Antidiabetic and antioxidant properties of Ficus deltoidea fruit extracts and fractions

BMC Complementary and Alternative Medicine

Norhaniza Aminudin¹  Azlina Abdul Aziz²  Hasni Misbah³ 

[1]Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603, Kuala Lumpur, Malaysia

[2]University Malaya Centre for Proteomics Research (UMCPR), Medical Biotechnology Laboratory, Faculty of Medicine, University of Malaya, 50603, Kuala Lumpur, Malaysia

[3]Department of Molecular Medicine, Faculty of Medicine, University of Malaya, 50603, Kuala Lumpur, Malaysia

关键词: SELDI-TOF MS;    SDS-PAGE;    Phenolic;    Ficus deltoidea;    Diabetes;    Antioxidant;   

Others  :  1229905
DOI  :  10.1186/1472-6882-13-118

 received in 2013-02-08, accepted in 2013-05-23,  发布年份 2013

【 摘 要 】

Background

Diabetes is a serious metabolic disorder affecting the metabolism of carbohydrate, protein and fat. A number of studies have shown that diabetes mellitus is associated with oxidative stress, leading to an increased production of reactive oxygen species. Ficus deltoidea is traditionally used in Malaysia for regulating blood sugar, blood pressure and cholesterol levels. The use of F. deltoidea as an alternative medicinal herb is increasingly gaining popularity with the sale of F. deltoidea tea bags and capsules in the local market. The present study was undertaken to investigate the antidiabetic and antioxidant activities of the fruits from different varieties of F. deltoidea, employing in vitro methods.

Method

Two fruit varieties of F. deltoidea (var. angustifolia (SF) and var. kunstleri (BF)) were extracted separately using double-distilled water. The resulting aqueous extracts were partitioned using ethyl acetate to obtain the ethyl acetate and water fractions. The crude aqueous extracts and the corresponding fractions were evaluated for their phenolic, flavonoid, sugar and protein contents. Protein profiling of the extracts and fractions were also carried out by means of SDS-PAGE and SELDI-TOF MS. Antidiabetic activities were assessed based on the ability of the samples to inhibit yeast and mammalian α-glucosidase as well as α-amylase. Antioxidant capacities were examined by measuring the ability of the samples to reduce ferric ions and to scavenge DPPH, superoxide anion, ABTS and nitric oxide radicals.

Results

The crude extracts and fractions of SF and BF inhibited both yeast and rat intestinal α-glucosidases in a dose-dependent manner, but did not inhibit porcine pancreatic α-amylase. The water fraction of BF showed the highest percentage of α-glucosidase inhibition while having the highest amount of protein (73.33 ± 4.99 μg/mg fraction). All the extracts and fractions exhibited antioxidant activities, with SF crude extract showing the highest antioxidant activity and phenolic content (121.62 ± 4.86 mg/g extract). Fractionation of the crude extracts resulted in loss of antioxidant activities. There was no positive correlation between phenolic and flavonoid content with α-glucosidase inhibitory activities. However, phenolic content correlated well with antioxidant activities of the crude extracts but not with the fractions.

Conclusions

The antioxidant activities of the fruits of F. deltoidea might be asserted by the phenolic content but other polar plant components were possibly involved in the antidiabetic properties. The study of these compounds having both antihyperglycemic and antioxidant activities may provide a new approach in the treatment of diabetes mellitus.

