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Cytotoxic Ent-Kaurane Diterpenoids from Salvia Cavaleriei

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Cytotoxic Ent-Kaurane Diterpenoids from Salvia Cavaleriei Article pubs.acs.org/jnp Cytotoxic ent-Kaurane Diterpenoids from Salvia cavaleriei † ‡ † ‡ † † † † ‡ Heng Zheng, , Qiong Chen, , Mengke Zhang, Yongji Lai, Liang Lei, Penghua Shu, Jinwen Zhang, † † § † † Yongbo Xue, Zengwei Luo, Yan Li, Guangmin Yao,*, and Yonghui Zhang*, † Hubei Key Laboratory of Natural Medicinal Chemistry and Resource Evaluation, School of Pharmacy, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, People’s Republic of China ‡ Tongji Hospital Affiliated to Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, People’s Republic of China § State Key Laboratory of Phytochemistry and Plant Resources in West China, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650204, People’s Republic of China *S Supporting Information ABSTRACT: Fifteen new ent-kaurane diterpenoids, compounds 1−15, and two known analogues, 4-epi-henryine A (16) and leukamenin E (17), were isolated from the whole plants of Salvia cavaleriei. The structures of the new compounds were established by spectroscopic methods, and their absolute configurations were determined by electronic circular dichroism and single- crystal X-ray diffraction analyses with Cu Kα radiation. Compounds 1−15 were evaluated for their cytotoxicity against five human cancer cell lines, HL-60, SMMC-7721, A-549, MCF-7, and SW480, as well as the noncancerous Beas-2B cell line. Compounds 1−10, 12, 14,and15 showed broad-spectrum cytotoxicity, with compounds 1, 3, 6−10, 12, and 15 exhibiting more potent cytotoxicity than the positive control, cis-platin, with IC50 values ranging from 0.65 to 6.4 μM. Salvia L., the largest genus of the family Lamiaceae, comprises active components. In the process, 15 new ent-kaurane over 1000 species, which are widely distributed in tropical and diterpenoids, compounds 1−15, and two known ent-kaurane temperate regions of the world,1 and some species have been diterpenoids, 4-epi-henryine A (16)14 and leukamenin E (17),15 cultivated for use as herbal medicines and ornamentals.2,3 were isolated. Here, we describe the isolation, structure Studies on the chemical constituents of Salvia revealed the elucidation, and cytotoxicity of compounds 1−15. presence of polyphenolics2 and terpenoids.3,4 The identified diterpenoids mainly belong to seven skeletal types, abietane, ■ RESULTS AND DISCUSSION clerodane, pimarane, labdane, ent-kaurane, icetexane, and 11α-Hydroxyleukamenin E (1) was obtained as colorless 3,4 apianane. Collectively, these compounds possess antibacte- needles, mp 195−197 °C. The molecular formula of 1 was rial, antileishmanial, antimicrobial, antioxidant, antispasmolytic, − assigned as C22H32O6 by the HRESIMS of the pseudomolecular 3 6 + antituberculosis, and antitumor activities. Interestingly, ion [M + Na] at m/z 415.2067 (calcd for C22H32O6Na, although ent-kaurane diterpenoids are common in plants of 415.2097), indicating seven indices of hydrogen deficiency. The the genus Isodon (Lamiaceae),7 only one ent-kaurane UV absorption maximum at 234 nm was consistent with the diterpenoid