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Flavonoid Glycosides from the Stem Bark of Margaritaria Discoidea Demonstrate Antibacterial and Free Radical Scavenging Activities

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Flavonoid Glycosides from the Stem Bark of Margaritaria Discoidea Demonstrate Antibacterial and Free Radical Scavenging Activities PHYTOTHERAPY RESEARCH Phytother. Res. 28: 784–787 (2014) Published online 22 August 2013 in Wiley Online Library (wileyonlinelibrary.com) DOI: 10.1002/ptr.5053 SHORT COMMUNICATION Flavonoid glycosides from the stem bark of Margaritaria discoidea demonstrate antibacterial and free radical scavenging activities Edmund Ekuadzi,1 Rita Dickson,1 Theophilus Fleischer,2 Kofi Annan,2 Dominik Pistorius,3 Lukas Oberer4 and Simon Gibbons5* 1Department of Pharmacognosy, Faculty of Pharmacy and Pharmaceutical Sciences, College of Health Sciences, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana 2Department of Herbal Medicine, Faculty of Pharmacy and Pharmaceutical Sciences, College of Health Sciences, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana 3Natural Product Unit, Novartis Institutes for Biomedical Research, Basel 4056, Switzerland 4Analytical Sciences, Novartis Institutes for BioMedical Research, Basel 4056, Switzerland 5Department of Biological and Pharmaceutical Chemistry, UCL School of Pharmacy, 29-39 Brunswick Square, London WC1N 1AX, UK One new flavonoid glycoside, along with three known flavonoid glycosides were isolated from the stem bark of Margaritaria discoidea, which is traditionally used in the management of wounds and skin infections in Ghana. The new flavonoid glycoside was elucidated as hydroxygenkwanin-8-C-[α-rhamnopyranosyl-(1 → 6)]-β- glucopyranoside (1) on the basis of spectroscopic analysis. The isolated compounds demonstrated free-radical scavenging as well as some level of antibacterial activities. Microorganisms including Staphylococcus aureus are implicated in inhibiting or delaying wound healing. Therefore, any agent capable of reducing or eliminating the microbial load present in a wound as well as decreasing the levels of reactive oxygen species may facilitate the healing process. These findings therefore provide some support to the ethnopharmacological usage of the plant in the management of wounds. Copyright © 2013 John Wiley & Sons, Ltd. Keywords: Margaritaria discoidea; flavonoid glycosides; margadiscoside; fagovatin; antibacterial activities; antioxidant activities. INTRODUCTION MATERIALS AND METHODS Margaritaria discoidea (Baill.) G.L. Webster (Euphorbiaceae), General experimental procedures. NMR spectra were previously referred to as Phyllanthus discoideus, is a tree that recorded on a Bruker AV-III-600 spectrometer equipped finds use in ethnomedicine as a treatment against wounds and with a 1.7 mm TXI cryoprobe. The mass spectra were infectious skin diseases (Abbiw, 1990; Irvine, 1961). Earlier performed by ESI in positive-ion mode using an LTQ phytochemical investigationshaveshownthepresenceof Orbitrap XL mass spectrometer (ThermoScientific). IR eight Securinega alkaloids (Fehler, 2000; Mensah et al., 1988; spectra were measured as a solid film with a Bruker Weenen et al., 1990) and betulinic acid (Calixto et al., 1998). Hyperion 2000 FTIR microscope connected to a Vertex In an earlier work, we reported the antibacterial, antioxidant 70 spectrometer. Flash chromatography was carried out and anti-inflammatory activities of the 70% ethanol extract on RediSep Rf normal phase disposable columns. Prep of the M. discoidea leaves and stem bark (Dickson et al., LC/MS was carried out on an Agilent Technologies 1200 2010). Here, we identify and characterize the compounds series Chromatograph fitted with an Agilent 1100 series that may be contributing to the biological activities LC/MSD quadrupole mass spectrometer. observed in our earlier study. The isolation, structure elucidation, antioxidant and antibacterial activities of one new flavone glycoside (1) along with three known Plant material. The stem bark of M. discoidea was flavonoid glycosides (2, 3 and 4) are reported herein for collected from Kente in the Amansie Central District the first time in this species. The structure of compound in June 2009. A voucher specimen (KNUST/HM1/2010/ 1 was established using NMR spectroscopy, IR, UV and S003) has been deposited at the Department of Pharma- MS data (Fig. 1). cognosy Herbarium. Extracts of Margaritaria discoidea are well known as wound healing remedies in Ghana. The presence of these compounds may contribute in part to the wound healing benefits derived from the plant when used traditionally. Extraction and isolation of compounds. The dried pow- dered stem bark (2.5 kg) was successively Soxhlet-extracted using petroleum ether (50.50 g), EtOAc (208.75 g) and 70% * Correspondence to: Professor Simon Gibbons, Department of Biological and Pharmaceutical Chemistry, UCL School of Pharmacy, 29–39 Brunswick EtOH (386.25 g). The resulting extracts were evaporated Square, London WC1N 1AX, UK. on a rotary