【 授权许可】

   
2013 Misbah et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Teixeira CC, Rava CA, Da-Silva PM, Melchior R, Argenta R, Anselmi F, Almeida CR, Fuchs FD: Absence of antihyperglycemic effect of jambolan in experimental and clinical models. J Ethnopharmacol 2000, 71:343-347.
• [2]Youn J, Park H, Cho K: Anti-hyperglycaemic activity of Commelina communis L.: inhibition of α-glucosidase. Diabetic Res Clin Prac 2004, 665:S149-S155.
• [3]Saito N, Sakai H, Sekihara H, Yajima Y: Effect of α-glucosidase inhibitor (voglibose), in combination with sulphonylureas, on glycaemic control in type 2 diabetes patients. J Int Med Res 1998, 26:219-232.
• [4]Bhandari MR, Jong-Anurakkhun N, Hong G, Kawabata J: α-glucosidase and α-amylase inhibitory activities of Napalese medicinal herb Pakhanbhed (Bergenia ciliata, Haw). Food Chem 2008, 106:247-252.
• [5]Rhabasa-Lhoret R, Chiasson JL: Glucosidase inhibitors. In International Textbook of Diabetes Mellitus. 3rd edition. Edited by Defronzo RA, Ferrannini E, Keen H, Zimmet P. UK: John Wiley & Sons Ltd; 2004. 1: 901–914
• [6]Bonnefont-Rousselot D, Bastard JP, Jaudon MC, Delattre J: Consequences of the diabetic status on the oxidant/antioxidant balance. Diabetes Metab 2000, 26:163-176.
• [7]Ceriello A: Oxidative stress and diabetes-associated complications. Endocr Pract 2006, 12:60-62.
• [8]Rains JL, Jain SK: Oxidative stress, insulin signaling and diabetes. Free Radic Biol Med 2011, 50:567-575.
• [9]Pasupathi P, Rao YY, Faook J, Saravanan G, Bakthavathsalam G: Oxidative stress and cardiac biomarkers in patients with acute myocardial infarction. Eur J Sci Res 2009, 27:275-285.
• [10]Calabrese V, Mancuso C, Sapienza M, Puleo E, Calafato S, Cornelius C, Finocchiaro M, Mangiameli A, Di-Mauro M, Giuffrida Stella AM, Castellino P: Oxidative stress and cellular stress response in diabetic nephropathy. Cell Stress Chaperones 2007, 12:299-306.
• [11]Grover JK, Yadav S, Vats V: Medicinal plants of India with antidiabetic potential. J Ethnopharmacol 2002, 81:81-100.
• [12]Manickam M, Ramanathan M, Jahromi MA, Chansouria JP, Ray AB: Antihyperglycemic activity of phenolics from Pterocarpus marsupium. J Nat Prod 1997, 60:609-610.
• [13]Panda S, Kar A: Apigenin (4′,5,7-trihydroxyflavone) regulates hyperglycaemia, thyroid dysfunction and lipid peroxidation in alloxan-induced diabetic mice. J Pharm Pharmacol 2007, 59:1543-1548.
• [14]Yoshikawa M, Wang T, Morikawa T, Xie H, Matsuda H: Bioactive Constituents from Chinese Natural Medicines XXIV Hypoglycemic Effects of Sinocrassula indica in Sugar-Loaded Rats and Genetically Diabetic KK-Ay Mice and Structures of New Acylated Flavonol Glycosides, Sinocrassosides A1, A2, B1, and B2. Chem Pharm Bull 2007, 55:1308-1315.
• [15]Dineshkumar B, Mitra A, Mahadevappa M: Antidiabetic and hypolipidemic effects of mahanimbine (carbazole alkaloid) from murraya koenigii (rutaceae) leaves. Int J Phytomed 2010, 2:22-30.
• [16]Sharma B, Salunke R, Balomajumder C, Daniel S, Roy P: Anti-diabetic potential of alkaloid rich fraction from Capparis decidua on diabetic mice. J Ethnopharmacol 2010, 127:457-462.
• [17]Tan MJ, Ye JM, Turner N, Hohnen-Behrens C, Ke CQ, Tang CP, Chen T, Weiss HC, Gesing ER, Rowland A, James DE, Ye Y: Antidiabetic activities of triterpenoids isolated from bitter melon associated with activation of the AMPK pathway. Chem Biol 2008, 15:263-273.
• [18]Contreras C, Roman R, Perez C, Alarcon F, Zavala M, Perez S: Hypoglycemic activity of a new carbohydrate isolated from the roots of Psacalium peltatum. Chem Pharm Bull 2005, 53:1408-1410.
• [19]Farsi E, Shafaei A, Sook YH, Khadeer Ahamed BM, Mun FY, Idress HA, Zaini MA, Ismail Z: Correlation between enzymes inhibitory effects and antioxidant activities of standardized fractions of methanolic extract obtained from Ficus deltoidea leaves. Afr J Biotechnol 2011, 10:15184-15194.
• [20]Choo CY, Sulong NY, Man F, Wong TW: Vitexin and isovitexin from the Leaves of Ficus deltoidea with in-vivo α-glucosidase inhibition. J Ethnopharmacol 2012, 142:776-781.
