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Inhibitory Properties of Saponin from Eleocharis Dulcis Peel Against Α-Glucosidase

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Inhibitory Properties of Saponin from Eleocharis Dulcis Peel Against Α-Glucosidase RSC Advances View Article Online PAPER View Journal | View Issue Inhibitory properties of saponin from Eleocharis dulcis peel against a-glucosidase† Cite this: RSC Adv.,2021,11,15400 Yipeng Gu, a Xiaomei Yang,b Chaojie Shang,a Truong Thi Phuong Thaoa and Tomoyuki Koyama*a The inhibitory properties towards a-glucosidase in vitro and elevation of postprandial glycemia in mice by the saponin constituent from Eleocharis dulcis peel were evaluated for the first time. Three saponins were isolated by silica gel and HPLC, identified as stigmasterol glucoside, campesterol glucoside and daucosterol by NMR spectroscopy. Daucosterol presented the highest content and showed the strongest a-glucosidase inhibitory activity with competitive inhibition. Static fluorescence quenching of a-glucosidase was caused by the formation of the daucosterol–a-glucosidase complex, which was mainly derived from hydrogen bonds and van der Waals forces. Daucosterol formed 7 hydrogen bonds with 4 residues of the active site Received 19th March 2021 and produced hydrophobic interactions with 3 residues located at the exterior part of the binding Accepted 9th April 2021 pocket. The maltose-loading test results showed that daucosterol inhibited elevation of postprandial Creative Commons Attribution-NonCommercial 3.0 Unported Licence. DOI: 10.1039/d1ra02198b glycemia in ddY mice. This suggests that daucosterol from Eleocharis dulcis peel can potentially be used rsc.li/rsc-advances as a food supplement for anti-hyperglycemia. 1. Introduction a common hydrophytic vegetable that grows in Japan, China, India and other Asian countries.13,14 The edible corms are a-Glucosidase hydrolyzes terminal non-reducing a-1,4-glyco- consumed as a fruit or vegetable, and also used to produce sidic bonds to release a glucose molecule, which is involved in starch and canned foods.15 In China, fresh-cut Eleocharis dulcis glycometabolism and plays an important role in maintaining is very popular due to its unique sweet taste and medicinal This article is licensed under a the normal physiological function of the body.1–3 This enzyme is properties. As a traditional Chinese medicine, the corm of located in the brush border of the small intestine and catalyzes Eleocharis dulcis has been applied to treat constipation, phar- the hydrolysis of polysaccharides or oligosaccharides into yngitis, laryngitis, hypertension and chronic nephritis.16,17 Open Access Article. Published on 26 April 2021. Downloaded 9/26/2021 8:17:46 PM. glucose to induce postprandial hyperglycemia; by regulating However, a large amount of peel is produced as a waste product in this process, diabetic patients can control glucose uptake and fruit processing and accumulates, causing rot and serious environ- suppress rapid rises of blood glucose levels to prevent the mental pollution.18 It has been reported that twenty avonoids iso- development of diabetes-associated complications.4,5 Currently, lated from Eleocharis dulcis peel show strong 2,2-diphenyl-1- the widely used clinical antidiabetic drugs are a-glucosidase picrylhydrazyl (DPPH) radical scavenging activity.15 The ethanol inhibitors, such as acarbose, voglibose and miglitol, to inhibit extract from Eleocharis dulcis with high values of phenolic and the intestinal absorption of glucose, but the long-term admin- avonoids compounds showed an inhibitory value of 65.74% against istration of these agents may produce adverse side effects and a-glucosidase at a concentration of 2000 ppm.19 However, there are high cost.6,7 In search of appropriate hypoglycemic medications, currently few reports about saponins from Eleocharis dulcis peel. attention has been focused on edible plants for several years, Saponins are widely distributed in natural medicines with various whose extracts contain bioactive components that demonstrate pharmacological activities, such as antimicrobial, antioxidant, 20 signicant a-glucosidase inhibitory activity, such as L-arabi- antithrombotic, antitumor, hypoglycemic, etc. Hence, this study nose, salacinol, mangiferin and soybean isoavone.8–12 aimedtoresearchthesaponinconstituentinEleocharis dulcis peel Eleocharis dulcis (also known as Chinese water chestnut), and evaluate its inhibition of a-glucosidase and elevation of post- a perennial sedge belonging to the family Cyperaceae, is prandial glycemia in mice aer maltose-loading for the rst time, and it is expected to be applied in functional foods in the future. aLaboratory of Nutraceuticals and Functional Foods Science, Graduate School of Marine Science and Technology, Tokyo University of Marine Science and Technology, 4-5-7 Konan, Minato, Tokyo 108-8477, Japan. E-mail: tskoyama@ 2. Materials and methods kaiyodai.ac.jp 2.1 Materials bInstitute of Food Science and Technology, Hezhou University, Hezhou 542899, China † Electronic supplementary information (ESI) available. See DOI: The fresh