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In Vitro Studies of Α-Glucosidase Inhibitors and Antiradical Food Chemistry 136 (2013) 1390–1398 Contents lists available at SciVerse ScienceDirect Food Chemistry journal homepage: www.elsevier.com/locate/foodchem In vitro studies of a-glucosidase inhibitors and antiradical constituents of Glandora diffusa (Lag.) D.C. Thomas infusion ⇑ Federico Ferreres a, , Juliana Vinholes b, Angel Gil-Izquierdo a, Patrícia Valentão b, ⇑ Rui F. Gonçalves b, Paula B. Andrade b, a Research Group on Quality, Safety and Bioactivity of Plant Foods, Department of Food Science and Technology, CEBAS (CSIC), P.O. Box 164, 30100 Campus University Espinardo, Murcia, Spain b REQUIMTE/Laboratório de Farmacognosia, Departamento de Química, Faculdade de Farmácia, Universidade do Porto, Rua de Jorge Viterbo Ferreira, n.° 228, 4050-313 Porto, Portugal article info abstract Article history: Glandora diffusa (Lag.) D.C. Thomas (Boraginaceae) is a species traditionally consumed as an infusion. The Received 25 June 2012 phenolic profile of its aqueous extract was assessed by HPLC–DAD–ESI/MSn. Twenty-seven compounds Received in revised form 12 August 2012 were identified, comprising caffeic and p-coumaric acids, seventeen polymers of caffeic acid and eight Accepted 24 September 2012 3-O-glycosylated flavonols. Caffeic, rosmarinic, and salvianolic acids were the most representative com- Available online 5 October 2012 pounds, accounting for more than 75% of the phenolic fraction. The potential of G. diffusa aqueous extract to act as radical scavenger was assessed against DPPHÅ, superoxide and nitric oxide. A dose-dependent Keywords: response was observed against all reactive species. Moreover, the extract showed promising results as Glandora diffusa (Lag.) D.C. Thomas inhibitor of -glucosidase, being almost 9 times more effective than acarbose. Both activities are related Polyphenolic compounds a HPLC–DAD–ESI/MSn with the presence of polyphenolic compounds. Therefore, the combination of a-glucosidase inhibition Oxidative stress with its antiradical capacity opens a new perspective for the use of G. diffusa by patients with diabetes Diabetes mellitus mellitus. As far as we know, this is the first study assessing the chemical composition and biological potential of G. diffusa. Our results can boost the consumption of G. diffusa species as an infusion or in food and pharmaceutical preparations. Ó 2012 Elsevier Ltd. All rights reserved. 1. Introduction Glandora diffusa (Lag.) D.C. Thomas (synonyms: Lithospermum diffusum Lag. and Lithodora diffusa (Lag.) I.M. Johnst.) being one of Boraginaceae family comprises more than 2700 species distrib- them. This herbal species, commonly known as ‘‘scrambling- uted among 150 genera. The different species can be commonly gromwell’’, grows spontaneously in the Mediterranean basin found in cosmopolitan fields especially in tropic, Turian region (Thomas, Weigend, & Hilger, 2008). Traditionally, its infusion is (Iran) and Mediterranean regions (Flora Ibérica, 2012). A diversity consumed for diuretic, depurative and anti-hypertensive purposes. of species from this family has been traditionally used as diuretic, Additionally, its pollen is found in some honeys (Sá-Otero, anti-inflammatory, diaphoretic, sedative, in the treatment of cough, Armesto-Baztan, & Díaz-Losada, 2006). However, as far as we know, bronchitis and throat infections, as well as rheumatic pain and there is no report about the chemical composition of this species. as poultice in burns (Crellin, Philpott, & Bass, 1990; Khan & Phenolic compounds are secondary metabolites commonly Abourashed, 2009). Chemically, this family is characterised by the found in nature (Petersen & Simmonds, 2003). These compounds, presence of naphtoquinones, such as shikonin and its derivatives namely flavonoids and phenolic acids, are well known for their (Brigham, Michaels, & Flores, 1999; Staniforth, Wang, Shyur, & Yang, antioxidant properties, since they can scavenge different radical 2004; Yoon, Kim, Lim, Jeon, & Sung, 1999), pyrrolizidine alkaloids species (Andjelkovic et al., 2006; Burda & Oleszek, 2001; Fan, (Krenn, Wiedenfeld, & Roeder, 1994; Roeder & Rengel, 1990) and Terrier, Hay, Marston, & Hostettmann, 2010). In addition, recent phenolic compounds, such as rosmarinic acid and its derivatives: studies point to their ability to inhibit enzymes, such as cholines- (i) lithospermic acid, a conjugate of rosmarinic and caffeic acids, terases and a-glucosidase, which are associated to different and (ii) lithospermic acid B, a dimer of rosmarinic acid (Petersen & pathologies (Fan et al., 2010; Ferreres et al., 2012; Min et al., Simmonds, 2003). Glandora is a genus that includes 6 species, 2010; Tadera, Minami, Takamatsu, & Matsuoka, 2006). Since the family to which G. diffusa belongs is recognised for its interesting phenolic composition, one aim of this work was to ⇑ Corresponding