• [21]Omar MH, Mullen W, Crozier A: Identification of proanthocyanidin dimers and trimers, flavone C-Glycosides, and antioxidants in Ficus deltoidea, a Malaysian herbal tea. J Agric Food Chem 2011, 59:1363-1369.
• [22]Adam Z, Khamis S, Ismail A, Hamid M: Ficus deltoidea: A potential alternative medicine for diabetes mellitus. Evidence-Based Complementary Altern Med 2012, 201(2):632763.
• [23]Armaghan S, Elham F, Khadeer BMH, Jamshid MAS, Idress HA, Ismail Z, Zaini MA: Evaluation of toxicological and standardization parameter and phytochemical investigation of Ficus deltoidea. Am J Biochem Mol Biol 2011, 1:237-243.
• [24]Adam Z, Hamid M, Ismail A, Khamis S: Effect of Ficus deltoidea aqueous extract on blood glucose level in normal and mild diabetic rats. Malaysian J Health Sci 2007, 5:9-16.
• [25]Aminudin N, Chung YS, Eue SC, Kang IN, Lee R: Blood glucose lowering effect of Ficus deltoidea aqueous extract. Malaysian J Sci 2007, 26:73-78.
• [26]Adam Z, Khamis S, Ismail A, Hamid M: Inhibitory properties of Ficus deltoidea on α-glucosidase activity. Res J Med Plant 2010, 4:61-75.
• [27]Sulaiman MR, Hussain MK, Zakaria ZA: Evaluation of the antinociceptive activity of Ficus deltoidea aqueous extract. Fitoterapia 2008, 79:557-561.
• [28]Siti Fatimah Zahra MA, Mahmood AA, Hapipah MA, Suzita MN, Salmah I: Anti-ulcerogenic activity of aqueous extract of Ficus deltoidea against ethanol-induced gastric mucosal injury in rats. Res J Med Sci 2009, 3:42-46.
• [29]Hakiman M, Maziah M: Non enzymatic and enzymatic antioxidant activities in aqueous extract of different Ficus deltoidea accessions. J Med Plants Res 2009, 3:120-131.
• [30]Abdullah Z, Hussain K, Zhari I, Rasadah MA, Mazura P, Jamaludin F, Sahdan R: Evaluation of extracts of leaf of three Ficus deltoidea varieties for antioxidant activities and secondary metabolites. Pharmacogn Res 2009, 1:216-223.
• [31]Zakaria ZA, Hussain MK, Mohamad AS, Abdullah FC, Sulaiman MR: Anti-inflammatory activity of the aqueous extract of Ficus deltoidea. Biol Res Nurs 2012, 14:90-97.
• [32]Oh MJ, Abdul Hamid M, Ngadiran S, Seo YK, Sarmidi MR, Park CS: Ficus deltoidea (Mas cotek) extract exerted anti-melanogenic activity by preventing tyrosinase activity in vitro and by suppressing tyrosinase gene expression in B16F1 melanoma cells. Arch Dermatol Res 2011, 303:161-170.
• [33]Singleton UL, Rossi J: Colorimetry of total phenolics with phosphomolybdic-posphotungustic acid reagent. Am J Enol Vit 1965, 16:144.
• [34]DuBois MK, Gils JK, Hanniton PA, Robes , Smith F: Use of phenol reagent for the determination of total sugar. Anal Chem 1956, 28:350.
• [35]Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
• [36]Braca A, Tommasi ND, Bari LD, Pizza C, Politi M, Morelli I: Antioxidant principles from Bauhinia terapotensis. J Nat Prod 2001, 64:892-895.
• [37]Benzie IFF, Strain JJ: Ferric reducing ability of plasma (FRAP) as a measure of antioxidant power: the FRAP assay. Anal Biochem 1996, 239:70-76.
• [38]Nishikimi M, Appaji N, Yagi K: The occurrence of superoxide anion in the reaction of reduced phenazine methosulfate and molecular oxygen. Biochem Biophys Res Commun 1972, 46:849-854.
• [39]Sindhu RK, Griffin DH, Walton DC: Abscisic aldehyde is an intermediate in the enzymatic conversion of xanthoxin to abscisic acid in Phaseolus vulgaris L leaves. Plant Physiol 1990, 93:689-694.
• [40]Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
• [41]Lau BF, Aminudin N, Abdullah N: Comparative SELDI-TOF-MS profiling of low-molecular-mass proteins from Lignosus rhinocerus (Cooke) Ryvarden grown under stirred and static conditions of liquid fermentation. J Microbiol Methods 2011, 87:56-63.
• [42]Anam K, Widharna RM, Kusrini D: α-glucosidase inhibitor activity of Terminalia species. Int J Pharmacol 2009, 5:277-280.
• [43]Momo CEN, Fuh Ngwa A, Dongmo GIF, Oben JE: Antioxidant properties and α amylase inhibition of Terminalia superba Albizia sp., Cola nitida, Cola odorata and Harungana madagascarensis used in the management of diabetes in Cameroon. J Health Sci 2009, 55:732-738.
