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Phytochemical Analysis, Antioxidant, Anti-Hyperglycemic and Antituberculosis Activities of Phylogenetically Related Garcinia mangostana (Mangosteen) and Garcinia hombroniana (Seashore Mangosteen).

Byline: Nargis Jamila, Naeem Khan, Amir Atlas Khan, Sadiq Noor Khan and Kyong Su Kim

Summary: Species of genus Garcinia belonging to family Clusiaceae are traditionally known for the treatment of ulcer, gonorrhea, leucorrhoea and abdominal pain. This genus is also reported to be a rich source of xanthones, benzophenones, flavonoids, biflavonoids and triterpenes showing significant pharmacological activities. Garcinia mangostana L. (mangosteen) and Garcinia hombroniana Pierre (seashore mangosteen) are evergreen tropical trees grown in Malaysia, Indonesia, Thailand and other tropical countries. The fruits of G. mangostana (queen of fruits), and roots and leaves decoction of G. hombroniana are commonly used for skin allergies, infections after childbirth, trauma and diarrhea. This study aimed to evaluate the bark and fruit extracts of G. mangostana and G. hombroniana for phytochemicals analysis, total phenolic and flavonoid contents, antioxidant, anti-hyperglycemic and antituberculosis activities.

Total phenolic contents were evaluated by Folin-Ciocalteu reagent colorimetric method. For antioxidant activities, radical scavenging assays of 2,2-diphenyl-1-picrylhydrazyl (DPPH) and 2'-azino-bis-3-ethyl benzthiazoline-6-sulphonic acid (ABTS), and ferric ion reducing antioxidant power (FRAP) were used. Anti- hyperglycemic activity was determined using a-glucosidase and a-amylase enzymes. In quantitative phytochemical analysis, the extracts of G. mangostana showed significantly higher content of phenolics [3498.7 uM GAE/g (gallic acid equivalent per gram), ethyl acetate; bark], carbohydrates (14.2 g/100g, aqueous; fruit) and reducing sugars (13.9 g/100g, aqueous; fruit).

Also, in antioxidant activities, G. mangostana showed comparatively high activities with the ethyl acetate extract as the most potent showing IC50 2.78 ug/ml in DPPH, 1.19 ug/ml in ABTS, and 8742.7 uM TE/g in FRAP assays. G. mangostana was also more potent in anti-hyperglycemic properties (IC50 182.9 ug/ml, a- glucosidase, 247.8 ug/ml, a-amylase) compared to G. hombroniana. In antituberculosis study, the ethyl acetate extracts of both plants showed equipotent activity with minimum inhibitory concentration (MIC) of 62.5 ug/ml. Based on the results, it was concluded that the presence of bioactive phytochemicals may be responsible for their traditional uses for treatment of diseases.

Keywords: Garcinia mangostana L., Garcinia hombroniana Pierre, Total phenolic content, Antioxidant, DPPH, a-amylase

Introduction

Garcinia; the largest genus of the Clusiaceae (Guttiferae) family with about 450 species is indigenous to tropical Asia, tropical and southern Africa, Madagascar, North East Australia, West Polynesia and tropical America, and can also be found near seashore, lowland and up to the mountain forests [1]. It is a rich source of xanthones, benzophenones, flavonoids, biflavonoids and triterpenes [2, 3] of significant antimicrobial, anti- inflammatory, antioxidant, anticancer and anti HIV activities [4-6]. Extracts from various parts of these plants are used in the preparation of many herbal medicines for the traditional treatment of abdominal pain, infections, leucorrhoea, chronic ulcer gonorrhea and obesity [7, 8].

Garcinia mangostana L., is a common tropical fruit famed as "queen of tropical fruit" and found in Malaysia, India, Myanmar, Philippines, Sri Lanka and Thailand. It is used in the treatment of inflammations, diarrhea and dysentery. The published literature on its pericarp, whole fruit, stem, leaves, seeds, arils and heartwood revealed that G. mangostana is a rich source of xanthones and their derivatives which are important for antioxidant, antimicrobial, cytotoxic, anti-inflammatory and anti- HIV activities [7-12].

