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Germacrane Sesquiterpenoids with an Unusual Δ3-15,6-Lactone Moiety

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Germacrane Sesquiterpenoids with an Unusual Δ3-15,6-Lactone Moiety Phytochemistry 96 (2013) 378–388 Contents lists available at ScienceDirect Phytochemistry journal homepage: www.elsevier.com/locate/phytochem Scapiformolactones A–I: Germacrane sesquiterpenoids with an unusual D3-15,6-lactone moiety from Salvia scapiformis Yongji Lai a,1, Yongbo Xue a,1, Mengke Zhang a, Jinwen Zhang b, Wei Tang c, Junjun Liu a, Liang Lei a, ⇑ ⇑ Juming Yan d, Zengwei Luo a, Jianping Zuo c, Yan Li d, Guangmin Yao a, , Yonghui Zhang a, a Hubei Key Laboratory of Natural Medicinal Chemistry and Resource Evaluation, School of Pharmacy, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, PR China b Tongji Hospital Affiliated to Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, PR China c State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai 201203, PR China d State Key Laboratory of Phytochemistry and Plant Resources in West China, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650204, PR China article info abstract Article history: Nine germacrane sesquiterpenoids with an unusual D3-15,6-lactone moiety, scapiformolactones A–I(1– Received 9 November 2012 9), and one known seco-germacrane sesquiterpenoid, 3,7,11-trimethyldodeca-l,6,9-triene-3,11-diol (10), Received in revised form 17 May 2013 were isolated from whole plants of Salvia scapiformis Hance. Their structures were elucidated by spectro- Available online 1 November 2013 scopic methods including HR-ESIMS, IR, UV, NMR, and CD, as well as by quantum mechanical calculations and chemical transformations. Structures of compounds 1–3 were also confirmed by single-crystal X-ray Keywords: diffraction analysis. Six germacrane 6,15-diol derivatives (11–16) were obtained by chemical transforma- Salvia scapiformis tion. Compounds 1–9 and 11–16 were evaluated for their in vitro immunomodulatory effects on T and B Lamiaceae cells, as well as their in vitro cytotoxicity against five human cancer cell lines, HL-60, SMMC-7721, A-549, Germacrane sesquiterpene Conformation MCF-7, and SW480. Chemical transformation Ó 2013 Elsevier Ltd. All rights reserved. Quantum mechanical calculation Cytotoxicity Immunomodulatory activity 1. Introduction Salvia species, S. palaefolia (González et al., 1989), S. glutinosa (Rus- taiyan et al., 1992), S. roborowskii (Li et al., 2003; Liu et al., 2009), S. Salvia is one of the largest genera of the family Lamiaceae (for- nubicola (Ali et al., 2007), S. castanea (Xu et al., 2005, 2008), S. chin- merly Labiatae). It comprises of over 1000 species and is distrib- ensis (Wang et al., 2008), and S. trijuga (Pan et al., 2010). uted throughout tropical and temperate zones of the world; Salvia scapiformis Hance is widely distributed in Fujian, Guang- there are 84 species in China (Li and Ian, 1994). More than 1000 dong, Guangxi, Guizhou, Hunan, Jiangxi, Zhejiang, Taiwan, and as bioactive natural products including sesquiterpenoids, diterpe- well as the Philippines (Li and Ian, 1994). Whole plants of S. scap- noids, sesterterpenoids, steroids, triterpenoids, and