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Chemical Composition of the Essential Oils of Variegated Pink-Fleshed Lemon (Citrus X Limon L

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Chemical Composition of the Essential Oils of Variegated Pink-Fleshed Lemon (Citrus X Limon L Chemical Composition of the Essential Oils of Variegated Pink-Fleshed Lemon (Citrus x limon L. Burm. f.) and their Anti-Infl ammatory and Antimicrobial Activities Dalia Hamdana, Mohamed L. Ashourb, Sri Mulyaningsihc, Assem El-Shazlya, and Michael Winkc,* a Department of Pharmacognosy, Faculty of Pharmacy, Zagazig University, 44519 Zagazig, Egypt b Department of Pharmacognosy, Faculty of Pharmacy, Ain Shams University, Abbassia, 11566 Cairo, Egypt c Institute of Pharmacy and Molecular Biotechnology, Heidelberg University, Im Neuenheimer Feld 364, D-69120 Heidelberg, Germany. Fax: +49 6221 54 4884. E-mail: [email protected] * Author for correspondence and reprint requests Z. Naturforsch. 68 c, 275 − 284 (2013); received December 18, 2012/May 13, 2013 The volatile secondary metabolites of essential oils from fruit peel and leaves of variegated pink-fl eshed lemon (Citrus x limon) were investigated using GLC and GLC-MS (gas-liquid chromatography-mass spectroscopy). Altogether 141 compounds were identifi ed and quanti- fi ed, accounting for 99.59% and 96.33% of the total hydrodistilled peel and leaf oil, respec- tively. Limonene occurred in higher amounts in fruit peel (52.73%) than in leaf oil (29.13%). Neral (12.72%), neryl acetate (8.53%), ρ-menth-1-en-7-al (4.63%), β-pinene (6.35%), and nerol (4.42%) were the most abundant constituents in leaf oil, whereas γ-terpinene (9.88%), β-pinene (7.67%), geranial (4.44%), and neral (3.64%) dominated in the fruit peel oil. The antioxidant, anti-infl ammatory, antitrypanosomal, and antimicrobial activities of the fruit peel essential oil were evaluated. The oil had a low antioxidant activity with an IC50 value of (26.66 ± 2.07) mg/ml as compared to the effi cient antioxidant ascorbic acid [IC50 (16.32 ± 0.16) μg/ml]. The oil moderately inhibited soybean 5-lipoxygenase (5-LOX) with an IC50 value of (32.05 ± 3.91) μg/ml and had moderate antitrypanosomal activity [IC50 (60.90 ± 0.91) μg/ml]. In addition, moderate antimicrobial activities were detected against Gram-positive bacteria (Bacillus subtilis, Staphylococcus capitis, Micrococcus luteus), one Gram-negative bacterium (Pseudomonas fl uorescens), and yeasts (Saccharomyces cerevisiae, Candida parapsilosis). Key words: Pink Lemon, Essential Oil, Bioactivities Introduction out the year, but mainly in late winter, spring, and early summer. The fruit peel has a striped Products from Citrus species (Rutaceae) have green and cream colouration. When fully ripe, been used not only for food and drinks but also the stripes fade and the peel turns yellow with in perfumes, soaps, and many other commodities distinct pink oil glands. The fl esh is light pink at (Crupi et al., 2007; Ladaniya, 2008; Tranchida et full maturity; it has few seeds but the taste would al., 2012). In addition, plants from this genus have be sour (Shamel, 1932). been extensively studied for their antimicrobial, In the context of our chemical and biologi- antioxidant, anti-infl ammatory, antiedemic, car- cal investigation of Citrus species cultivated diovascular, antihyperglycaemic, and antitumour in Egypt (El-Readi et al., 2010; Hamdan et al., properties (Johann et al., 2007; Benavente-Garcia 2010, 2011a, b), essential oils from the fruit peel and Castillo, 2008; Fisher and Phillips, 2008; Shen and leaves of variegated pink-fl eshed lemon et al., 2012; Mencherini et al., 2013; Wesołowska were analysed by high-resolution capillary GLC et al., 2012). and GLC-MS (gas-liquid chromatography-mass Variegated pink-fl eshed Eureka lemon (pink spectroscopy). In order to understand their bio- lemon) is a small fragrant tree (4 − 5 m in height). logical properties, antioxidant, anti-infl ammato- The variegated green and white leaves are of or- ry, antitrypanosomal, and antimicrobial activi- namental interest. Fruits are produced through- ties were assessed. © 2013 Verlag der Zeitschrift für Naturforschung, Tübingen · http://znaturforsch.com 276 D. Hamdan et al. · Essential Oils of Variegated Pink Lemon Material and Methods tioned for GLC. Compounds were identifi ed by Plant material comparing their spectral data and retention indi- ces with Wiley Registry of Mass Spectral Data 8th The fresh ripe fruits and leaves of variegated edition, NIST Mass Spectral Library (December pink-fl eshed lemon (Citrus x limon L. Burm. f.) 2005), and the literature (Adams, 2007; El-Shazly (Rutaceae) were collected on the Research Sta- et al., 2004; El-Shazly and Hussein, 2004). The tion of the Faculty of Agriculture, Benha Univer- identifi ed constituents are listed in the order of sity, Benha, Egypt in March 2009 and 2010. The their elution in Table I. identity of the plant was confi rmed by Dr. B. M. Houlyel, Faculty