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Publicly Available Published by De Gruyter January 28, 2016

Salaterpene E, a eudesmane-type sesquiterpene from Salacia longipes var. camerunensis

  • Brice Mittérant Mba’ning EMAIL logo , Bruno Lenta Ndjakou EMAIL logo , Ferdinand Mouafo Talontsi , Alain Meli Lannang , Birger Dittrich , Silvère Augustin Ngouela , Etienne Tsamo , Norbert Sewald and Hartmut Laatsch

Abstract

A mixture of two compounds with potent antiplasmodial activity in vitro against the W2 strain of Plasmodium falciparum (half maximal inhibitory concentration, 1.12 μg/mL) was obtained in a previous investigation of the CH2Cl2-MeOH extract of the seeds of Salacia longipes var. camerunensis. Separation by column chromatography led now to the isolation of salaterpene E (1) and (1R,2R,4S,5S,6R,7R,9S,10R)-2-acetoxy-1,6,9-tribenzoyloxy-4-hydroxy-dihydro-β-agarofuran (2). The structure of 1 was elucidated by spectroscopic analysis, and its absolute configuration was established unambiguously by means of single-crystal X-ray diffraction. Also the absolute configurations of the recently described salaterpenes A (2a) and D (2b) were determined by this method using the anomalous scattering of the oxygen atoms only.

1 Introduction

The Salacia genus (family Celastraceae) is widespread in almost all tropical rainforests and comprises about 180–200 species, including 29 in America, 90 in Africa (50 in Cameroon, 3 in Senegal, 48 in Ivory Coast, 54 in the Democratic Republic of Congo, and 13 in Mozambique), 2 in Madagascar, 14 in Indochina, and 29 in Malaysia. The Cameroon-Gabon forests, with more than 60 species, appear to be the richest region of Salacia in the world [1]. This genus is also widely distributed in India, Sri Lanka, China, and other Southeast Asian countries [2].

Salacia longipes Oliv. is a woody climbing shrub, of which three varieties have been distinguished: S. longipes itself, S. longipes var. camerunensis Loes., and S. longipes var. longipetiolata Loes. S. longipes var. camerunensis is a liana of about 10–15 m in height and 3–4 cm in diameter, compared to S. longipes, which only grows to about 4–6 m in height. This species is widely distributed in Cameroon [1].

Plants from the genus Salacia are used in traditional medicine as anti-inflammatory, antioxidant, analgesic, carminative, thermogenic, stomachic, and depurative agents and as liver/blood tonics and analgesics [3–5]. They are used in the treatment of malaria, rheumatism, pruritus, asthma, fever, menorrhagia, diabetes, hemorrhoids, inflammation, leucorrhea, leprosy, skin diseases, amenorrhea, dysmenorrhea, wounds, ulcers, hyperhydrosis, hepatopathy, dyspepsia, flatulence, colic, and spermatorrhea [2, 3, 5–7].

Salacia species are known to contain anthocyanidins, catechins, phenolic acids, quinones, triterpenoids, gutta-percha, xanthones, stilbenes, eudesmane-type sesquiterpenes, and megastigmane glycosides [3, 5, 8, 9]. The xanthone mangiferin is the major constituent of almost all Salacia species and has been proven to possess significant antidiabetic, antihypertensive, and hypolipidemic properties [10, 11]. Therefore, the roots of Salacia species have been extensively consumed in the USA, Japan, and other countries as food supplement for the prevention of diabetes and obesity [2]. Many of the medicinal properties associated with these Celastraceae species have been attributed to a large family of highly oxygenated sesquiterpenoids, based on the dihydroagarofuran skeleton, which are chemotaxonomic markers for the family.

Previously, we isolated and characterized one new triterpene from the roots [12] and four new sesquiterpenes from the seeds [13] of S. longipes var. camerunensis. In a continuing search for bioactive compounds from this plant, we have investigated a mixture of two compounds that exhibited a good antiplasmodial activity against the Plasmodium falciparum W2 strain in vitro with a half maximal inhibitory concentration (IC50) of 1.12 μg/mL. Extensive chromatographic purification of this mixture afforded a new sesquiterpene (1) together with the known (1R,2R,4S,5S,6R,7R,9S,10R)-2-acetoxy-1,6,9-tribenzoyloxy-4-hydroxy-dihydro-β-agarofuran (2) [13, 14]. We report herein the structure analysis of 1 together with its X-ray diffraction results and those of the previously reported salaterpenes A (2a) and D (2b).

