17 (δ wasH 1.18) determined to both oxy-tertiary to be C20H34 carbonsO3 by means at δC 77.4of analyzing and 81.1 suggestedits NMR spectroscopic that both C-13 data and (Table C-16 were1), and subsitituted further verified with a hydroxyby the HR-EIMS group, respectively. data with m/z 345.2405 [M +In Na] the+ ROESY(calcd 345.2400) (rotating frame(Figure nuclear S3). The Overhauser molecule effectof 1 spectroscopy)has four double-bond spectrum equivalences. (Figure S10), theHowever, presence no ofcarbonyl the ROE absorption (rotating was frame observed Overhauser in the effect) IR spectrum. correlations As evidenced (Figure3) offrom H-2 the ( δ H1H3.87) and with13C NMR H2-20 spectral suggested data the(Table hydroxy 1) (Figures group S4–S6) of C-2 as to well be β as-oriented. the HMQC In addition,correlation the data presence (Figure of S7), the ROEthe 20 correlations carbons of ofcompound H-5 (δH 0.82)1 were to characterized H3-18 and the as lack four of methyl ROE cross-peaks groups (δH of 0.87, H-5 0.93,1.09, to H-2 and and H 31.18-19 suggested(each 3H, s); H-5 δC to19.4 be (q),β-oriented.
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