Phytochemical and biological investigations of Albizzia lebbeck Benth.
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1 2008 The Authors Derechos de Publicación 2008 Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas, 7 (5), BLACPMA ISSN Artículo Original Original Article Benth. [Estudios fitoquímicos y biológicos sobre la Albizzia lebbeck Benth.] Mohammad M. HUSSAIN 1, Mohammad S. RAHMAN 1, Abdul JABBAR 1, Mohammad A. RASHID 1,2* 1. Department of Pharmaceutical Chemistry, Faculty of Pharmacy, University of Dhaka, Dhaka-1000, Bangladesh. 2. Centre for Biomedical Research, University of Dhaka, Dhaka-1000, Bangladesh. *Contact: rashidma@aitlbd.net ; rashid_phdu@yahoo.com Received Recibido 11/06/08; Aceptado Accepted: 21/09/2008; Publicado Published 30/09/2008 Abstract Lupeol (1), stigmasterol (2), 4-hydroxy-3-methoxycinnamic acid (3) and trans-p-coumaric acid (4) were isolated from the n-hexane and chloroform soluble fractions of a methanol extract of the root of Albizzia lebbeck Benth. The structures of the isolated compounds were elucidated as by extensive spectroscopic studies, including high field NMR analyses. Different partitionates of the methanol extract exhibited mild to moderate antimicrobial activity and varying degrees of toxicity. This is the first report of isolation of compounds 1-4 from this species. Key words: Albizzia lebbeck, Leguminosae, lupeol, stigmasterol, 4-hydroxy-3-methoxycinnamic acid, trans-p-coumaric acid. Resumen Desde la fracción soluble en hexano obtenida a partir de un extracto metanólico de las raíces de Albizzia lebbeck Benth. se aislaron lupeol (1), estigmasterol (2), ácido 4-hidroxi-3-metoxicinámico (3) y ácido trans-p-cumárico (4). Las estructuras de los compuestos aislados se establecieron por estudios espectroscópicos, incluyendo estudios de RNM de alta resolución. Las diferentes fracciones del extracto metanólico mostraron actividad antimicrobiana desde leve hasta moderada y diversos niveles de actividad toxicidad. Este es el primer informe sobre el aislamiento de los compuestos 1-4 de esta especie. Palabras clave: Albizzia lebbeck, Leguminosae, lupeol, estigmasterol, ácido 4-hidroxi-3-metoxicinámico, ácido trans-p-cumárico. INTRODUCTION (4) as well as preliminary antimicrobial activity and toxicity of the extractives against Artemia salina. Albizzia lebbeck Benth., Leguminosae (Bengali name- Shirish, Kalo koroi) is an unarmed deciduous tree of m height that grows all over Bangladesh. The root of the plant has astringent property and is useful in opthalmia and skin diseases. The leaves are used in the treatment of night blindness and syphilis. The flowers of the plant are reputed for its aphrodisiac properties and are also useful in asthma and snake bite. The bark of the plant is anthelmintic and used in the treatment of inflammation, bronchitis, toothache and leprosy (Rashid et al., 2003; Kirtikar and Basu, 1980). Previous phytochemical investigations with A. lebbeck revealed the occurrences of glycosides (Varshney, 1976), alkaloids (Dixit and Misra, 1997), terpenoids, steroids, saponins (Pal et al., 1995), anthraquinones and other phenolics (Deshpande and Shastri, 1977). We, herein, report the isolation of lupeol (1), stigmasterol (2), 4-hydroxy-3- methoxycinnamic acid (3) and trans-p-coumaric acid MATERIALS AND METDS General Experimental Procedures The 1 H NMR spectra were recorded using a Bruker AMX-400 (400 MHz) instrument in CDCl 3 and the δ values for were referenced to the residual nondeuterated solvent signal. Plant Material Root of A. lebbeck Benth. was collected from Dhaka in the month of September A voucher specimen for this collection has been maintained in Bangladesh National Herbarium (DACB 32758), Dhaka, Bangladesh. Extraction and Isolation The powdered root (1 kg) of the plant was soaked in 1.5 L of methanol for 16 days and then filtered through a cotton plug followed by Whatman filter