has been previously reported from the Salvia presence of an α,β-unsaturated carbonyl group. The IR − genus.8 spectrum suggested the presence of hydroxy (3394 cm 1), an − − Salvia cavaleriei Levĺ is endemic to China and is distributed in ester carbonyl (1725 cm 1), a double bond (1647 cm 1), and − the Guizhou, Sichuan, Guangdong, Guangxi, Hubei, Hunan, conjugated carbonyl (1705 cm 1) functionalities. The 1H NMR 9 δ Jiangxi, Shaanxi, and Yunnan provinces. The whole plant of S. spectrum (Table 1) showed resonances for three methyls ( H δ cavaleriei is used as a Chinese herbal medicine to treat 0.92, H3-18; 0.99, H3-19; 1.34 H3-20), an acetyl ( H 2.07), four δ β β hematemesis, metrorrhagia, dysentery with bloody stools, and oxymethines ( H 3.98, ddd, H-11 ; 4.07, dd, H-7 ; 4.62, t, H- traumatic hemorrhage.10 Previous phytochemical investigations 3α; 5.10, s, H-14α), and two olefinic protons arising from an 11 δ on S. cavaleriei var. cavaleriei and S. cavaleriei var. exocyclic double bond ( H 6.04, s, H-17a; 5.42, s, H-17b). The 13 simplicifolia12 have resulted in the isolation of depsides, C NMR and DEPT spectra (Table 4) of 1 displayed a total of δ phenolic glycosides, triterpenoids, and steroids. In our search 22 carbon resonances assignable to a ketocarbonyl ( C 209.0, 13 δ δ for anticancer agents from Chinese herbal medicines, we C-15), an acetyl ( C 172.7, 21.3), an exocyclic double bond ( C found that the 95% EtOH extract of the whole plants of S. cavaleriei showed significant cytotoxicity against the HL-60 cell Received: July 24, 2013 line, which encouraged us to pursue the characterization of the Published: November 20, 2013 © 2013 American Chemical Society and American Society of Pharmacognosy 2253 dx.doi.org/10.1021/np400600c | J. Nat. Prod. 2013, 76, 2253−2262 Journal of Natural Products Article dichroism (ECD) spectrum.17 The NOESY correlations of H- 11 to H-9β and H-12β and the large coupling constants J = δ 13.0, 8.0, and 6.0 Hz of H-11 ( H 3.98, ddd) with H-9 and H- 12 established the β-orientation of H-11. Analyses of the 2D NMR data, including HSQC, 1H−1H COSY, HMBC, and NOESY (Figure 1), defined compound 1 as 7α,11α,14β- trihydroxy-3β-acetoxy-ent-kaur-16-en-15-one. The structure was confirmed by single-crystal X-ray diffraction analysis, and its absolute confi guration was assigned as 3S,5S,7R,8R,9S,10R,11R,13S,14R based on a Flack parameter of 0.19(14)18 (Figure 2). 11β-Hydroxyleukamenin E (2) exhibited a pseudomolecular ion at m/z 415.2065 [M + Na]+ in the HRESIMS, which is in agreement with the molecular formula C22H32O6 (calcd for C22H32O6Na, 415.2097). Compound 2 has the same molecular formula as 1, and the NMR resonances for 2 (Tables 1 and 4) resemble those of 1. The obvious difference is that the multiplicity and coupling constants of H-11 are a doublet (J = 4.5 Hz) in 2 instead of a doublet of doublets of doublets (J = δ 13.0, 8.0, 6.0 Hz) in 1. Correspondingly, C-11 ( C 65.5) in 2 δ was shifted upfield compared to the corresponding signal in 1 150.2, C-16; 117.1, C-17), three methyls ( C 29.2, C-18; 22.5, δ (δ 69.5). These differences suggest that 2 is the 11-epimer of C-19; 19.3, C-20), four methylenes ( C 41.1, C-12; 36.2, C-1; C δ 1. The α-orientation of H-11 in 2 was