Garcinia hombroniana Pierre, known as seashore mangosteen is endemic to Malaysia, and the Andaman and Nicobar Islands of the North Indian Ocean [13]. Its roots and leaves decoction are used for itching problems and postpartum infections [14, 15]. Previous investigation on the isolation of phytochemicals from its leaves, pericarp and twigs yielded xanthones, benzophenones flavonoids, biflavonoids and triterpenes showing antioxidant, antimicrobial, cytotoxic and anticholinesterase activeties [5, 16-20].

From the phylogenetic and Internal Transcribed Spacers (ITS) sequence analyses, G. mangostana is reported to be allopolyploid, and is considered to be derived from the hybridization of G. hombroniana and G. malaccensis. In addition, Richard (1990) [21] reported that G. mangostana is intermediate between these two species with 13 identical morphological characters (flowering time, latex colour, petal colour, stigma, stigma surface, stigma lobes, stigma diameter, stamen mass, female flower, fruit shape, fruit surface and fruit colour). Among these characters, four; latex colour, petal colour, sessile stigma and fruit colour of G. mangostana were similar to G. malaccensis, four; smooth stigma surface, stamen mass clearly lobed, fruit globose and surface smooth to G. hombroniana whereas the remaining five characters were found to be fallen between these two species. Richard (1990) suggested G. hombroniana as a mother and a wild G. malaccensis as a father of G. mangostana (Fig. 1).

However, the ITS sequence analysis of some Garcinia species revealed that G. mangostana is more closely related to G. malaccensis than to G. hombroniana [22]. According to Yapwattanaphun and S. Subhadrabandhu [23], fresh fruit of G. hombroniana is similar to small mangosteen and has a taste like a peach but the pulp is somewhat sour.

From the studies of phytochemical investigations on different Garcinia species, it is found that G. mangostana and G. hombroniana are significantly different in phytochemistry from other species [24]. Considering the similarities and pharmacological importance of both G. mangostana and G. hombroniana, this study was aimed to evaluate, quantify and compare the phytochemicals such as phenols, flavonoids, tannins, carbohydrates, reducing sugars, alkaloids, terpenoids and steroids, and to evaluate the antioxidant, anti-hyperglycemic and antituberculosis activities of the bark and fruit extracts of G. mangostana and G. hombroniana.

Experimental

The sampling for this study includes G. hombroniana and G. mangostana bark and fruit. The bark of these two species and the fruit of G. hombroniana were collected from Penang Botanical Garden, Penang, Malaysia with voucher specimens PBGK12 and PBGKGM-12, respectively. The fruit of G. mangostana was purchased from local Super Market (TESCO) of Malaysia.

Instruments and Chemicals

Chemicals for phytochemical analysis and antioxidant activities such as Follin Ciocalteu reagent, glucose, arsenomolybdate reagent, potassium ferrocyanide, DPPH (2,2-diphenyl-1-picrylhydrazyl), ABTS (2'-azino-bis-3-ethyl benzthiazoline-6- sulphonic acid), TPTZ (2,4,6-tripyridyl-s-triazine), tannic acid, trolox, ascorbic acid, gallic acid, rutin and quercetin were purchased from Sigma-Aldrich (Steinheim, Germany) and Merck (Darmstadt, Germany). Chemicals of the antihyperglycemic activities; soluble starch, porcine pancreatic a- amylase (PPA), a-glucosidase and acarbose were purchased from Sigma Aldrich, USA. M. tuberculosis H38Rv was purchased from American Type Culture Collection (Rockville, USA). All the chemicals used in extraction and isolation were of analytical grade.

Extraction and Isolation

The air dried ground bark (1 kg) each of G. hombroniana and G. mangostana were defatted using Soxhlet extractor with n-hexane at 40 degC. The defatted materials were then extracted with dichloromethane, ethyl acetate methanol and water by separatory funnel. The filtered extracts were evaporated to dryness using a rotary evaporator at 40 degC. From fruits, extraction was carried out by maceration in water to get aqueous extracts. The extracts thus obtained were analyzed for various phenolic compounds, flavonoids, tannins, saponins, carbohydrates and reducing sugar contents. In addition, antioxidant, anti-hyperglycemic and antituberculosis activities were also evaluated.

