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Antiplasmodial and Antimycobacterial Cyclopeptide Alkaloids from the Root of Ziziphus Mauritiana

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Antiplasmodial and Antimycobacterial Cyclopeptide Alkaloids from the Root of Ziziphus Mauritiana Phytochemistry 72 (2011) 909–915 Contents lists available at ScienceDirect Phytochemistry journal homepage: www.elsevier.com/locate/phytochem Antiplasmodial and antimycobacterial cyclopeptide alkaloids from the root of Ziziphus mauritiana Panomwan Panseeta a, Kanlaya Lomchoey a, Samran Prabpai b, Palangpon Kongsaeree b,c, ⇑ Apichart Suksamrarn d, Somsak Ruchirawat e, Sunit Suksamrarn a, a Department of Chemistry and Center of Excellence for Innovation in Chemistry, Faculty of Science, Srinakharinwirot University, Bangkok 10110, Thailand b Department of Chemistry, Faculty of Science, Mahidol University, Bangkok 10400, Thailand c Center for Excellence in Protein Structure and Function, Faculty of Science, Mahidol University, Bangkok 10400, Thailand d Department of Chemistry, Faculty of Science, Ramkhamhaeng University, Bangkok 10240, Thailand e Chulabhorn Research Institute, Chemical Biology Program, Center for Environmental Health, Toxicology and Management of Chemicals (ETM), Chulabhorn Graduate Institute, Vipavadee Rangsit Highway, Bangkok 10210, Thailand article info abstract Article history: Investigation of the MeOH extract obtained from the root of the Ziziphus mauritiana grown in Thailand Received 6 October 2010 resulted in the isolation of two 14- and 13-membered cyclic alkaloids, mauritine L (1) and mauritine Received in revised form 26 January 2011 M(2), and three known cyclopeptide alkaloids, nummularines H (3), B (4) and hemsine A (5). Their struc- Available online 28 March 2011 tures were elucidated on the basis of extensive NMR spectroscopic analysis. The first single crystal X-ray diffraction study of the 13-membered ring cyclopeptide, nummularine B methiodide (40), revealed all S Keywords: configurations on the amino acid residues. The isolated alkaloids exhibited potent antiplasmodial activity Ziziphus mauritiana against the parasite Plasmodium falciparum with the inhibitory concentration (IC ) ranging from 3.7 to Rhamnaceae 50 10.3 M. Compounds 2 and 3 also demonstrated antimycobacterial activity against Mycobacterium tuber- Cyclopeptide alkaloid l Mauritines L and M culosis with the MIC of 72.8 and 4.5 lM, respectively. Antiplasmodial activity Ó 2011 Elsevier Ltd. All rights reserved. Antimycobacterial activity 1. Introduction subgroup of alkaloid obtained, whereas only one 13-membered macrocyclic alkaloid isolated from this plant (Gournelis et al., Phytochemical investigations have established the genus Zizi- 1998). These included the 4(14)-membered ring class: mauritine phus (Rhamnaceae family) to be a rich source of cyclopeptide alka- C, amphibine F and frangufoline (Tschesche et al., 1974b); the loids (Hesham et al., 2007; Tan and Zhou, 2006), lupane and 5(14)-membered ring type: mauritines A and B (Tschesche et al., ceanothane triterpenes (Suksamrarn et al., 2006). Cyclopeptide 1972), DÀF(Tschesche et al., 1974b), H (Tschesche et al., 1977), J macrocycles of Ziziphus species showed interesting biological prop- (Jossang et al., 1996), K (Singh et al., 2007), and amphibines B erties, including, for example, sedative (Han et al., 1989), analgesic and E (Tschesche et al., 1974b), D (Tschesche et al., 1972), and (Trevisan et al., 2009), antibacterial (Morel et al., 2002), antifungal the 4(13)-membered cyclic alkaloid sativanine K (Singh et al., (Pandy and Devi, 1990), antiplasmodial (Suksamrarn et al., 2005) 2007). The low natural abundance together with the interesting and immunostimulant (Lin et al., 2000) activities. Ziziphus mauriti- scaffold of cyclopeptides has attracted several synthetic groups ana Lam. or Phut-sa in Thai is a medium-sized tree, native to Thai- to increase their availability (Schmidt et al., 1983; Heffner et al., land and Asian countries and has been used traditionally for 1992; Gournelis et al., 1998; Temal-Laïb et al., 2002; He et al., treatment of diarrhea, ulcers, vomiting and indigestion (Bunyapra- 2007; Toumi et al., 2007a, 2007b, 2008), including mauritines A– phatsara and Chokechaijaroenporn, 1999). In continuation of our C, F (Laib et al., 2000; Cristau et al., 2005), mauritine D and amphi- work on new antimalarial substance of new structural type from bine E and their epimers (Kim et al., 2003; Joullie and Richard, Ziziphus, the root extract of Z. mauritiana was screened and 2004) and frangufoline (Xiao et al., 1998). In this paper, the isola- exhibited in vitro antiplasmodial potential against Plasmodium tion and structure elucidation of two new cyclopeptide alkaloids falciparum. Previous phytochemical studies of this plant species of the 4(14)-type, mauritine L (1), and the 5(13)-type, mauritine established the 14-membered ring cyclopeptides to be the largest M(2), are described together with three known alkaloids nummu- larines H and B (3–4) and hemsine A (5) from the root of Z. mauri- ⇑ Corresponding author. Tel.: +66 2 6495000x8217; fax: +66 2 2600128. tiana. Antimalarial and antimycobacterial evaluations of the E-mail address: [email protected] (S. Suksamrarn). isolates are also reported here (Fig. 1). 