• [44]Oki T, Matsui O, Osajima Y: Inhibitory effect of alpha-glucosidase inhibitors varies according to its origin. J Agric Food Chem 1999, 47:550-553.
• [45]Shai LJ, Masoko P, Mokgotho MP, Magano SR, Mogale AM: Yeast alpha glucosidase inhibitory and antioxidant activities of six medicinal plants collected in Phalaborwa, South Africa. South Afr J Bot 2010, 76:465-470.
• [46]Kim JS, Kwon CS, Son KH: Inhibition of alpha-glucosidase and amylase by luteolin, a flavonoid. Biosci Biotechnol Biochem 2000, 64:2458-2461.
• [47]Kim YM, Wang MH, Rhee HI: A novel alpha-glucosidase inhibitor from pine bark. Carbohydr Res 2004, 339:715-717.
• [48]Schafer A, Hogger P: Oligomeric procyanidins of French maritime pine bark extract (Pycnogenol®) effectively inhibit α-glucosidase. Diabetes Res Clin Pract 2007, 77:41-46.
• [49]Iwai K: Antidiabetic and antioxidant effects of polyphenols in brown alga Ecklonia stolonifera in genetically diabetic KK-Ay mice. Plant Foods Hum Nutr 2008, 63:163-169.
• [50]Gao H, Kawabata J: α-glucosidase inhibition of 6-hydroxyflavones. Part 3: synthesis and evaluation of 2,3,4-trihydroxybenzoyl-containing flavonoid analogs and 6-aminoflavones as α-glucosidase inhibitors. Bioorg Med Chem 2005, 13:1661-1671.
• [51]Rahimi R, Nikfar S, Larijani B, Abdollahi M: A review on the role of antioxidants in the management of diabetes and its complications. Biomed Pharmacother 2005, 59:365-373.
• [52]Tchinda AT, Tchuendem MH, Khan SN, Omar I, Ngandeu F, Nkeng PEA, Choudhary IM: Antioxidant activity of the crude extract of the fruits of Pycnanthus angolensis and α-glucosidase inhibitory activity of its constituents. Pharmacologyonline 2008, 1:422-431.
• [53]Yao Y, Sang W, Zhou M, Ren G: Antioxidant and alpha-glucosidase inhibitory activity of colored grains in China. J Agric Food Chem 2010, 58:770-774.
• [54]Wu N, Fu K, Fu YJ, Zu YG, Chang FR, Chen YH, Liu XL, Kong Y, Liu W, Gu CB: Antioxidant Activities of Extracts and Main Components of Pigeonpea [Cajanus cajan (L) Millsp] Leaves. Molecules 2009, 14:1032-1043.
• [55]Jain DP, Pancholi SS, Patel R: Synergistic antioxidant activity of green tea with some herbs. J Adv Pharm Technol Res 2011, 2:177-183.
• [56]Carpenter A, Siggia S, Carter S: Separation and/or Concentration of phenolic materials from dilute aqueous solutions. Anal Chem 1976, 48:225-228.
• [57]Azevedo CR, Maciel FM, Silva LB, Ferreira AT, Da-Cunha M, Machado OL, Fernandes KV, Oliveira AE, Xavier-Filho J: Isolation and intracellular localization of insulin-like proteins from leaves of Bauhinia variegate. Braz J Med Biol Res 2006, 39:1435-1444.
• [58]Yuan X, Gu X, Tang J: Purification and characterisation of a hypoglycemic peptide from Momordica Charantia L. Var abbreviata Ser. Food Chem 2008, 111:415-420.
• [59]Fenglin L, Qingwang L, Dawei G, Yong P, Caining F: Preparation and antidiabetic activity of polysaccharide from Portulaca oleracea L. Afr J Biotechnol 2009, 8:569-573.
• [60]Kim HM, Kang JS, Kim JY, Park SK, Kim HS, Lee YJ, Yun J, Hong JT, Kim Y, Han SB: Evaluation of antidiabetic activity of polysaccharide isolated from Phellinus linteus in non-obese diabetic mouse. Int Immunopharmacol 2010, 10:72-78.
• [61]Paul A, Raychaudhuri SS: Medicinal uses and molecular identification of two Momordica charantia varieties - a review. Electron J Biol 2010, 6:43-51.
• [62]Kim H, Choi H, Moon J, Kim Y, Mosaddik A, Cho S: Comparative antioxidant and antiproliferative activities of red and white pitayas and their correlation with flavonoid and polyphenol content. J Food Sci 2010, 76:C38-C45.
• [63]Razab A, Abdul Aziz A: Antioxidants from tropical herbs. Nat Prod Commun 2010, 5:441-445.
• [64]Sariburun E, Sahin S, Demir C, Turkben C, Uylaser V: Phenolic content and antioxidant activity of raspberry and blackberry cultivars. J Food Sci 2010, 75:C328-C335.
• [65]Papale M, Pedicillo MC, Thatcher BJ, Di-Paolo S, Lo Muzio L, Bufo P, Rocchetti MT, Centra M, Ranieri E, Gesualdo L: Urinary profiling by SELDITOF/MS: monitoring of the critical steps in sample collection, handling and analysis. J Chromatogr B 2007, 856:205-213.