Phytochemical Screening

Phytochemical screening of terpenoids, phytosterols, carbohydrates, glycosides, phenolics, flavonoids, saponins tannins and alkaloids in n- hexane, dichloromethane, ethyl acetate, methanol and aqueous extracts of bark, and aqueous extract of fruits were qualitatively screened according to the procedures of Sofowora (1993) [25]. Quantitative determination of total phenolic, flavonoids and tannins contents was also carried out by spectroscopic calorimetric methods. The total phenolic contents of the extracts were evaluated by method of Thaipong et al. (2006) [26]. Results were expressed as umol gallic acid equivalent (uM GAE) per g of extract. Total flavonoid contents were determined according to Zhishen et al. (1999) method [27]. Rutin and quercetin were used as standards and the results represented as umol rutin equivalent (uM RE/g) and umol quercetin equivalent (uM QE/g) per gram of extract.

The total carbohydrate contents were estimated using standard Anthrone method [28] and the contents were calculated from the standard graph curve of glucose. The contents of reducing sugars were analyzed by Somogyi method [29] and calculated from the standard (glucose) graph curve drawn. For tannin contents determination, 100 mg of the samples were dissolved in 10 ml of distilled water in a plastic bottle. These were shaken in a mechanical shaker for 1 h. Then, the samples were filtered and transferred to conical flasks. Then, 5 ml of the samples were pipetted out in a tube from the conical flasks and 3 ml of 0.1 N FeCl3 in 0.1 N HCl and 0.008 M potassium ferrocyanide was added. A blank was prepared by mixing 3 ml of 0.1 N FeCl3 and 10 ml of distilled water. Tannic acid was used as a standard. After 5 min, the absorbance of the samples and blank was recorded at 120 nm. The contents of tannins were calculated as g/100g.

Evaluation of Antioxidant, Antihyperglycemic and Antituberculosis Activities

Antioxidant activities of the extracts were evaluated by free radical scavenging of DPPH, ABTS and ferric ion reducing antioxidant power (FRAP) assays [26]. Gallic acid, ascorbic acid and trolox were used as standards. The scavenging capacities of the DPPH and ABTS radicals were calculated by the following equation.

% Scavenging = [(1-(Asample/Acontrol)] x 100

The results of DPPH and ABTS inhibition were represented in terms of IC50 and uM TE/g of extract while that of FRAP assay were represented as uM TE/g.

The anti-hyperglycemic activity of the fruit extracts of G. mangostana and G. hombroniana were determined using two enzymes; a-glucosidase and a- amylase. The a-glucosidase inhibitory activity was performed according to Matsui et al. [30] whereas a- amylase inhibitory activity of the extracts was analyzed according to Xiao et al. [31] microplate method. The enzyme activities were expressed as % inhibition and IC50 values as follow;

% relative enzyme activity = enzyme activity of test/enzyme activity of control)*100

% inhibition in the a-amylase activity = 100 - % relative enzyme activity)

Antituberculosis activity was evaluated against M. tuberculosis H37Rv according to the method of Collins's BACTEC 460 system [32].

Statistical Analyses

All data were analyzed and expressed as means +- standard deviation of three replicates (n = 3). The differences between the assayed values were analyzed using One-Way Analysis of Variance (ANOVA), followed by Tukey's HSD Test at 95% and 99% confidence interval with SPSS software, version 19.0 (SPSS Inc., Chicago, USA). IC50 values were calculated using GraphPad Prism 6.02 (GraphPad Software Inc., La Jolla, USA).

Results and Discussion

Phytochemicals such as phenolic acids, flavonoids, xanthones, benzophenones, tannins, lignans, alkaloids and triterpenoids are generally assumed to be the active secondary and non-nutritive constituents contributing to protective and pharmacological effects. In this investigation, the well-known fruit of G. mangostana and less known fruit of G. hombroniana, and their barks were analyzed for phytochemicals using simple laboratory tests as well as UV instrumental calorimetric spectroscopic determination. In both of the species, alkaloids, carbohydrates, glycosides, terpenes, phytosterols, phenolics, flavonoids and tannins were detected (Table-1). G. mangostana extracts were found to be richer in phenolics and tannins whereas G. hombroniana extracts were rich in flavonoids, terpenoids and phytosterols. Ethyl acetate, methanol and water extracts showed abundance of the polyphenolic constituents, whereas n-hexane and dichloromethane extracts were rich in triterpenoids and phytosterols.