2 Results and discussion

The separation of a mixture obtained from the investigation of the seeds of S. longipes var. camerunensis, which showed potent antiplasmodial activity, yielded salaterpene E (1) and (1R,2R,4S,5S,6R,7R,9S,10R)-2-acetoxy-1,6, 9-tribenzoyloxy-4-hydroxy-dihydro-β-agarofuran (2), see Fig. 1.

Fig. 1: Chemical structures of salaterpenes E (1), A (2a), D (2b), and compound 2.
Fig. 1:

Chemical structures of salaterpenes E (1), A (2a), D (2b), and compound 2.

Compound 1 was obtained as colorless crystals: m.p. 190–191 °C, [α]D20=+69 (c = 0.5; CHCl3). Its molecular formula, C31H34O9, was determined from NMR data and its positive ESI HR mass spectrum, which showed a quasi-molecular ion peak [M+Na]+ at m/z = 573.20957 (calcd. 573.20950 for C31H34O9Na). UV absorptions at 245, 275, and 343 nm suggested the presence of aromatic moieties. The IR spectrum showed absorption bands for hydroxyl (3513 cm−1) and carbonyl (1745 and 1712 cm−1) groups.

The 1H NMR spectrum (Table 1) of compound 1 showed four methyl and one acetyl singlets (H-2″′) and signals of two methylene groups. Four methine groups (of which three were oxygenated), one hydroxyl group at δ = 3.52 ppm, and two A2MX2 spin systems characteristic for two benzoyl groups were further observed.

Table 1

1H (500 MHz) and 13C NMR data (125 MHz) of salaterpene E (1) in CDCl3.

NoδCδH (m, J in Hz)
177.05.91 (s)
2201.0
355.12.63 (d, 12.5), 3.16 (d, 12.5)
474.7
591.2
680.45.74 (br s)
748.92.50 (br t, 3.6)
832.22.37 (brdd, 3.6, 16.4), 2.67 (ddd, 3.6, 7.3, 16.4)
972.95.19 (br d, 7.3)
1053.1
1185.6
1229.71.66 (s)
1325.81.64 (s)
1424.91.38 (s)
1520.61.37 (s)
1′166.0
2′129.0
3′,7′130.18.23 (dd, 1.2, 7.7)
4′,6′128.77.51 (t, 7.7)
5′133.77.63 (br t, 7.7)
1″165.1
2″129.5
3″,7″129.78.06 (dd, 1.2, 7.7)
4″,6″128.67.48 (t, 7.7)
5″133.67.61 (br t, 7.7)
1″′169.3
2″′20.01.76 (s)

The 13C NMR spectrum (Table 1) of compound 1 showed signals of 31 carbon atoms that were classified by distortionless enhancement by polarization transfer (DEPT) and heteronuclear single quantum correlation (HSQC) spectra as 10 quaternary carbons including 4 carbonyl groups, 14 methines, 2 methylenes, and 5 methyl groups. All these data indicated that 1 was a penta-substituted sesquiterpene with a dihydro-β-agarofuran skeleton [15].

The positions of the acetate and benzoate groups were determined from HMBC experiments, where correlations were observed between the proton H-1 and the acetate carbonyl. In a similar way, the protons H-6 and H-9 correlated with the benzoate carbonyls at δ = 166.0 and 165.1 ppm, respectively.

The relative stereochemistry of compound 1 has been established from a careful study of coupling constants in the 1H NMR spectrum, which showed an equatorial/axial relationship between H-9 and Hax-8 (δ = 2.67 ppm, J8ax,9 = 7.3 Hz). This was confirmed by X-ray structure determination, which also delivered the absolute structure (Fig. 2; see also Experimental Section). Consequently, compound 1 was assigned as 1α-acetoxy-6β,9β-dibenzoyloxy-4β-hydroxy- 2-oxo-dihydro-β-agarofuran and named salaterpene E.

Fig. 2: Key HMBC correlations and Ortep view of the molecular structure of 1 in the crystal.
Fig. 2:

Key HMBC correlations and Ortep view of the molecular structure of 1 in the crystal.

In the course of this investigation, we were also able to determine the absolute configurations of salaterpene A (2a, C35H40O12) and salaterpene D (2b, C37H39NO10) by single-crystal X-ray diffraction and to confirm our previous results (Fig. 3) [13] (see Experimental Section).