phenolic com- iformis, known as a folk medicine ‘‘Bai-Bu-Yao’’ in China, are used pounds have also been isolated from 134 Salvia species (Wu et al., to treat cough, hemoptysis, traumatic injuries, traumatic hemor- 2012). Germacrane-type sesquiterpenoids are quite rare in Salvia rhage, dysentery, and furunculosis (Fang and Liao, 2006). However, species, however, although they are the most abundant among there have been no phytochemical investigations reported on any all known sesquiterpenoids. To date, there have been 24 germacra- part of this plant. In the course of searching for bioactive natural ne sesquiterpenoids reported belonging to four structural subtypes products from Chinese folk medicines, nine new germacrane ses- of germacrane sesquiterpenes (Li et al., 2003; Pan et al., 2010; quiterpenoids with an unusual D3-15,6-lactone moiety, scapifor- Wang et al., 2008; Xu et al., 2008), germacrane furanosesquiterpe- molactones A–I(1–9)(Fig. 1), and one known seco-germacrane noids (Li et al., 2003; González et al., 1989; Rustaiyan et al., 1992; sesquiterpene, 3,7,1l-trimethyldodeca-l,6,9-triene-3,ll-diol (10) Xu et al., 2005, 2008), 12,6-germacranolides (Liu et al., 2009), and (Grande et al., 1992), were isolated from the acetone extract of 12,8-germacranolides (Ali et al., 2007; Xu et al., 2008) from seven the whole plants of S. scapiformis. Their structures were deter- mined by means of spectroscopic methods including HR-ESIMS, ⇑ Corresponding authors. Tel.: +86 27 83692311; fax: +86 27 83691325. IR, UV, NMR, CD, and single-crystal X-ray diffraction analysis, as E-mail addresses: [email protected] (G. Yao), [email protected] well as by quantum mechanical calculations and chemical trans- (Y. Zhang). 1 These authors contribute equally to this work. formation. The known seco-germacrane sesquiterpene 10 was 0031-9422/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.phytochem.2013.10.003 Y. Lai et al. / Phytochemistry 96 (2013) 378–388 379 (Table 1) showed resonances of five methyl doublets at dH 0.92 (J = 5.9 Hz), 1.10 (J = 7.0 Hz), 1.12 (J = 5.9 Hz), 1.17 (J = 6.9 Hz), and 1.22 (J = 6.4 Hz), one methyl singlet of acetyl group at dH 1.98, one vinyl triplet at dH 6.95 (t, 4.4), and three oxygen-bearing methine protons at dH 5.05 (dd, J = 9.0, 1.6 Hz), 5.29 (m), and 5.41 (d, J = 7.7 Hz). The 13C NMR (Table 3) and DEPT spectrum displayed six methyls, three methylenes, eight methines (one olefinic and three oxygenated), and five quaternary carbons (one olefinic, three ester carbonyls, and one ketone carbonyl). One double bond, three ester carbonyls, and one ketone carbonyl account for five degrees of unsaturation, with the remaining two degrees of unsaturation suggesting existence of two rings in 1. The gross structure of 1 was deduced from extensive analyses of the 2D NMR spectroscopic data, including 1H–1H COSY, HSQC, and HMBC data (Fig. 2). Analysis of the 1H–1H COSY and HSQC spectra Fig. 1. Chemical structures of compounds 1–16. suggested the existence of three partial structures: (I) C-2/C-3, (II) C-5/C-6(O)/C-7[C-11(C-12)/C-13]/C-8(O)/C-9/C-10/C-14, and (III) 0 0 0 0 isolated from the Salvia genus for the first time. Six new germacra- C-5 /C-2 /C-3 /C-4 . HMBC correlations of