Plant phenolics are pharmacologically important constituents having antioxidant potential due to the reducing abilities of their hydroxyl groups. The hydroxyl groups donate hydrogen to free radicals and thus, prevent the free radical chain reactions. Generally, total phenolic contents are estimated by Folin-Ciocalteu method, chromatographic response function and reversed phase HPLC methods. In Folin-Ciocalteu method, reduced molecules are oxidized by a mixture of oxidants phosphotungstic and phosphomolybdic acids [33]. In present study, the bark and fruit extracts of G. mangostana and G. hombroniana were evaluated for their phenolic contents and detailed results are summarized in Fig. 2. Among the bark extracts, ethyl acetate extract of G. mangostana showed the highest contents of phenolics with 3498.7uM GAE/g followed by methanol extract. Among G. hombroniana extracts, ethyl acetate and methanol extracts showed closely similar phenolic contents.

On the other hand, the aqueous extracts of fruit of G. mangostana and G. hombroniana comparatively showed lower phenolics. Overall, the quantitative evaluation of total phenolic contents of the extracts of these two plants showed that G. mangostana is richer in phenolics than G. hombroniana. The results of total phenolic contents for fruit extracts of both the species coincided with the report published by Jantan et al. [34] in which the phenolics of G. mangostana fruit were higher than that of G. hombroniana. On the other hand, the study of Acuna et al. [24] showed that the lyophilized methanolic extract of G. hombroniana fruit had higher total phenolic contents than that of G. mangostana.

The most diverse phenolics are the flavonoids which have long been recognized as potent antioxidants. Therefore, it is important to determine total flavonoid contents of medicinal plants. In current study, the total flavonoid contents of the extracts of G. mangostana and G. hombroniana were evaluated by aluminium chloride colorimetric method in which a keto group (C-4), hydroxyl groups at C-3 and C-5 or the ortho dihydroxyl groups in the A or B ring of flavonoids form a pink complex with high electropositive aluminium (Al3+) from AlCl3, and the complex is spectrophotometrically measured at 510 nm. The results of total flavonoid contents (Fig. 3A and B) showed that the extracts of G. mangostana had comparatively lower contents of flavonoids than G. hombroniana.

Among the extracts of G. hombroniana analyzed, ethyl acetate bark extract exhibited the highest content of flavonoids followed by its methanolic bark extract. The aqueous extracts of fruits of G. mangostana and G. hombroniana showed total flavonoids content of 1938.6 uM RE/g and 2599.4 uM QE/g, respectively.

Table-1 Phytochemical screening of the bark and fruit extracts of G. mangostana (GM) and G. hombroniana (GH)

###Extract###n-hexane###Dichloromethane###Ethyl acetate###Methanol###Aqueous###Aqueous (Fruit)

###Phytochemical

###GM###GH###GM###GH###GM###GH###GM###GH###GM###GH###GM###GH

###Phenols

###Ferric chloride test###-###-###-###+###+++###+++###+++###+++###+++###+++###+++###+++

###Lead acetate test###-###-###-###+###+++###+++###+++###+++###+++###+++###+++###+++

###Liebermann test###-###-###-###+###+++###+++###+++###+++###+++###+++###+++###+++

###Flavonoids

###Alkaline reagent (NH4OH, NaOH)###-###-###-###-###+++###+++###+++###+++###+++###+++###+++###+++

###Shinodas test###-###-###-###-###+++###+++###+++###+++###+++###+++###+++###+++

###Carbohydrate and Reducing sugar

###Fehling test###-###-###-###-###++###++###+++###+++###+++###+++###+++###+++

###Benedicts test###-###-###-###-###++###++###+++###+++###+++###+++###+++###+++

###Molisch test###-###-###-###-###++###++###+++###+++###+++###+++###+++###+++

###Alurone grains###-###-###-###-###++###++###+++###+++###+++###+++###+++###+++

###Tannins

###Ferric chloride test###-###-###-###-###-###-###-###-###+++###+++###+++###+++

###Lead acetate test###-###-###-###-###-###-###-###-###+++###+++###+++###+++

###Alkaloids

###Dragendorff's test###-###-###-###-###-###-###-###-###-###-###-###-

###Wagner's test###-###-###-###-###-###-###-###-###-###-###-###-

###Mayer's test###-###-###-###-###-###-###-###-###-###-###-###-

###Terpenoids and Steroids

###Liebermann Burchard test###+###+###+++###+++###+++###++###-###-###-###-###-###-