2 paper number 1. The extract was concentrated with a rotary evaporator and it afforded 20 g of the methanol extract. A portion (4 g) of it was fractionated by the modified Kupchan partitioning protocol (Kupchan et al., 1975; Vanwagenen et al., 1993) into n-hexane, carbon tetrachloride, chloroform and aqueous soluble fractions. In brief, the methanol extract (4 g) was dissolved in 100 ml of 10% aqueous methanol and extracted three times with 300 ml of n-hexane. The remaining aqueous phase was then increased in polarity to 20% H 2 O and extracted three times with 300 ml of carbon tetrachloride. The remaining aqueous phase was increased further in polarity to 40% H 2 O and extracted three times with 300 ml of CHC1 3. Subsequent evaporation of solvents afforded n-hexane (0.88 g), carbon tetrachloride extract (0.50 g), chloroform (1.06 g) and aqueous soluble materials (1.40 g). The n-hexane and chloroform soluble partitionates were separately chromatographed over silica gel (Kiesel gel 60, mesh ) and both the columns were eluted with pet ether-ethyl acetate and ethyl acetate-methanol mixtures of increasing polarities. Compound 1 was isolated as colorless needles from the column fractions of the n-hexane partitionate eluted with 15 % ethyl acetate in pet ether, while fractions eluted with 20% ethyl acetate upon rechromatography over silica gel F 254 provided compound 2 in pure form. Similar column chromatographic separation of the chloroform soluble materials eluted with 20-30% ethyl acetate in n- hexane afforded compounds 3 and 4. Elucidation Compound 1: Lupeol (4 mg, % yield): White gum; 1 H NMR (400 MHz, CDCl 3 ): δ 4.67 & 4.55 (each 1H, br.s, H 2-29), 3.20 (1H, dd, J=5.03, 11.5 Hz, H-3), 2.28 (1H, m, H-19), 1.67 (3H, s, H 3-30), 1.02 (3H, s, H 3-26), 0.95 (3H, s, H 3-23), 0.93 (3H, s, H 3-27), 0.84 (3H, s, H 3-25), 0.82 (3H, s, H 3-28), 0.78 (3H, s, H 3-24). Compound 2: Stigmasterol (5 mg, % yield): Colorless powder; 1 H NMR (400 MHz, CDCl 3 ): δ 5.35 (1H, m, H-6), 5.14 (1H, dd, J = 15.0, 6.5 Hz, H-22), 5.04 (1H, dd, J = 15.0, 9.0 Hz, H-23), 3.51 (1H, m, H-3), 1.00 (3H, s, H 3-19), 0.92 (3H, d, J = 6.0 Hz, H 3-21), 0.84 (3H, d, J = 6.0 Hz, H 3-26), 0.82 (3H, t, J = 6.5 Hz, H 3-29), 0.80 (3H, d, J = 6.0 Hz, H 3-27), 0.67 (3H, s, H 3-18). Compound 3: 4-Hydroxy-3-methoxycinnamic acid (5 mg, % yield); Amorphous ; 1 H NMR (400 MHz, CDCl 3 ): δ 7.61 (1H, d, J = 16.9 Hz, H-7), 7.06 (1H, dd, J = 8.4, 1.5 Hz, H-6), 7.02 (1H, d, J = 1.5 Hz, H-2), 6.81 (1H, d, J = 8.4 Hz, H-5), 6.28 (1H, d, J = 16.9 Hz, H-8); 3.91 (3H, s, OMe-3). Compound 4: trans-p-coumaric acid (5 mg, % yield); Colorless powder; 1 H NMR (400 MHz, CDCl 3 ): δ 7.59 (1H, d, J = 16.9 Hz, H-7), 7.42 (1H, d, J = 8.4, H-2 & H-6), 6.81 (1H, d, J = 8.4 Hz, H-3 & H-5), 6.26 (1H, d, J = 16.9 Hz, H-8). Antimicrobial Screening The disc diffusion method (Barry, 1980; Bauer et al., 1966) was used to test antimicrobial activity of the extractives against thirteen bacteria and three fungi (Table 1) collected as pure cultures from the Institute of Nutrition and Food Science (INFS), University of Dhaka, Bangladesh. Solutions of known concentration (μg/ml) of the test samples were made by dissolving measured amount of the samples in calculated volume of solvents. Dried and sterilized filter paper discs (6 mm diameter) were then impregnated with known amounts of the test substances using micropipette and the residual solvents were completely evaporated. Discs containing the test materials were placed on nutrient agar medium uniformly seeded with the test microorganisms. Standard disc of kanamycin (30 μg/disc) and blank discs (impregnated with solvents followed by evaporation) were used as positive and negative control, respectively. These plates were then kept at low temperature (4 o C) for 24 hours to allow maximum difusión of test materials and kanamycin. The plates were then incubated at 37 o C for 24 hours to allow maximum growth of the organisms. The test material having antimicrobial activity inhibited the growth of the microorganisms and a clear, distinct zone of inhibition was visualized surrounding the discs. The antimicrobial activity of the test agents was determined by measuring the diameter of zone of inhibition expressed in mm. The experiment was carried out in triplicate. Brine shrimp lethality bioassay Brine shrimp lethality bioassay (McLaughlin et al., 1998; Meyer et al., 1982; Persoone, 1980) technique was applied for the determination of general toxic property of the plant extractives. Preparation of positive control group Vincristine sulphate was used as the positive control. Measured amount of vincristine sulphate was dissolved in DMSO to get an initial concentration of Bol. Latinoam. Caribe Plant. Med. Aromaticas Vol. 7 (5)
