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New Cytotoxic Seco-Type Triterpene and Labdane-Type Diterpenes from Nuxia Oppositifolia

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New Cytotoxic Seco-Type Triterpene and Labdane-Type Diterpenes from Nuxia Oppositifolia molecules Article New Cytotoxic Seco-Type Triterpene and Labdane-Type Diterpenes from Nuxia oppositifolia Shaza M. Al-Massarani 1, Ali A. El-Gamal 1,2,*, Mohammad K. Parvez 1, Mohammed S. Al-Dosari 1, Mansour S. Al-Said 1, Maged S. Abdel-Kader 3,4 and Omer A. Basudan 1 1 Department of Pharmacognosy, College of Pharmacy, King Saud University, Riyadh 11451, Saudi Arabia; [email protected] (S.M.A.-M.); [email protected] (M.K.P.); [email protected] (M.S.A.-D.); [email protected] (M.S.A.-S.); [email protected] (O.A.B.) 2 Department of Pharmacognosy, Faculty of Pharmacy, Mansoura University, El-Mansoura 35516, Egypt 3 Department of Pharmacognosy, College of Pharmacy, Prince Sattam bin Abdulaziz University, Al-kharj 11942, Saudi Arabia; [email protected] 4 Department of Pharmacognosy, College of Pharmacy, Alexandria University, Alexandria 21215, Egypt * Correspondence: [email protected]; Tel.: +966-569-780-176 Academic Editor: Isabel C. F. R. Ferreira Received: 26 January 2017; Accepted: 27 February 2017; Published: 2 March 2017 Abstract: Chromatographic purification of the n-hexane and dichloromethane extracts of Nuxia oppositifolia aerial parts, growing in Saudi Arabia, resulted in the isolation and characterization of three new labdane-type diterpene acids, 2β-acetoxy-labda-7-en-15-oic acid (1), 2β-acetoxy-7- oxolabda-8-en-15-oic acid (2), 2β-acetoxy-6-oxolabda-7-en-15-oic acid (3), and one new seco-triterpene, 3,4-seco olean-12-en-3,30 dioic acid (4), together with 10 known lupane, oleanane and ursane-type triterpenes, as well as the common phytosterols, β-sitosterol and stigmasterol (5–16). Their structures have been assigned on the basis of different spectroscopic techniques including 1D and 2D NMR. Moreover, 13 of the isolated compounds were tested on the human cancer cell lines HeLa (cervical), A549 (lung) and MDA (breast), and most of the compounds showed potent cytotoxic activities in vitro. Keywords: Nuxia oppositifolia; labdane-type diterpene; seco-triterpene; triterpenes; cytotoxicity 1. Introduction The genus Nuxia (family Buddlejaceae) comprises ca. 40 species of shrubs and trees distributed over the southern region of the Arabian peninsula, tropical Africa (Madagascar, Comoro and the Mascarene Islands) and South Africa [1]. Nuxia is represented in Saudi Arabia by only two species, viz. N. oppositifolia Benth and N. congesta Fresen, with limited distribution in the southwestern parts of the Hijaz area [2,3]. Several Nuxia species are plants of economic and medicinal interest with a rich diversity of ethnobotanical uses. Some species are used for the treatment of urine albumin, venereal disease, and as purgatives [4]. Leaves of N. sphaerocephala Baker are used in the traditional medicine of Madagascar to treat malarial splenomegaly and infantile hydrocephalus [5]. The dichloromethane leaf extract of N. verticillata, endemic to the Mascarene Archipelago, had potential anti-proliferative activity and selectively inhibited cancer cell growth in comparison with normal cells [4]. Some of the Nuxia plants have been studied phytochemically, revealing the presence of phenylpropanoid glycosides such as verbascoside [6], in addition to clerodane and labdane diterpenoids, and pentacyclic triterpenes [5]. Recently, various studies have shown pentacyclic triterpenes as valuable candidates to treat cancer by several modes of action [7]. Reviewing literature revealed that few phytochemical and biological Molecules 2017, 22, 389; doi:10.3390/molecules22030389 www.mdpi.com/journal/molecules Molecules 2017, 22, 389 2 of 11 Molecules 2017, 22, 389 2 of 11 studies have been conducted on N. oppositifolia, where only two compounds, namely verbascoside andverbascoside the acylated and diglycosidethe acylated 2 00diglycoside-acetyl-300-benzoyl-nuxioside, 2′′-acetyl-3′′-benzoyl-nuxioside, have been reported have been [6] reported These facts [6] encouragedThese facts encouraged us to reinvestigate us to reinvestigate the chemical constituentsthe chemical and constituents biological and activities biological of N. activities oppositifolia of, aimingN. oppositifolia to find, new aiming entities to find able new to cure entities contemporary able to cure diseases contemporary such as cancer. diseases In thissuch paper, as cancer. we describe In this thepaper, isolation we describe and structural the isolation elucidation and structural of four newelucidation compounds of four and new 11 knowncompounds compounds and 11 asknown well ascompounds assessment as ofwellin vitroas assessmentcytotoxic activitiesof in vitro of cytotoxic some of activities the isolated of some compounds of the isolated against threecompounds cancer cellagainst lines. three cancer cell lines. 