evaporator under reduced pressure at a temper- Email: [email protected] ature of less than 40 °C. 20 g of the 70% EtOH extract was Received 26 March 2013 Revised 06 June 2013 Copyright © 2013 John Wiley & Sons, Ltd. Accepted 08 July 2013 ANTIBACTERIAL AND ANTIOXIDANT FLAVONOID GLYCOSIDES 785 polarities to yield fractions A (0.07 g), B (1.06 g), C (3.72 g), D (2.89 g) and E (3.66 g). Fraction D was subjected to prep-LC/MS using a SunFire C-18 Optimal Bed Density column (150 × 30 mm; 5 μm particle diameter; Waters) with a flow rate of 60 mL/min and a mobile phase of H2O and MeCN, each containing 0.1% HCOOH, with a linear gradient from 10% to 30% MeCN in 15 min to yield fractions D1 (58.20 mg), D2 (18.05 mg) and D3 (9.30 mg). Fraction D3 afforded pure compound 2 (9.30 mg; 0.0072%w/w). Further fractionation of D1 and D2 on a Luna Phenyl-Hexyl column (150 × 21 mm; 5 μm particle diameter; Phenomenex) with a flow rate of 24 mL/min and a mobile phase of H2O and MeCN, each containing 0.1% HCOOH, with a linear gradient from 15% to 40% MeCN in 15 min yielded compounds 3 (7.50 mg; 0.0058%w/w), 4 (7.88 mg; 0.0061%w/w) and 1 (1.42 mg; 0.0011% w/w), respectively. Bioactivity of isolated compounds. Broth microdilution assay. Minimal inhibitory concentration values of the compounds were determined based on a broth micro-well dilution method (Eloff, 1998). The iocula of microorganisms Figure 1. Selected COSY (bold faced bonds) and HMBC (arrows) were prepared from 12-h broth cultures, and serial dilutions correlations of compound 1. were made to achieve a suspension of approximately 105 CFU/mL. Growth of the microorganisms was deter- mined by adding 20 μL of a 5% solution of tetrazolium salt and incubating for a further 30 minutes. Amoxycillin was included as the positive control. All experiments Table 1. Antibacterial activity of isolated compounds were carried out in triplicate. MIC (μg/mL) Microorganisms 12 3 4 Free radical scavenging activity (DPPH method). The isolated compounds were compared to n-propyl gallate Gram-positive (in methanol), and the DPPH method (Blois, 1958) Bacillus subtilis NCTC 10073 500 500 >500 >500 was used. A 20 mg/L solution of DPPH in methanol Staphylococcus aureus 500 500 >500 >500 was prepared, and 3 mL of this solution was added to ATCC 25923 1 mL each of the test compounds at 1, 0.5, 0.1 and 0.05 mg/mL in methanol. After 3 min, the absorbance Gram-negative was measured at 517 nm using a T90+ UV/VIS Proteus vulgaris NCTC 4635 500 500 500 500 > > Spectrometer (PG Instruments Limited). 1 mL of methanol Pseudomonas aeruginosa 500 500 500 500 was added to 3.0 mL DPPH solution which served as a ATCC 27853 negative control. All experiments were carried out in All experiments were carried out in triplicates. MIC readings for all wells triplicate. Inhibition of radical scavenging was calculated were the same. 200 μg/mL of amoxicillin served as positive control. according to the following equation: MIC readings for all wells of the same compound were identical. % DPPH scavenging activity ¼ ½ðÞA0 À A1 =A0 x 100 Table 2. IC50 values (μg/mL) for free radical scavenging activity with A being the absorbance of the control, and A , the of the isolated compounds 0 1 absorbance in the presence of the test sample. Data were Compounds IC50 DPPH (μg/mL) presented as % DPPH scavenging effect against concen- tration and the IC50 determined. 1 17.45 2 20.34 3 68.94 4 24.88 RESULTS AND DISCUSSION n-Propyl gallate 7.983 All experiments were carried out in triplicates. n-Propylgallate Compound 1 was obtained as a yellow amorphous solid. served as positive control. Its IR spectrum exhibited absorption bands for an α, β- unsaturated ketonic functional group (1652 and 1607 cmÀ1) and hydroxyl groups (3381 cmÀ1). The UV subjected to silica gel Flash Chromatography (≤4bar)using spectrum of 1 in methanol displayed two major a ternary gradient consisting of C6H14, EtOAc and MeOH absorption peaks at 245.4 (with a shoulder) and starting with nonpolar conditions and gradually of increasing 346.2 nm +indicative of a flavone natural product with Copyright © 2013 John Wiley & Sons, Ltd. Phytother. Res. 28: 784–787 (2014) 786 E. EKUADZI ET AL. Table 3. 1H and 13C NMR chemical shifts of compounds 1 and 2 (in DMSO-d6, 600 MHz) 12 Chemical shifts Chemical shifts Chemical shifts Chemical shifts Carbon no. (ppm) 1H NMR (ppm) 13C NMR (ppm) 1H NMR (ppm) 13C NMR 2 - 164.3; 164.1 - 165.5; 164.0 3 6.70 102.5 6.88 (s); 6.86 (s) 103.4 4 - 182.0; 181.7 - 182.5; 182.0 5 - 160.3; 159.5 - 159.5; 160.5 6 6.78; 6.80 91.0; 90.1 - 110.0 7 - 164.8; 163.6 - 165.3; 164.0 8 - 109.5; 109.4 6.85 (s); 6.84 (s) 91.0; 92.0 9 - 156.8; 156.6 - 156.8; 157.0 10 - 107.0 - 104.0; 104.5 C-1′ - 104.6; 104.1 - 121.0 C-2′ 7.42 112.8 7.98 (d, 7.3 Hz) 129.0 C-3′ - 146.1 6.95 (d, 8.8 Hz) 116.0 C-4′ - 156.8 - 161.7 C-5′ 6.83 115.8 6.95 (d, 8.8 Hz) 116.0 C-6′ 7.45 119.4 7.98 (d, 7.3 Hz) 129.0 8-C-Glc 6-C-Glc C- 1″ 4.58 (d, 9.9 Hz); 4.60 (d, 9.9 Hz) 72.9 4.58 (d, 9.9 Hz); 4.60 (d, 9.9 Hz) 73.0; 72.5 C- 2″ 3.97 (t, 8.8, 8.
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