Fig. 3: Ortep representations of the molecular structures of salaterpenes A (2a) (left) and D (2b) (right) in the crystal. Displacement parameters are shown at a probability level of 50 %.
Fig. 3:

Ortep representations of the molecular structures of salaterpenes A (2a) (left) and D (2b) (right) in the crystal. Displacement parameters are shown at a probability level of 50 %.

The structures of dihydro-β-agarofuransesquiterpenes isolated from plants vary strongly, although the substituents encountered in most of the molecules described in the literature are the same. Gao et al. [16] reported a total of 462 dihydro-β-agarofuransesquiterpenoids of 74 structural types isolated from about 64 species of Celastraceae, three species of Hippocrateaceae, and one species of Lamiaceae from January 1990 to June 2006. About 13 papers on this group of compounds have been published on Celastraceae species [13, 17–30], describing about 84 new compounds in the past 8 years. Dihydro-β-agarofurans are unusually highly oxygenated sesquiterpenoids with the 5,11-epoxy-5β,10α-eudesman-4-(14)-ene skeleton (Fig. 4) bearing up to nine ester groups. Beside hydroxyl and carbonyl groups, the esterifying moieties are mostly acetic, benzoic, cinnamic, nicotinic, 2-methylbutyric, and furoic acid, and in some cases also substituted nicotinic acid (Fig. 4). These compounds exhibited a broad range of biological activities including antifungal, antitumoral, antimalarial, insecticidal, antifeedant, anticancer, antituberculosis, cytotoxic, anticarcinogenic, antiviral, immunosuppressive, anti-HIV, and antimicrobial activities [13, 17–30].

Fig. 4: General scaffold of dihydro-β-agarofurans with commonly occurring substituents.
Fig. 4:

General scaffold of dihydro-β-agarofurans with commonly occurring substituents.

The results obtained in this study, in addition to those of the previous investigations of members of the Celastraceae family, highlight the occurrence of dihydro-β-agarofuran sesquiterpenes in this family of plants.

3 Experimental section

3.1 General experimental procedures

Melting points were determined on a ThermoFisher Scientific Digital M.P., serial IA 9000 melting point apparatus. Optical rotations were measured on a JASCO P-2000 spectropolarimeter. UV spectra were recorded on a Cary 300 spectrophotometer. IR spectra were recorded on a JASCO Fourier Transform IR spectrometer. 1H and 13C NMR spectra were recorded on a Bruker Advance spectrometer operating at 500 MHz (1H) and 125 MHz (13C), respectively, with TMS as internal standard. HR-ESIMS were recorded on a SCA Pharma Stbg QToF. Silica gel 230–400 mesh (Merck) and silica gel 70–230 mesh (Merck) were used for flash and column chromatography, whereas precoated aluminum silica gel 60 F254 sheets were used for TLC with different mixtures of n-hexane-ethyl acetate and dichloromethane-methanol as eluents. Spots were visualized with UV light (254 and 365 nm) or using MeOH-H2SO4 reagent.

3.1.1 Plant material

Salacia longipes var. camerunensis was collected in December 2008 at Mount Kala (Yaoundé) in the Centre Region of Cameroon and identified by Nana Victor, a botanist at the National Herbarium. A voucher specimen has been deposited there with the registration number 28963/SRF/Cam.

3.1.2 Extraction and purification

The seeds of S. longipes var. camerunensis (1.5 kg), separated from the fruit pericarp, were pulverized and extracted at room temperature with a mixture of CH2Cl2-MeOH (1:1), (2 × 2 L, 48 h each) [13]. The solvent was removed under reduced pressure to afford 139.2 g of extract [13]. The ground pericarp (1 kg) was extracted at room temperature with a mixture of CH2Cl2-MeOH (1:1) (2 × 1 L, 24 h each) [13]. The solvent was removed under reduced pressure to yield 45.2 g of extract [13]. These two extracts were screened for their antiplasmodial activity in vitro [13]. The extract from the seeds showed moderate antiplasmodial activity (IC50 of 2.28 μg/mL), whereas that from the pericarp showed no significant activity [13].

