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Comparison of Antidiabetic Potential of (+) and (−)-Hopeaphenol, a Pair Of RSC Advances View Article Online COMMUNICATION View Journal | View Issue Comparison of antidiabetic potential of (+) and (À)-hopeaphenol, a pair of enantiomers isolated Cite this: RSC Adv.,2016,6, 77075 from Ampelocissus indica (L.) and Vateria indica Linn., with respect to inhibition of digestive enzymes and induction of glucose uptake in L6 Received 2nd June 2016 myotubes† Accepted 25th July 2016 P. Sasikumar,a B. Prabha,a T. R. Reshmitha,bc Sheeba Veluthoor,d A. K. Pradeep,e DOI: 10.1039/c6ra14334b K. R. Rohit,a B. P. Dhanya,ab V. V. Sivan,f M. M. Jithin,f N. Anil Kumar,f I. G. Shibi,*g bc ab www.rsc.org/advances P. Nisha* and K. V. Radhakrishnan* The remarkable a-glucosidase inhibition exhibited by the acetone Creative Commons Attribution 3.0 Unported Licence. 1. Introduction extract of the rhizome of Ampelocissus indica (L.) and stem bark of Vateria indica m À1 Linn. (IC50 23.2 and 1.47 gmL )encouragedusto Polyphenols, constituting oligomers of resveratrol ranging from isolate the phytochemicals from these plants. (+) and (À)-hope- dimers to octamers are found abundantly in plants belonging to aphenol (1)and(2) were isolated from A. indica (L.) and V. indica Linn. the Vitaceae, Dipterocarpaceae, Leguminosae and Cyperaceae Æ respectively. Compounds 1 and 2 displayed IC50 values of 21.21 families. These naturally occurring polyphenols are common 0.987 and 9.47 Æ 0.967 mMinana-glucosidase inhibitory assay. The building blocks of a large number of complex natural products effect of glucose uptake performed by 2-NBDG in L6 rat skeletal in terms of structure and stereochemistry. The biological muscle cells using flow cytometry (BD FACS Aria II, USA) showed activities such as anti-bacterial,1 anti-HIV,2 anti-inammatory,3,4 This article is licensed under a potent glucose uptake by (+) and (À)-hopeaphenol of 31% and 26.4%, and anti-proliferative property5 make resveratrol a potential respectively. The data from an MTT cell viability assay revealed that the drug candidate. The evaluation of the mechanism underlying compounds are not toxic to the cells up to 200 mM. Molecular docking the biological activities of resveratrol oligomers would provide studies show that the compounds bind effectively to the active sites of Open Access Article. Published on 03 August 2016. Downloaded 12/05/2017 10:33:03. a substantial clue in the development of new drug leads. Due to the proteins 1BVN, 3A4A and 3AJ7, which supported the observed the pharmaceutical importance of resveratrols, the research a-glucosidase inhibition. The structures of these compounds were group of Snyder and Nicolaou independently developed proto- determined by the analysis of various spectroscopic data including cols for the total synthesis of resveratrols despite of their HRMS-ESI, 2D NMR, CD spectroscopy, optical activity and were structural complexity. Among the resveratrol oligomers, the unequivocally established by single crystal X-ray crystallography. tetramer hopeaphenol shows a wide range of biological activi- Herein we are reporting the phytochemicals from Ampelocissus indica ties.6–8 In 2006, Merillon and co-workers isolated (+)-hope- (L.) and their antidiabetic activities for the first time. aphenol from commercially available wine from North Africa.9 Recently Quinn et al. reported the isolation of (À)-hopeaphenol from Anisoptera species which inhibit the bacterial virulence aOrganic Chemistry Section, National Institute for Interdisciplinary Science and type III secretion system (T3SS).10 Technology (CSIR), Trivandrum 695019, India. E-mail: [email protected] It is evident from the literature that resveratrols are also b Academy of Scienti c and Innovative Research (AcSIR), New Delhi 110001, India accountable for antidiabetic activity and the recent works by cAgroprocessing and Natural Product Division, National Institute for Interdisciplinary Sharma et al. proved the efficacy of resveratrol as an effective Science and Technology (CSIR), Trivandrum 695019, India 11 dCoreValley's Herbal Technologies, 133-H, Mini Industrial Estate, Nallalam, Calicut- therapeutic adjuvant for diabetes mellitus. Most of the avail- 673027, Kerala, India able drugs used for curing type 2 diabetes causes serious side eDepartment of Botany, Calicut University, Calicut, Kerala, India effects such as obesity, sexual and urologic complications. Kahn fM. S. Swaminathan Research Foundation-Community Agrobiodiversity Centre et al. reported a single mechanism to explain the link between (MSSRF-CAbC), Puthurvayal, Wayanad, Kerala, India obesity, insulin resistance and type 2 diabetes.12 The perva- g Department of Chemistry, Sree Narayana College, Chempazhanthy, siveness of type 2 diabetes is growing globally, and thus there is Thiruvananthapuram, Kerala, India urgency for new antidiabetic drugs with less/no side effects. The † Electronic supplementary information (ESI) available. CCDC 1035198 and 1061115. For ESI and crystallographic data in CIF or other electronic format see plant derived antidiabetic drugs available