0031-9422/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.phytochem.2011.03.003 910 P. Panseeta et al. / Phytochemistry 72 (2011) 909–915 Fig. 1. Chemical structures of compounds 1–5. 2. Results and discussion 2.05. From the 1H–1H COSY and 1H–13C HMQC spectra of 1 and comparison with the reported values led to a conclusion for the The pulverized, dried root of Z. mauritiana was extracted succes- presence of p-oxystyrylamine group, b-phenylserine, isoleucine sively with EtOAc and MeOH. The resulting extracts were tested for and N-methylisoleucine amino acid units (Tan and Zhou, 2006). antimalarial and antituberculosis activities and only the MeOH ex- Analysis of the COSY, HMBC and NOESY spectra provided the con- tract was active to the antiplasmodial test. A typical intense blue nections among these subunits (Fig. 1). The signal for p-oxystyryla- coloration with anisaldehydeÀH2SO4 reagent for the MeOH extract mino NH-3 (dH 6.57) showed weak NOESY correlation to signal at indicated the presence of cyclopeptide alkaloid (Suksamrarn et al., dH 4.03 (H-5) and the HMBC correlations of the resonance at dY 2005). However, the EtOAc extract gave very weak blue color 6.71 (H-2) to C-14 and of H-1 (dH 6.36) to C-2 allowed the place- development. The MeOH soluble extract was therefore selected ment of an isoleucine moiety next to the styrylamine group. The for further chromatographic separations and resulted in the isola- correlations of H-8 (dY 4.64, dd, J = 8.4, 6.3 Hz) to NH-6 (dY 6.42, 0 tion of two new, in addition to three known, cyclopeptide alka- d, J = 7.8 Hz) and H-22 (dY 7.50) in the NOESY and of H-9 (dY loids. The UV absorption bands at around 270 and 320 nm were 6.17, d, J = 6.3 Hz) to C-7 (dC 171.5), C-21 (dC 137.2) and C-22 (dC observed for the 13-membered cyclopeptides 2–4, which is the 127.5) in the HMBC experiments established the connection of iso- characteristic styrylamine chromophore. Due to the strain of the leucine to b-phenylserine fragments in the macrocyclic ring. The ring system in the molecule, the 14-membered cyclopeptide alka- NOESY cross-peak for methine proton H-9 to aromatic signal at loid lacked these absorption bands, except for the presence of tryp- dH 7.34 (H-12) was also observed. The b-phenylserine moiety tophan moiety, which showed the absorption bands at around 220, was characterized as erythro relative configuration by the vicinal 270 and 290 nm (Gournelis et al., 1998). Their IR spectra exhibited coupling constant (J=6.3 Hz) between H-8 and H-9 and the rela- À1 13 diagnostic peaks for amino (3291–3393 cm ), amide (1679– tively upfield shift of the C NMR signal of C-9 (dC 81.4) compared À1 À1 1693 cm ), and aryl ether (1221–1237 cm ) functions. with dC 86.3 of condaline A for the threo form (Morel et al., 2005). Compound 1 was isolated as a colorless powder and the molec- NOE enhancements displayed between NH-25 to H-8 and H-27 in ular formula C30H40N4O4 was established by HRTOFMS at m/z the NOESY spectrum, and the HMBC of the latter with the carbonyl + 13 521.3124 [M + H] . The C NMR and DEPT spectra (CDCl3, carbon signal at dC 173.5 (C-26) supported that the N-methyliso- 75 MHz) indicated 30 signals attributable to four methyls, one N- leucine unit was attached to the phenylserine at N-25. HMBC cor- methyl, two methylenes, seventeen (including one oxygenated relations of the methyl proton signals at dH 0.62 (H-31) and dH 2.05 and two olefinic) methines and six quaternary carbons, three of (N-CH3) to the signal at dC 69.6 (C-27) were also observed (Fig. 2). which corresponded to the carbonyl groups (Table 1). The 1H The CD spectrum of 1 displayed an intense negative and a weak NMR spectrum of 1 (Table 1) displayed signals corresponding to positive Cotton effect bands at 239 and 279 nm, respectively, con- Z-olefinic protons of styrylamine at dY 6.36 (d, J = 7.3 Hz) and sistent with the 5S,8S,9S-configurations presented in the 14- 6.71 (dd, J = 9.7, 7.3 Hz), a number of aromatic, methine, methylene membered ring nucleus (Gournelis et al., 1998). In addition, the and methyl protons including a singlet of N-methyl proton at dH NMR spectroscopic data of the macrocyclic part of 1 are in good P. Panseeta et al. / Phytochemistry 72 (2011) 909–915 911 Table 1 1H and 13C NMR spectroscopic data for compounds 1, 2, 4 and 40.a Position dH dC 1b 2b 4b 40c 1b 2b 4b 40c 1 6.36 d (7.3) 5.91 d (9.0) 5.95 d (8.9) 6.11 d (8.9) 115.5 107.2 107.2 110.7 2 6.71 dd (9.7, 7.3) 6.91 dd (11.2, 9.0) 6.94 dd (11.0, 8.9) 6.87 d (8.9) 125.5 121.3
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