3 20 μg/ml from which serial dilutions were made using DMSO to get 10 μg/ml, 5 μg/ml, 2.5μg/ml, 1.25 μg/ml, μg/ml, μg/ml, μg/ml, μg/ml, μg/ml. Then the solutions were added to the premarked vials containing ten live brine shrimp nauplii in 5 ml simulated sea water. Preparation of negative control group 100 μl of DMSO was added to each of three premarked glass vials containing 5 ml of simulated sea water and 10 shrimp nauplii. If the brine shrimps in these vials show a rapid mortality, then the test is considered as invalid as the nauplii died due to some reasons other than the cytotoxicity of the compounds. Preparation of test groups 4 mg of each of the partitionates obtained by Kupchan fractionation was dissolved in DMSO and solutions of varying concentrations such as 400, 200, 100, 50, 25, 12.50, 6.25, 3.125, and µg / ml were obtained by serial dilution technique. Then the solutions were added to the premarked vials containing ten live brine shrimp nauplii in 5 ml simulated sea water. Counting of nauplii After 24 hours, the vials were inspected using a magnifying glass and the number of survived nauplii in each vial was counted. From this data, the percent (%) of lethality of the brine shrimp nauplii was calculated for each concentration. The median lethal concentration (LC 50 ) of the test samples was obtained by a plot of percentage of the shrimps killed against the logarithm of the sample concentration. Statistical analysis For each of the extracts, three samples were prepared for each of the bioassays. The zone of inhibition and LC 50 were calculated as mean ± SD (n=3) for the antimicrobial screening and brine shrimp lethality bioassay, respectively. RESULTS AND DISCUSSION A total of four compounds were isolated from n- hexane and chloroform soluble fractions of a methanolic extract of the root bark of A. lebbeck Benth. by repeated chromatographic separation and purification over silica gel. The structures of the isolated compounds were solved by extensive NMR data analyses. The 1 H NMR spectrum (400 MHz, CDCl 3 ) of compound 1 showed a double doublet (J = 11.5, 5.03 Hz) of one proton intensity at δ 3.17 typical for H-3 of a terpene type carbon skeleton confirming β orientation. The spectrum displayed seven singlets at δ 0.95, 0.78, 0.84, 1.02, 0.93, 0.82 and 1.67 (3H each) assignable to the protons of methyl groups at C-4 (H 3-23, H 3-24), C-10 (H 3-25), C-8 (H 3-26), C-14 (H 3-27), C-17 (H 3-28) and C-20 (H 3-30), respectively. The spectrum also displayed two singlets at δ 4.67 and δ 4.55 (1H each) which indicated the presence of an iosprenyl side chain protons (H a -29 and H b -29). This suggested its relation with lupane-type of triterpenoid. By comparing the 1 H NMR data of compound 1 with previously published values (Aratanechemuge et al., 2004), it was characterized as lupeol (Figure 1). The identity was further substantiated by Co-TLC with authentic sample. Compound 2 (Figure 1) was characterized as stigmasterol by comparing of its 1 H NMR spectral data with reported values (Ikan, 1991) as well as by Co-TLC with standard stigmasterol. The 1 H-NMR spectrum (CDCl 3, 400 MHz) of compound 3 displayed a singlet of three proton intensity at δ 3.91 suggesting the presence of methoxyl protons. It also displayed two doublets centered at δ 7.02 (1H, J = 1.5 Hz), and δ 6.81 (1H, J = 8.4 Hz) and a double doublet (J = 8.4, 1.5 Hz) at δ 7.06 typical for 1, 3, 4 trisubstituted aromatic moiety in compound 3. The doublets (J = 16.9 Hz) at δ 7.61 and δ 6.28 could be assigned to the