in market reveals the DOI: 10.1039/c6ra14334b potential of phytochemicals to regulate this metabolic disorder, This journal is © The Royal Society of Chemistry 2016 RSC Adv.,2016,6, 77075–77082 | 77075 View Article Online RSC Advances Communication compelling the search for new naturally inspired antidiabetic 2.3. Biological screening drug leads.13 2.3.1 Total phenolic content (TPC). TPC of the various In the limelight of these reports and due to our interest in solvent fractions were determined using Folin–Ciocalteu the chemical proling of the plants of ethnobotanical impor- reagent and was expressed in mg GAE per g of the dry extract.15 tance, rst we selected the plant species Ampelocissus indica L. Absorbance was then read at 725 nm using a multiplate reader (AI). We have isolated E-resveratrol, (3)-viniferin, b-sitoster- (Synergy, Biotek, USA). olglucoside and pauciorol along with the (+)-hopeaphenol. 2.3.2 DPPH radical scavenging activity. DPPH radical scav- Inspired by the structural features of (+)-hopeaphenol, we enging activity was estimated according to the method of Brand- decided to isolate and compare the resveratrol tetramers from Williams, Cuvelier and Berset.16 Various concentrations of the another plant Vateria indica Linn. (VI) found in the Western extracts were added to 1 mL of DPPH solution (0.2 mM) and kept Ghats region in Kerala, as a source of resveratrol oligomers. for incubation at room temperature in dark for about 30 minutes. Among these plants the chemical constituents of the former one A control and blank were also performed simultaneously. Gallic A. indica, to the best of our knowledge, is unknown to the acid was used as the standard. The absorbance was read at 517 nm phytochemical research community. using a multiplate reader (Synergy 4 Biotek. USA). The percentage In this paper, antidiabetic activity of different extracts, the radical scavenging capacity was determined using the formula, isolation and characterization of (+) and (À)-hopeaphenol from A. indica (L.) and V. indica Linn. are described. Successively we % RSA ¼ [(A0 À AS)/A0]  100 studied the antidiabetic effect by digestive enzyme inhibition ff and glucose uptake in muscle cells. Di erent characterization where A0 is the absorbance of control and AS is the absorbance techniques such as NMR, MS, CD, optical activity measure- of tested samples. A graph was plotted with concentration along ments and single crystal X-ray crystallography were utilised for x-axis and absorbance along y-axis and IC50 value was calculated m À1 the structural elucidation. While preparing the manuscript, and expressed in gmL .IC50 value signi es the concentration a Creative Commons Attribution 3.0 Unported Licence. Chang and Hou et al. reported the anti- -glucosidase and anti- of tested samples to scavenge 50% of the DPPH radical. dipeptidyl peptidase-IV activities of extracts and puried 2.3.3 a-Amylase inhibition assay. a-Amylase inhibition compounds from Vitis thunbergii var. taiwaniana.14 The in vitro activity was carried out in a microlitre plate according to Xiao antidiabetic data for (+) and (À)-hopeaphenol seems to be et al.17 based on the starch-iodine test. Starch containing À highly promising and warranted further evaluation. a-amylase solution (1 U mL 1) and different concentrations of extracts/compounds were incubated at 50 C for 30 min. Aer incubation, the reaction was stopped with 1 M HCl and 100 mL 2. Materials and methods of iodine reagent was added to the reaction mixture. The 2.1. Plant material absorbance was read at 580 nm on a microplate reader using This article is licensed under a a The Rhizomes of Ampelocissus indica (L.) were collected from Synergy 4 Biotek multiplate reader (USA). The known -amylase Calicut, Kerala and deposited in Calicut University herbarium inhibitor, acarbose, was used a positive control. The percentage (Voucher no. 6781). The bark of Vateria indica Linn. was inhibition was calculated using following equation Open Access Article. Published on 03 August 2016. Downloaded 12/05/2017 10:33:03. collected from Wayanad and deposited in M. S. Swaminathan % inhibition ¼ Research Foundation, Wayanad, Kerala (Voucher no. absorbance of control À absorbance of sample  100 M.S.S.H.0763). absorbance of control 2.2. General experimental procedure A graph was plotted with concentration along the x axis and Optical activity was recorded on a Jasco P-1020 Polarimeter. percentage inhibition along the y axis to obtain the IC50 value. NMR spectra were recorded at 25 C on 500 MHz BRUKER 2.3.4 a-Glucosidase inhibition assay. a-Glucosidase inhib- instrument. The 1H and 13C NMR chemical shis were refer- itory activity was assayed as described by Disakwattana et al.18 enced to the tetramethylsilane (TMS) as standard. HRMS-ESI Different concentrations of extracts/compounds containing À was recorded on a Thermo Scientic Exactive Column used: a-glucosidase solution (1 U mL 1) were vortexed and kept at C18 (reverse phase column), CD spectrum was recorded on room temperature for 5 min, aer incubation 250 mLofPNPG JASCO 810 Spectropolarimeter.
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