H-2 (dH 3.34, 3.68), H-9 ne derivatives with a 6,15-diol moiety 11–16 were obtained by (dH 1.55, 2.22), H-10 (dH 2.74), and Me-14 (dH 1.17) with C-1 (dC chemical transformation. In this paper, the isolation, structural elu- 209.4), and of H-2 (dH 3.34, 3.68), H-5 (dH 2.95, 3.02), and H-6 cidation, and in vitro immunomodulatory effects on murine T and B (dH 5.05) with C-4 (dC 132.5) suggested that fragments I and II were cells, as well as in vitro cytotoxicity against five human cancer cell connected by C-1 and C-4, and further established the ten-mem- lines, HL-60, SMMC-7721, A-549, MCF-7, and SW480, of com- bered ring of the germacrane skeleton. The connection of partial pounds 1–9 and 11–16, are reported. structures II to III through an ester carbonyl C-10 was deduced by 0 0 HMBC correlations of H-8 (dH 5.41), H-2 (dH 2.76), and Me-5 (dH 0 1.10) with C-1 (dC 173.2). Moreover, HMBC correlations of H-3 2. Results and discussion (dH 6.95), H-5(dH 2.95, 3.20), and H-6 (dH 5.05) with an ester car- bonyl C-15 (dC 171.3) moiety suggested that the lactone ring is lo- 0 Compound 1 was obtained as colorless crystals, m.p. 130.0– cated between C-6 (dC 77.0) and C-15. Correlations of H-3 (dH 5.29) 00 00 131.0 °C. Its molecular formula was deduced as C22H32O7 from and acetyl CH3-2 (dH 1.98) with acetyl carbonyl C-1 (dC 170.4) in (+)-HRESIMS at m/z 409.2199 [M+H]+ (calcd 409.2226), inferring the HMBC spectrum implied that the O-acetyl group was attached seven degrees of unsaturation. In the UV spectrum, an absorption to C-30. maximum at 229 nm suggests the presence of an a,b-unsaturated The relative configuration of compound 1 was determined by ester carbonyl. The IR spectrum showed the presence of an unsat- NOESY analysis (Fig. 2). Assuming H-10 to be b-oriented, the À1 À1 urated lactone (1766 cm ), and ketone carbonyl (1715 cm ), and NOESY correlation of H-10 (dH 2.74) and H-8 (dH 5.41) indicated double bonds (1680 cmÀ1) functionalities. The 1H NMR spectrum that H-8 was b-oriented; furthermore, correspondingly, the Table 1 1H NMR spectroscopic data of compounds 1–5a (400 MHz). Position 1b 2b 3b 4ab 4bb 5ac 5bc 1 4.15 (m) 4.08 (m) 3.65 (m) 3.62 (m)d 2b 3.34 (dd, 16.7, 5.4) 3.28 (dd, 16.7, 5.6) 3.32 (ddd, 16.6, 5.7, 2.69 (m) 2.82 (m)d 2.49 (m) 2.55 (m)d 1.5) 2a 3.68 (dd, 16.7, 11.3) 3.67 (dd, 16.7, 11.3) 3.67 (dd, 16.6, 11.3) 2.88 (m)d 2.82 (m) 2.61 (m) 2.71 (m)d 3 6.95 (t, 4.4) 6.87 (m) 6.97 (m) 6.75 (dt, 13.3, 6.66 (ddd, 11.2, 5.7, 6.85 (dt, 12.8, 6.71 (ddd, 12.2, 4.8, 3.1) 2.0) 3.0) 2.1) 5b 2.95 (dd, 15.5, 9.0) 2.92 (dd, 15.7, 9.0) 2.94 (dd, 15.7, 9.0) 2.80 (m)d 2.97 (dd, 14.5, 6.9) 2.75 (m)d 2.85 (m)d 5a 3.20 (d, 15.5) 3.20 (d, 15.7) 3.20 (d, 15.7) 3.18 (d, 15.5) 3.69 (d, 14.5) 2.85 (d, 15.4) 3.24 (d, 14.5) 6 5.05 (dd, 9.0, 1.6) 5.03 (dd, 9.0, 3.1) 5.06 (dd, 9.0, 3.2) 4.95 (dd, 9.0, 4.88 (dd, 8.8, 7.2) 4.84 (dd, 8.8, 4.63 (dd, 8.9, 7.0) 3.2) 3.7) 7 1.84 (m) 1.99 (m) 1.90 (dd, 3.2, 10.2) 1.75 (m) 1.81 (dd, 8.8, 3.5) 1.62 (m) 1.64 (m) 8 5.41 (d, 7.7) 5.45 (d, 8.0) 5.46 (d, 7.9) 5.24 (d, 8.2) 5.50 (dd, 11.3, 7.5) 4.89 (d, 8.0) 5.18 (t, 8.6) 9b 1.55 (ddd, 16.6, 7.7, 1.61 (ddd, 16.5, 8.0, 1.56 (ddd, 4.4, 7.9, 1.49 (m) 2.02 (m) 1.39 (m) 1.60 (m)d
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