trans coupling protons H-7 and H-8, respectively. The relatively low field resonance of H-7 could be explained by its beta position to the carbonyl group, probably in the form of a carboxylic acid. On this basis compound 3 was identified as 4-hydroxy-3- methoxycinnamic acid (Figure 1). The identity of compound 3 was further confirmed by comparison of its spectral data with published literature (Xu et al., 2005). The 1 H-NMR spectrum of compound 4 revealed two doublets (J = 8.4 Hz) centered at δ 6.81 and δ 7.42, each integrating for two protons each. Two downfield doublets centered at δ 7.59 (1H, J =16.9 Hz) and δ 6.26 (1H, J = 16.9 Hz) suggested the presence of a pair of trans coupled olefinic protons at H-7 & H-8, respectively. The up field resonance of one of these signals at δ 6.81 suggested an oxygenated functional group, probably in the form of a hydroxyl group, to its close proximity. The splitting pattern and coupling constants of the aromatic protons indicated the presence of a 1,4-disubstituted Bol. Latinoam. Caribe Plant. Med. Aromaticas Vol. 7 (5)
4 benzene ring. On the basis of the above spectral data and by comparison of these values with those reported for trans-p-coumaric acid. Their identity of compound 4 (Figure 1). was confirmed as trans-pcoumaric acid (Kort et al., 1996). In the antimicrobial screening, the carbon tetrachloride, chloroform and aqueous soluble fractions of the methanolic extract exhibited moderate inhibitory activity against most of the test organisms (Table 1) with the zone of inhibition of 9-17 mm, 9-18 mm and 9-16 mm, respectively at a concentration of 400 μg/disc. On the other hand, the crude methanolic extract of the root showed very weak inhibitory activity and the n-hexane partitionate remained insensitive to the microorganisms at the test Figures 1-4: Lupeol (1), stigmasterol (2), 4-hydroxy-3- methoxycinnamic acid (3) and trans-p-coumaric acid (4) concentration. 1 The carbon tetrachloride soluble fraction of the methanolic extract showed strong inhibitory activity against S. dysenteriae with a zone of inhibiton of mm whereas moderate activity was noticed against V. mimicus (16.23 mm), S. paratyphi (15.33 mm), V. parahemolyticus (14.44 mm) and B. subtilis (14.25 mm). Again, the chloroform extractive exhibited strong activity against S. dysenteriae (18.26 mm) and V. parahemolyticus (17.31 mm). The growth of S. boydii (16.23 mm), V. mimicus (15.41 mm) and S. aureus (15.31 mm) was significantly inhibited by it. The aqueous fraction showed moderate inhibition against P. aeruginosa (16.23 mm), B. subtilis (15.30 mm) and S. boydii (15.11 mm). In case of fungal strains, the carbon tetrachloride soluble fraction revealed highest zone of inhibition against C. albicans (16.37 mm) while the chloroform soluble fraction was found significantly inhibitory against the growth of A. niger (17.34 mm). The aqueous fraction showed average zone of inhibition mm against the tested fungi. H H 3 CO H O 21 OH O OH 28 Bol. Latinoam. Caribe Plant. Med. Aromaticas Vol. 7 (5)
5 Table 1: Antimicrobial activity of test samples of A. lebbeck Benth. (400 µg/disc) and kanamycin (30 µg/disc ) Diameter of zone of inhibition (mm) Test microorganisms MER HX CT CF AQ KAN Gram positive bact. Bacillus cereus ± ± ± ± 0.65 B. megaterium ± ± ± ± ± 0.55 B. subtilis 9.25 ± ± ± ± ± 0.52 Staphylococcus aureus 8.21 ± ± ± ± ± 0.23 Sarcina lutea 9.34 ± ± ± ± ± 0.89 Gram negative bact. Escherichia coli ± ± ± ± 0.16 Pseudomonas aeruginosa 9.32 ± ± ± ± ± 0.62 Salmonella paratyphi 8.25 ± ± ± ± ± 0.42 S. typhi ± ± ± ± 0.13 Shigella boydii 8.29 ± ± ± ± ± 0.34 S. dysenteriae ± ± ± ±0.27 Vibrio mimicus 8.38 ± ± ± ± ± 0.37 V. parahemolyticus ± ± ± ± 0.21 Fungi Candida albicans 9.28 ± ± ± ± ±0.13 Aspergillus niger ± ± ± ± ± 0.36 Sacharomyces cerevacae ± ± ± ± ± 0.68 The diameter of zone of inhibition are expressed as mean ± SD (n=3); a diameter less than 8 mm was considered inactive; MER: methanolic extract of the root; HX: n-hexane soluble fraction of the methanolic extract; CT: carbon tetrachloride soluble fraction of the