determined by the 29.3, C-6; 24.0, C-2), four oxymethines ( C 79.2, C-3; 76.3, C- δ NOESY correlations between H-11 and both H-1α and H - 14; 76.0, C-7; 69.5, C-11), three methines ( C 61.2, C-9; 49.3, 3 δ 20α. Detailed 2D NMR analyses confirmed the identification of C-5; 47.4, C-13), and three quaternary carbons ( C 62.8, C-8; 42.6, C-10; 38.1, C-4). The 13C NMR spectrum of 1 is similar 2 as 7α,11β,14β-trihydroxy-3β-acetoxy-ent-kaur-16-en-15-one. to that of the co-occurring known compound 17 (leukamenin The absolute configuration of 2 was determined as E),15 except for a C-11 oxymethine group in 1 replacing a 3S,5S,7R,8R,9S,10R,11S,13S,14R by single-crystal X-ray diffrac- methylene in 17. Thus, 1 is the 11-OH derivative of 17. 1H−1H tion with Cu Kα radiation (Figure 3). COSY correlations from H-11 to both H-9 and H-12, together The molecular formula of 11-oxoleukamenin E (3) was with HMBC correlations of H-11 to C-8 and C-10, supported determined to be C22H30O6 by the HRESIMS ion at m/z + the above assignment. The NOESY correlations (Figure 1) of 413.1923 [M + Na] (calcd for C22H30O6Na, 413.1940). H-14/H3-20 and H-5/H-9 allowed assignment of 1 as an ent- Comparison of the NMR data of 3 (Tables 1 and 4) with those 16 δ kaurane diterpenoid, which was further supported by the of 2 indicated that a C-11 oxo ( C 206.8) group in 3 replaced ff λ δ negative Cotton e ect at max 342 nm in the electronic circular the oxymethine function in 2 ( C 65.5). This suggestion was Table 1. 1H NMR [δ, mult (J in Hz)] Data for Compounds 1−5 (400 MHz) position 1a 2a 3b 4a 5a 1α 2.52 ddd (14.0, 3.5, 3.3) 1.64 overlap 1.32 ddd (13.8, 3.3, 3.3) 2.57 ddd (14.5, 8.5, 6.6) 1.58 overlap 1β 1.37 ddd (14.0, 13.3, 3.8) 1.40 ddd (14.0, 13.5, 3.0) 1.41 ddd (13.8, 12.1, 3.0) 1.81 ddd (14.5, 10.5, 4.8) 1.24 m 2α 1.97 overlap 2.00 m 1.74 m 2.25 ddd (15.5, 8.5, 4.8) 1.90 overlap 2β 1.54 dddd (15.3, 3.4, 3.4, 3.3) 1.64 overlap 1.59 dddd (15.3, 3.3, 3.0, 3.0) 2.70 ddd (15.5, 10.5, 6.6) 1.53 overlap 3α 4.62 t (2.6) 4.66 t (2.8) 4.61 t (2.6) 3.36 t (3.5) 5β 1.47 dd (12.2, 1.5) 1.48 dd (12.5, 1.4) 1.43 dd (12.9, 1.4) 1.96 dd (13.0, 2.0) 1.49 dd (12.4, 1.9) 6α 1.70 ddd (12.8, 12.2, 12.0) 1.70 ddd (12.7, 12.5, 12.0) 1.82 ddd (12.9, 12.4, 11.9) 1.76 ddd (13.0, 12.8, 11.9) 1.84 overlap 6β 1.88 ddd (12.8, 3.9, 1.5) 1.90 ddd (12.7, 4.2, 1.4) 1.93 dd (12.4, 2.6) 1.89 ddd (12.8, 3.4, 2.0) 1.92 overlap 7β 4.07 dd (12.0, 4.0) 4.21 dd (12.0, 4.2) 4.37 dd (11.9, 4.3) 4.09 dd (11.9, 3.4) 4.22 dd (11.9, 4.6) 9β 1.69 d (8.0) 1.48 br s 1.81 br s 1.84 d (8.0) 1.75 br s 11α 3.96 d (4.5) 11β 3.98 ddd (13.0, 8.0, 6.0) 3.98 ddd (12.8, 8.0, 5.6) 12α 2.24 ddd (13.0, 12.8, 2.5) 2.22 ddd (14.7, 4.5, 3.1) 2.74 dd (16.5, 3.2) 2.16 ddd (12.8, 12.8, 1.8) 2.94 dd (16.5, 3.5) 12β 1.98 overlap 2.05 ddd (14.7, 3.8, 2.2) 2.57 br d (16.5) 1.99 ddd (12.8, 5.2, 5.6) 2.53 ddd (16.5, 3.0, 1.8) 13α 3.05 br s 2.96 br s 3.19 br s 3.06 br s 3.22 br s 14α 5.10 s 4.90 s 5.29 s 5.01 s 5.39 br s 17a 6.04 s 5.95 s 6.20 s 6.05 s 6.19 s 17b 5.42 s 5.34 s 5.53 s 5.43 s 5.61 s 18 0.92 s 0.94 s 0.87 s 1.15 s 0.99 s 19 0.99 s 0.98 s 0.91 s 1.10 s 0.91 s 20 1.34 s 1.08 s 1.11 s 1.21 s 1.17 s OAc 2.07 s 2.06 s 2.01 s a b Recorded in methanol-d4.
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