###Salkowski test###+###+###+++###+++###+++###++###-###-###-###-###-###-

###Protein and amino acids

###Millons test###-###-###-###-###-###-###-###-###-###-###-###-

###Biurette test###-###-###-###-###-###-###-###-###-###-###-###-

###Ninhydrin test###-###-###-###-###-###-###-###-###-###-###-###-

###Phlobatannins

###-###-###-###-###-###-###-###-###-###-###-###-

Table-2: Contents of carbohydrates, reducing sugars and tannins, and antioxidant activities of the extracts of G. mangostana and G. hombroniana

###Tannins

Pytochemical###Carbohydrates (g/100g)###Reducing sugars (g/100g)

###(g/100g)

###G.###G.

###Extracts###G. mangostana###G. hombroniana###G. mangostana###G. mangostana

###hombroniana###hombroniana*

###n-hexane###ND###ND###ND###ND###ND###ND

Dichloromethane###ND###ND###ND###ND###ND###ND

###Ethyl acetate###2.3a###1.7a###2.1a###2.08a###ND###ND

###Methanol###3.8b###3.3b###3.5b###3.1b###0.09a###0.06a

###Aqueous###9.9c###8.7c###8.5c###7.3c###0.16b###0.10a

Aqueous (Fruit)###14.2d###9.1c###13.9d###8.4d###0.23b###0.19b

Antioxidant activity###DPPH###ABTS###FRAP

###G. mangostana###G. hombroniana###G. mangostana###G. hombroniana###G. mangostana###G. hombroniana

###IC50###uM TE/g###IC50###uM TE/g###IC50###uM TE/g###IC50###uM TE/g###uM TE/g###uM TE/g

###n-hexane###30.0g###1937.9+-20.7a###>100###100###100###<15###~1000###100###<500###21.3f###100###<15###3169.3a+-53.1a### methanol > water > dichloromethane > n-hexane. The extracts of G. mangostana were more potent than that of G. hombroniana. Generally, compared to G. hombroniana, the bark and fruit extracts of G. mangostana have higher concentrations of the phytochemicals and more potent antioxidative properties.

The a-glucosidase inhibitory effect showed that an aqueous fruit extract of G. mangostana has higher inhibitory activity (IC50 = 182.9 ug/ml) than the standard reference acarbose (IC50 = 2561.7 ug/ml) whereas an inhibitory effect on a-amylase was found to be with IC50 of 247.8 ug/ml as compared to standard, acarbose (IC50 of 11.7 ug/ml). G. hombroniana aqueous extract showed comparatively lower inhibition of a-glucosidase (IC50 = 391.7 ug/ml) and a-amylase (IC50 = 474.2 ug/ml) than the aqueous extract of G. mangostana.

In antituberculosis studies, the ethyl acetate bark extracts of both the plants showed good inhibition with the MIC of 62.5 ug/ml, followed by aqueous extract of fruit of G. mangostana with MIC of 250 ug/ml compared with the reference standard, gentamicin ( MIC = 12.5 ug/ml). The other extracts did not show inhibition of H37Rv.

Conclusions

The bark and fruit extracts of G. mangostana and G. hombroniana were enriched with phenolic compounds analyzed by common chemical tests and quantitative spectroscopic determination. G. mangostana was richer in phenolic contents whereas the flavonoid contents were abundant in the ethyl acetate and methanol bark extracts of G. hombroniana. Both of the plants also displayed promising antioxidant activities by DPPH, ABTS and FRAP assays in which it was found that compared to G. hombroniana, G. mangostana extracts have stronger antioxidative properties. Similarly, in anti- hyperglycaemic activity, aqueous fruit extract of G. mangostana showed stronger inhibition than that of G. hombroniana. In addition, in anti-tuberculosis activity, the ethyl acetate extracts of G. mangostana and G. hombroniana were equipotent. However, the aqueous fruit extract of G. mangostana showed moderate inhibition of H37Rv.

Thus, from the results, it could be concluded that the significant and strong inhibition of free radicals, enzymes and H37Rv by G. mangostana and G. hombroniana might be due their high contents of phenolic compounds.

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Author:Jamila, Nargis; Khan, Naeem; Khan, Amir Atlas; Khan, Sadiq Noor; Kim, Kyong Su
Publication:Journal of the Chemical Society of Pakistan
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Geographic Code:9PAKI
Date:Dec 31, 2016
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