methanolic extract; CF: chloroform soluble fraction of the methanolic extract; AQ: aqueous fraction of the methanolic extract; KAN: kanamycin; - inactive The toxicity of the n-hexane (HX), carbon tetrachloride (CT), chloroform (CF) and aqueous soluble (AQ) fractions of the methanolic extract to brine shrimp was evaluated on A. salina. Table 2 shows the results of the brine shrimp lethality testing after 24 hours of exposure to the samples and the positive control, vincristine sulphate (VS). The LC 50 were found to be 2.14, 2.15, 3.14, 6.99 and 0.30 µg/ml for HX, CT, CF, AQ and VS, respectively. In comparison with the positive control (vincristine sulphate), the toxicity exhibited by the n-hexane and carbon tetrachloride soluble fractions of the methanolic extract was significant. CONCLUSION The phytochemical study of the n-hexane and chloroform extractives of the A. lebbeck Benth. afforded four purified compounds, lupeol (1), stigmasterol (2), 4-hydroxy-3-methoxycinnamic acid (3) and trans-p-coumaric acid (4) whose structures were established by extensive spectroscopic studies as well as comparison with published results. The bioactivities exhibited by the different extractives of A. lebbeck Benth. substantiate the folk uses of this plant species in various diseases. ACKNOWLEDGEMENT We wish to thank the Ministry of Science and Information & Communication Technology, Government of the Peoples Republic of Bangladesh for partial financial support for carrying out the research. REFERENCES Aratanechemuge Y, Hibasami H, Sanpin K, Katsuzaki H, Kunio I K, Komiya T Induction of apoptosis by lupeol isolated from mokumen Gossampinus malabarica L. Merr in human promyelotic leukemia HL-60 cells. Oncol Rep. 11: Barry AL Procedures for testing antimicrobial agents in agar media. In: Antibiotics in Laboratory medicines, Williams and Wilkins Co., Baltimore, USA. Bol. Latinoam. Caribe Plant. Med. Aromaticas Vol. 7 (5)
6 Bauer AW, Kirby WMM,. Sherris JC, Turck M Antibiotic susceptibility testing by a standard Bsingle disc method. Am J Clin Pathol. 45: Deshpande VH, Shastri RK Phenolics of Albizzia lebbek, A. amara and A. procera. Indian J Chem. 15B: Dixit AK, Misra LN Macrocyclic budmunchiamine alkaloids from Albizzia lebbek. Indian J Nat Prod. 60: Ikan R Natural product: A laboratory guide, 2nd Edition, Academic Press, N.Y., USA. Kirtikar KR., Basu BD Indian Medicinal Plants, Published by Singh B and Singh M P, India; 2 nd ed. Kort R, Vonk H, Xu XWD, Hoff, Crielaard W, Hellingwerf KJ Evidence for trans-cis isomerization of the p-coumaric acid chromophore as the photochemical basis fo the photocycle of photoactive yellow protein. FEBS Lett. 382: Kupchan S M., Britton RW, Lacadie JA, Ziegler MF, Sigel CW The isolation and structural elucidation of bruceantin and bruceantinol, new potent antileukemic quassinoids from Brucea antidysenterica. J Org Chem. 40: McLughilin JL, Rogers LL The use of Biological assays to evaluate botanicals. Drug Information J. 32: Meyer BN, Ferringni NR, Puam JE, Lacobsen LB, Nicols DE, McLaughilin JL Brine Shrimp: A convenient general bioassay for active constituents. Planta Med. 45: Pal BC, Achari B, Yoshikawa K, Arihara S Saponins from Albizzia lebbek. Phytochemistry 38: Persoone G Proceeding of the International Symposium on brine shrimp, Artemia salina, Vol. 1-3, Universa Press, Witteren, Belgium. Rashid RB, Chowdhury R., Hasan CM, Rashid MA Constituents of Albizzia lebbek and antibacterial activity of an isolated flavone derivative. Saudi Pharm J. 11: Vanwagenen BC, Larsen R, Cardellina JH II, Randazzo D, Lidert ZC, Swithenbank C Ulosantoin, a potent insecticide from the sponge Ulosa ruetzleri. J Org Chem. 58: Varshney IP Glycosides and carbohydrates from the members of the family Leguminosae. Univ Indore Res J Sci. 4: Xu F, Sun R, Sun J, Liu C, He B, Fan J Determination of cell wall ferulic and p-coumaric acids in sugarcane base. Anal Chim Acta. 552: The authors, licensee BLACPMA ISSN Bol. Latinoam. Caribe Plant. Med. Aromaticas Vol. 7 (5)
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