The seed extract (137.1 g) was chromatographed on silica gel using mixtures of n-hexane-ethyl acetate of increasing polarity as eluent. Seventy fractions of 400 mL each were collected and combined on the basis of TLC analysis to yield five main fractions labeled A (28.0 g), B (20.5 g), C (32.0 g), D (22.4 g), and E (30.0 g) [13]. Fractions A (28.0 g) and B (20.5 g) were complex mixtures of glycerol esters that were not further investigated [13]. Fraction C (32.0 g) was subjected to column chromatography over silica gel (70–230 mesh). Elution with n-hexane-ethyl acetate gradient mixtures resulted in 290 fractions of 100 mL each, which were combined on the basis of TLC analysis [13]. Further purification of sub-fractions 75–90 afforded salaterpene B (18.1 mg) [13] and (1R,2R,4S,5S,6R,7R,9S-10R)-2-acetoxy-1,6,9-tribenzoyloxy-4-hydroxy-dihydro-β-agarofuran (2, 30.4 mg) [13, 14]. Sub-fractions 119–127 yielded salaterpene C (17.5 mg) [13]. Chromatography of sub-fractions 153–175 afforded salaterpene A (2a, 40.1 mg) [13] and sub-fractions 253–259 afforded 1α,6β-diacetoxy-8β,9β-dibenzoyloxy-4β-hydroxy-2-oxo-dihydro-β-agarofuran (15.7 mg) [13, 31]. Purification of fraction D (22.4 g) with n-hexane-ethyl acetate (80:20 to 30:70) as eluent yielded salaterpene D (2b, 35.2 mg) [13].

Purification of sub-fractions 91–118 from the study of fraction C yielded a mixture of 1 and 2 (20.1 mg). A sub-sample of this mixture (5 mg) was crystallized from a CH2Cl2-n-hexane mixture and a crystal of 1 (Fig. 2) was collected at room temperature for X-ray diffraction. The mother liquor was further subjected to column chromatography over silica gel (35–70 mesh). Elution with n-hexane-ethyl acetate (9:1) yielded 1 (2.4 mg).

3.1.3 Salaterpene E [1α-acetoxy-6β,9β-dibenzoyloxy- 4β-hydroxy-2-oxo-dihydro-β-agarofuran] (1)

Colorless crystals: m.p. 190–191 °C. [α]D20=+69 (c = 0.5; CHCl3). – UV/Vis (CH2Cl2): λmax (log ε) = 245 (4.12), 275 (3.73), 343 (3.23) nm. – IR (KBr) νmax = 3513 (OH), 1712, 1745 cm−1. – 1H NMR (500 MHz) and 13C NMR (125 MHz) in CDCl3 (see Table 1). – HRMS ((+)-ESI): m/z = 1123.43083 (calcd. 1123.42979 for C62H68O18Na, [2M+Na]+), 573.20957 (calcd. 573.20950 for C31H34O9Na, [M+Na]+), 533.21768 (calcd. 533.21699 for C31H33O8, [M+H–H2O]+).

3.1.4 X-ray structure determinations

X-ray data for 1, salaterpene A (2a), and salaterpene D (2b) (Table 2) were measured with CuKα radiation (λ = 1.54178 Å, rotating anode) on a Bruker SMART 6000 diffractometer with a nitrogen gas-stream cooling device at a temperature of 100 K; data reduction was carried out with Bruker programs Saint [32] and Sadabs [33]. The structures were solved by Direct Methods with the program Shelxt [34].

Table 2

Crystal structure data for 1, 2a, and 2b.

12a2b
FormulaC31H34O9C35H40O12C37H39NO10
Mr550.58659.13657.69
Crystal size, mm30.05 × 0.07 × 0.090.17 × 0.18 × 0.230.14 × 0.22 × 0.37
Crystal systemMonoclinicMonoclinicOrthorhombic
Space groupP21 (No. 4)P21 (No. 4)P212121 (No. 19)
a, Å7.1828 (2)15.8248 (5)6.7870 (3)
b, Å9.1310 (2)28.2680 (9)17.4613 (7)
c, Å20.2366 (5)7.9828 (3)28.4742 (11)
β, deg91.798 (1)90.0129 (19)90
V, Å31442.94 (6)3571.0 (2)3374.5 (2)
Z244
Dcalcd, g/cm31.2671.2261.295
μ(CuKα), cm−10.7690.7690.778
F(000), e58413991392
hkl range–8:9, –11:11, –25:24–16:18, –33:33, –9:9–8:8, –20:20, –34:34
((sinθ)/λ)max, Å−10.62060.60260.5997
Reflections measured29 83252 08857 015
Reflections unique548412 5256072
Rint0.0240.0420.034
Parameters refined395882472
R1(F)/wR2(F2)a, b (all refl.)0.0157/0.04720.0349/0.08690.0240/0.0412
x (Flack)0.00 (5)0.03 (6)0.08 (3)
GoF (F2)c1.02331.0503.128
Δρfin (max/min), e/Å30.11/–0.090.22/–0.190.27/–0.14

aR1 = Σ||Fo| – |Fc||/Σ|Fo|. bwR2 = [Σw(Fo2Fc2)2w(Fo2)2]1/2 and w = [σ2(Fo2)+(AP)2+BP]−1, where P = (Max(Fo2, 0)+2Fc2)/3 and A and B are constants adjusted by the program. cGoF = S = [Σw(Fo2Fc2)2/(nobsnparam)]1/2, where nobs is the number of data and nparam is the number of refined parameters.