Eleocharis dulcis were purchased from the central 10.1039/d1ra02198b agricultural product market of Hezhou (Hezhou, Guangxi 15400 | RSC Adv.,2021,11,15400–15409 © 2021 The Author(s). Published by the Royal Society of Chemistry View Article Online Paper RSC Advances Province, China) and cleaned with water, and then the peels (Fig. S1A†). Furthermore, a Shimadzu HPLC System (Kyoto, without decay and deterioration were collected and dried with Japan) equipped with a Develosil ODS HG-5 column (4.6 mm  a DHG series heating and drying oven (DHG-9140A, Keelrein, 250 mm, Nomura Chemical, Japan) with isocratic elution of China) at 60 C for 36 h. Aer this, the dried peels were ground 100% methanol at 30 C (wavelength: 210 nm, ow rate: 1 À by a universal high-speed grinder (DFY-600, Linda Machinery mL min 1) also demonstrated no difference between the two Co., Ltd, China) and stored for further extraction. saponin fractions (Fig. S1B†). Fr.3 and Fr.4 were combined and a-Glucosidase (EC 3.2.1.20) from yeast was purchased from dried to obtain a powder (2.09 g). Oriental Yeast Co., Ltd (Tokyo, Japan), and dissolved in 0.1 M sodium phosphate buffer of pH 7.4. Methanol, acetonitrile and 2.3 Purication and structural elucidation of saponins distilled water as HPLC grade chemicals were purchased from The powder of the saponin fraction was dissolved in methanol, Kanto Chemical Co., Inc. (Tokyo, Japan). Acarbose and p- and a Prep LC System (PU2080 Plus, JASCO, Japan) in recycling nitrophenyl-a-D-glucopyranoside (pNPG) were purchased from mode was used to purify the saponins. The ultraviolet absorp- Tokyo Chemical Industry Co., Ltd (Tokyo, Japan). A Glucose C-II tion spectrum was obtained using a Develosil ODS HG-5 column Test Wako Kit was obtained from Fujilm Wako Pure Chemical (20 mm  250 mm, Nomura Chemical, Japan) and eluted with Industries, Ltd (Osaka, Japan). Pyridine-d for NMR spectros- 5 100% methanol at room temperature (wavelength: 210 nm, ow copy and maltose were purchased from Kanto Chemical Co., À rate: 8 mL min 1), and three components were collected in Inc. (Tokyo, Japan). All other reagents were of analytical purity. accordance with the chromatogram (Fig. S2†). Aer freeze- drying, compound 3 gave the highest amount with a total 2.2 Extraction and isolation of the saponin fraction yield of 961.5 mg, achieving 0.10% overall recovery; the compound 1 yield was 158.3 mg (0.02%), and that of compound The dried materials of Eleocharis dulcis peel (1 kg) were 2 was 260.1 mg (0.03%). The structures of all components were combined with 5 L methanol and kept in an ultrasonic reactor characterized by NMR spectroscopy techniques on a Bruker (KQ5200DV, Kunshan, China) at 40 kHz and 60 C for 2 h. The Creative Commons Attribution-NonCommercial 3.0 Unported Licence. Advance 600 MHz spectrometer (Bruker, Germany). Accord- ltered methanol extracts were concentrated by a rotary evap- ingly, the three compounds were identied as stigmasterol orator (N1300DW, EYELA, Japan) and dried by a freeze-dryer glucoside (1), campesterol glucoside (2) and daucosterol (3), as (FDU2110, EYELA, Japan), and then suspended with 0.2 L of shown in Fig. 2. Furthermore, the NMR data for the compounds distilled water and partitioned with n-butanol (1 L) twice. The were consistent with those reported in the literature.21–25 organic layer was collected and freeze-dried, and then these extracts were dissolved in methanol and ve volumes of acetone a in vitro were gradually added until complete precipitation. The precip- 2.4 -Glucosidase inhibitory activity assay itates were subjected to a silica gel column (4 cm  11 cm), and The a-glucosidase inhibitory activities were measured accord- This article is licensed under a eluted with n-hexane, ethyl acetate, methanol–ethyl acetate (v : v ing to a slightly modied method reported by Zhang et al.26 ¼ 1 : 1) and methanol, at ve times the column volume for each Several assay solutions containing 20 mLofa-glucosidase of 0.5 À eluent. The separation process is illustrated in Fig. 1. A Bruker UmL 1, 120 mL of phosphate buffer (pH 7.4) of 0.1 M, and 10 mL Open Access Article. Published on 26 April 2021. Downloaded 9/26/2021 8:17:46 PM. Advance 600 MHz spectrometer (Bruker, Germany) was used to of dimethyl sulfoxide solution of saponin were prepared at 1 À1 obtain H NMR spectra with pyridine-d5 as the solvent. Fr.3 and various concentrations from 0 to 1 mg mL mixed in a 96-well Fr.4 were detected, which showed similar saponin signals microtiter plate. The plate was incubated at 37 C for 10 min. The enzymatic reaction was initiated by adding 20 mLof5mM substrate pNPG solution in 0.1 M phosphate buffer of pH 7.4, and the nal reaction mixture was incubated for 10 min at 37 C. Subsequently, the absorbance of the reaction system was immediately transferred into a ThermoMax microplate reader (31139, Thermo, USA) and measured at 405 nm. The enzymatic activity assay without the saponin sample, which was replaced by dimethyl sulfoxide, was dened as the control, and that without a-glucosidase was used as a control blank to correct for background absorbance.
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