2. Results and Discussion 2.1. Phytochemical Study As part of ourour searchsearch forfor novelnovel medicinalmedicinal compoundscompounds fromfrom plants,plants, wewe investigatedinvestigated the aerial parts of N.N. oppositifolia oppositifolia. .Chromatographic Chromatographic separation separation and and purification purification resulted resulted in the in theisolation isolation and andfull fullidentification identification of three of threenew labdane new labdane diterpenoic diterpenoic acids (1 acids–3), a (new1–3), seco-triterpene, a new seco-triterpene, 3,4-seco olean-12- 3,4-seco olean-12-en-3,30en-3,30 dioic acid dioic (4), along acid (with4), along nine withknown nine triterpenes, known triterpenes, and the common and the phytosterols common phytosterols β-sitosterol βand-sitosterol stigmasterol and stigmasterol (5–16) (Figure (5– 1).16 ) (Figure1). HOOC 12 14 13 15 11 COOH 20 COOH H H 1 16 H O 9 8 17 O 2 10 H 3 5 O 7 O 4 6 O H H H 19 18 R HO H O 1, R= H 2 4 3, R= =O R1 R R R2 H H H H H H O HO O H 5, R= CHO 6 β-sitosterol 22−23 8, R= COOH, R1= CH3,R2=H 11,R=CH2OH 7 Δ , stigmasterol 9, R=COOH, R1= H, R2= CH3 R 3 R4 R2 O H H R1 COOH R H H HO O H H 10,R=H,R1=COOH,R2=CH3,R3=H,R4=CH3 16 12, R= OH, R1= COOH, R2= H, R3= R4= CH3 13, R= OH, R1= COOH, R2= R4= CH3,R3=H 14,R=H,R1=R2=CH3, R3= H, R4= COOH 15, R= H, R1= COOH, R2= H, RR3=R4= CH3 FigureFigure 1.1. StructuresStructures of of isolated isolated compounds compounds from from aerial aerial parts parts of N. oppositifolia.oppositifolia. The molecular formula of compound 1, obtained as a viscous liquid, was determined to be C22H36O4 by HR-EI-MS analysis (m/z 364.2614 [M+]) with five degrees of unsaturation. IR showed intense absorption bands at 3470 (OH), 1745 (CO2R), 1715 (CO2H) and 1665 (C=C), suggesting the Molecules 2017, 22, 389 3 of 11 The molecular formula of compound 1, obtained as a viscous liquid, was determined to be + C22H36O4 by HR-EI-MS analysis (m/z 364.2614 [M ]) with five degrees of unsaturation. IR showed intense absorption bands at 3470 (OH), 1745 (CO2R), 1715 (CO2H) and 1665 (C=C), suggesting the presenceMolecules of 2017 OH,, 22, 389 two carbonyl groups assigned to an ester and free carboxylic acid groups3 of and11 an olefinic double bond, respectively. The carbonyl groups showed signals at δC 170.8 and 179.0 ppm 13presence of1 OH, two carbonyl groups assigned to an ester and free carboxylic acid groups and an in C-NMR. H-NMR revealed the presence of six methyl groups at δH 2.00, 1.62, 0.93, 0.92, 0.87 and 0.79olefinic ppm, assigneddouble bond, to acetate, respectively. olefinic Th (Me-17),e carbonyl secondary groups showed methyl signals (Me-16), at δ andC 170.8 three and tertiary 179.0 ppm methyl in 13 1 groups,C-NMR. Me-19, H-NMR Me-18 revealed and Me-20, the presence respectively. of six Themethyl presence groups of at a δ trisubstitutedH 2.00, 1.62, 0.93, double 0.92, bond0.87 and was 0.79 ppm, assigned to acetate, olefinic (Me-17), secondary methyl (Me-16), and three tertiary methyl evident from an olefinic methyl group at δH 1.62 ppm allylically coupled to the olefinic proton at groups, Me-19, Me-18 and Me-20,1 respectively. The presence of a trisubstituted double bond was δH 5.34 (H-5). Additionally, the H-NMR spectra showed a downfield triplet centered at 4.95 ppm evident from an olefinic methyl group at δH 1.62 ppm allylically coupled to the olefinic proton at δH and correlated it directly to a carbon signal at δ 68.9 in an HSQC experiment, and assigned it to H-2. 5.34 (H-5). Additionally, the 1H-NMR spectra Cshowed a downfield triplet centered at 4.95 ppm and The 13C-NMR and distortionless enhancement by polarization transfer (DEPT) experiment afforded a correlated it directly to a carbon signal at δC 68.9 in an HSQC experiment, and assigned it to H-2. The total of 22 carbon atoms ascribed to six methyl, six methylene, five methine groups and five quaternary 13C-NMR and distortionless enhancement by polarization transfer (DEPT) experiment afforded a δ carbontotal atoms,of 22 carbon two of thematoms appearing ascribed to at sixC 170.8methyl and, six 179.0 methylene, ppm, assigned five methine to an acetategroups carbonyland five at C-2 and a free carboxylic acid carbonyl at C15. Based on the above spectral evidence, the structure of quaternary carbon atoms, two of them appearing at δC 170.8 and 179.0 ppm, assigned to an acetate (1) wascarbonyl proposed at C-2 toand be a a free labdane-type carboxylic diterpeneacid carbonyl with at an C15. acetoxyl Based group,on the above a trisubstituted spectral evidence, double bondthe 1 1 andstructure a free carboxylic of (1) was acidproposed group to [be5]. a ThelabdanH-e-typeH COSY diterpene experiment with an showedacetoxyl cross-peakgroup, a trisubstituted correlations betweendouble the bond downfield and a free proton carboxylic at δH 4.94 acid (H-2) group and [5].
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