Compound 1 (Fig. 2) crystallizes in space group P21, compound 2b (Fig. 3) in space group P212121. After initial least-squares refinement with Shelxl [35], we performed an invariom refinement [36] with the Xd program [37] on both compounds, which led to a considerable improvement in the figures of merit and reduced parameter standard deviations by taking into account the aspherical valence electron density in the scattering factor model. For structure 2b, minor disorder of the pyridine ring became apparent after invariom refinement. As treating the disorder in the independent atom model was unstable and did not improve the figures of merit, it was not taken into account in the final model. Both structures were determined with R1 factors of 0.0191 for 1 and 0.0235 for 2b, and both absolute structures were determined [38]; Flack parameters were 0.00(5) for 1 and 0.08(3) for 2b, respectively. For further crystallographic data, see Table 2.

Compound 2a (Fig. 3) crystallizes in the monoclinic space group P21 and was refined with Shelxl13 using anisotropic displacement parameters for non-hydrogen atoms by full-matrix least-squares methods [38]. Owing to merohedral twinning, apparent higher metric orthorhombic symmetry was found for 2a. The structure could not, however, be solved in space group P21212 that is suggested by Xprep, and the correct space group for the molecule is indeed P21. Intensity statistics (mean |E2–1| = 0.625) confirmed the twinning. The twin law is 1̅ 0 0, 0 1̅ 0, 0 0 1, and the structure 2a was refined as a two-component twin. Application of this twin law reduced R1(F) from 0.171 to 0.035. There is a comparatively large volume of 200–300 Å3 of the unit cell containing disordered solvent. As recommended by the Platon [39] CHECKCIF routine, this volume was filled with a highly restrained hexane solvent molecule with a site occupancy of 18 %. Remarkably, even the absolute structure of 2a could, despite the twinning and the disordered solvent, be determined reliably from the anomalous signal present in the data: Parsons’ quotient method [39], as implemented in Shelxl13, gave a value of –0.03(6) for the enantiomorph-distinguishing parameter. Thus, the absolute configuration of the chiral centers in 1, 2a, and 2b were successfully determined using the anomalous signal of the oxygen atoms. The crystal data and numbers pertinent to data collection and structure refinement are summarized in Table 2.

CCDC 965221 (1), 988230 (2a), and 1039879 (2b) contain the supplementary crystallographic data for this paper. These data can be obtained free of charge from The Cambridge Crystallographic Data Centre viawww.ccdc.cam.ac.uk/data_request/cif. The complete CIF files can be downloaded as Supporting Information (see below).

3.1.5 Antiplasmodial activity assay

The antiplasmodial activity of the mixture of 1 and 2 was determined as previously described [13]. The antiplasmodial activity of 1 alone was not evaluated owing to its small amount.

4 Supporting information

Complete crystallographic CIF files including the structure factors for 1, 2a, and 2b as well as pictures of the mass spectrum and various NMR spectra of 1 are given as Supporting Information available online (DOI 10.1515/znb-2015-0106).


Corresponding authors: Brice Mittérant Mba’ning, Department of Organic Chemistry, University of Yaoundé 1, P.O. Box 812, Yaoundé, Cameroon, e-mail: ; Bruno Lenta Ndjakou, Department of Chemistry, Higher Teacher Training College, University of Yaoundé 1, P.O. Box 47, Yaoundé, Cameroon, e-mail:

Acknowledgments

B.M. Mba’ning thanks the German Academic Exchange Service for a short-term grant in 2010 (A/10/90133). B. Dittrich thanks the Deutsche Forschungsgemeinschaft (grant DI921/6-1) for support. The authors also wish to acknowledge the Alexander von Humboldt Foundation for awarding a fellowship to Bruno N. Lenta at Bielefeld University.

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Supplemental Material

The online version of this article (DOI: 10.1515/znb-2015-0106) offers supplementary material, available to authorized users.


Received: 2015-6-25
Accepted: 2015-9-10
Published Online: 2016-1-28
Published in Print: 2016-2-1

©2016 by De Gruyter

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