of Agriculture, Benha Univer- DPPH free radical scavenging activity sity, Benha, Egypt. A voucher specimen of the plant material was deposited at the Department Differently graded dilutions of a stock solution of Pharmacognosy, Faculty of Pharmacy, Zagazig (200 μl in 1 ml MeOH) of the peel essential oil University, Zagazig, Egypt (accession no. P-78, 79). were mixed with 500 μl of 0.2 mM diphenylpicryl- hydrazine (DPPH) (Sigma-Aldrich, Taufkirchen, Germany), and the fi nal volume was brought to Sample preparation 1 ml. The mixtures were vigorously shaken and The fresh fruit peel and leaves (100 g of each) allowed to stand in the dark for 30 min at room were separately subjected to hydrodistillation for temperature. The absorbance was measured by 6 h using a Clevenger-type apparatus; the yields spectrophotometry (LKB Pharmacia Biochrom were 2% and 0.2%, respectively. Both oils were ULTROSPEC PLUS 4054 UV/VIS; Freiburg, dried over anhydrous sodium sulfate and kept in Germany) at 517 nm against a blank sample with- brown vials at 4 °C until further analyses. out DPPH (negative control). The antioxidant ac- tivity of the essential oil, expressed as IC50 (in mg/ GLC and GLC-MS ml), was compared with that of ascorbic acid as a The volatile oil constituents were analysed standard antioxidant (Hamdan et al., 2010). by high-resolution capillary GLC and GLC-MS. Samples of the oil (1 μl each was dissolved in 5-Lipoxygenase inhibition 1 ml n-hexane) were injected (1 μl volume) into Inhibition of 5-lipoxygenase (5-LOX) (Fluka, a gas chromatograph (TRACE GC ULTRA; Buchs, Switzerland) by the essential oil was deter- Thermo Scientifi c, Milan, Italy) under the follow- mined as previously reported (Baylac and Racine, ing conditions: column, RTX-5MS® fused silica 2003) under the following conditions: to 970 μl of capillary (Restek, Bellefonte, PA, USA) equiva- phosphate buffer, pH 9.0, 10 μl 5-LOX (1 mg/ml) lent to DB-5 (30 m x 0.32 mm i. d., 0.25 μm fi lm and 20 μl of twelve different concentrations of the thickness); carrier gas, He (2 ml/min); detector samples (10 − 350 μg/ml) were added and incubat- (FID) temperature, 300 °C; injection temperature, ed at room temperature for 10 min. The enzymat- 250 °C; oven temperature program: initial tem- ic reaction was started by adding 25 μl of 62.5 mM perature of 45 °C, 2 min isothermal, at 4 °C/min sodium linoleate; the absorbance was measured to 300 °C, then 20 min isothermal; split ratio, 1:15. photometrically at 234 nm every 10 s for 3 min. Kovat’s retention indices (RI) were calculated The initial reaction rates were determined from with respect to a set of co-injected standard hy- the slope of the linear part of the curve. Nordihy- drocarbons (C10 – C24). The identifi ed components droguaiaretic acid (NDGA) was used as a posi- were quantifi ed using the GLC “Peak Simple” tive reference compound. software. GLC-MS data were recorded on a Clarus 600 Anti-infective activities gas chromatograph (Shelton, CT, USA) equipped with an identical column used for separation and Antitrypanosomal activity quantifi cation. The capillary column was direct- The mature bloodstream forms of Trypanoso- ly coupled to a quadrupole mass spectrometer ma b. brucei TC221, the causative agent of Na- Clarus 600T. The ionization energy of the mass gana (which can be used as a model for human spectrometer was 70 eV and the split ratio 1:30; sleeping sickness), were grown in Baltz medium all other conditions were identical to those men- supplemented with 20% inactivated foetal bovine D. Hamdan et al. · Essential Oils of Variegated Pink Lemon 277 serum and 1% penicillin/streptomycin. The cells Statistical analysis were incubated in a humidifi ed atmosphere con- All experiments were carried out three times taining 5% CO at 37 °C. 2 unless indicated otherwise in the procedure. Con- Trypanocidal activity was determined using re- tinuous variables were presented as mean ± SD sazurin as a cell proliferation indicator dye as pre- of three individual experiments. The IC was viously described (Baltz et al., 1985; Nibret et al., 50 determined as the drug concentration which re- 2010). Briefl y, the samples were serially diluted sulted in a 50% reduction in cell viability or with the medium in a two-fold fashion to attain inhibition of the biological activity. IC values fi nal concentrations in the range 250 to 3.9 μg/ml 50 were calculated using a four-parameter logistic in 96-well plates. T. b. brucei was seeded into 96 curve (SigmaPlot® 11.0), and all data were sta- wells at a density of 1 · 104 cells per 100 μl of me- tistically evaluated using Student’s t-test and/or dium. The cells were then incubated with samples the Kruskal-Wallis test (GraphPad Prism® 5.01; of various concentrations for 24 h. Ten μl of resa- GraphPad Software, Inc., La Jolla, CA, USA) fol- zurin were added to each well and the mixture lowed by Dunn’s post-hoc multiple comparison incubated for further 24 h.
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