authors. Tel.: +351 220428654; fax: +351 226093390. n E-mail addresses: [email protected] (F. Ferreres), [email protected] (P.B. characterise these metabolites by means of HPLC–DAD–ESI/MS . Andrade). In addition, its biological potential has not been evaluated so far. 0308-8146/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.foodchem.2012.09.089 F. Ferreres et al. / Food Chemistry 136 (2013) 1390–1398 1391 Thus, since G. diffusa is mainly consumed as infusion, we also The extract was then filtered (0.2 lm) and studied by HPLC– aimed to assess the activity of its aqueous extract as antiradical DAD–ESI/MSn. and as a-glucosidase inhibitor. A possible relationship between Chromatographic analyses were carried out on a Luna C18 (2) chemical composition and activity was further considered. 100A column (150 x 1.0 mm, 3 lm particle size; Phenomenex, Macclesfield, UK). The mobile phase consisted of two solvents: 2. Materials and methods water (1% formic acid) (A) and methanol (B), starting with 30% B and using a gradient to obtain 50% B at 50 min and 80 % B at 2.1. Standards and reagents 60 min. The flow rate was 20 ll/min, and the injection volume 5 ll. Spectral data from all peaks were accumulated in the range Reference compounds and reagents were purchased from 240–600 nm, and chromatograms were recorded at 285, 330, 450 n different suppliers. Quercetin-3-O-rutinoside, kaempferol-3-O- and 550 nm. The HPLC–DAD–ESI/MS analyses were carried out rutinoside, isorhamnetin-3-O-glucoside and rosmarinic acid were in an Agilent HPLC 1200 series equipped with a diode array detec- from Extrasynthese (Genay, France), caffeic and p-coumaric acids, tor and mass detector in series (Agilent Technologies, Waldbronn, 2,2-diphenyl-1-picrylhydrazyl radical (DPPHÅ), b-nicotinamide Germany). The HPLC consisted of a binary pump (model G1376A), adenine dinucleotide reduced form (NADH), phenazine methosul- an autosampler (model G1377A) refrigerated at 4 °C (G1330B), a phate (PMS), nitroblue tetrazolium chloride (NBT), 5,50-dithi- degasser (model G1379B), and a photodiode array detector (model obis(2-nitrobenzoic acid) (DTNB), sulphanilamide, a-glucosidase G1315D). The HPLC system was controlled by ChemStation soft- ware (Agilent, v. B.01.03-SR2). The mass detector was a Bruker (type I from baker’s yeast) and 4-nitrophenyl a-D-glucopyranoside (PNP-G) were obtained from Sigma–Aldrich (St. Louis, MO, USA). ion trap spectrometer (model HCT Ultra) equipped with an electro- Sodium nitroprussiate was purchased from Riedel-de Haën (St. spray ionisation interface and was controlled by LCMSD software Louis, MO). N-(1-Naphthyl) ethylenediamine dihydrochloride, (Agilent, v. 6.1). The ionisation conditions were adjusted at methanol, acetonitrile, and phosphoric, formic and acetic acids 300 °C and 4.0 kV for capillary temperature and voltage, respec- were obtained from Merck (Darmstadt, Germany) and sulphuric tively. The nebulizer pressure and flow rate of nitrogen were acid from Pronalab (Lisboa, Portugal). The water was treated in a 5.0 psi and 3 l/min, respectively. The full scan mass covered the Milli-Q water purification system (Millipore, Bedford, MA, USA). range from m/z 100 up to m/z 1200. Target Mass 500. Collision-in- duced fragmentation experiments were performed in the ion trap using helium as the collision gas, with voltage ramping cycles from 2.2. Plant material 0.3 up to 2 V. Mass spectrometry data were acquired in the nega- tive and positive ionisation modes. MSn was carried out in the The dried aerial parts of G. diffusa, corresponding to a mixture of automatic mode on the more abundant fragment ion in MS(nÀ1). different individuals, were purchased in the local market from a Table 1 shows the compounds grouped by their polymerization de- medicinal plants distributor (Augusto Coutinho Ervanários, Porto, gree (dimers, trimers, tetramers and pentamers) and following Portugal). The identity was confirmed by the authors following their elution order. the characteristics described in Flora Ibérica (2012). The plant material was powdered (mean particle size lower than 910 lm). Voucher specimen was deposited at Laboratório de Farmacognosia, 2.5. Phenolic compounds quantification by HPLC–DAD Faculdade de Farmácia, Universidade do Porto (GD-AP-032012). For quantification purposes, 20 ll of the re-dissolved aqueous 2.3. Sample preparation extract (31.2 mg/ml in water) were analysed on an analytical HPLC unit (Gilson), with a Luna C18 column (250 Â 4.6 mm, 5 lm parti- An aqueous extract was prepared: 3 g of pulverized material cle size; Phenomenex, Macclesfield, UK), using the same elution were extracted with 600 ml of boiling water for 20 min, with sub- conditions described above, but with a flow rate of 0.8 ml/min. sequent filtration over a Büchner funnel. The resulting extract was Detection was achieved with a Gilson diode array detector. Spec- then lyophilized and maintained in a desiccator at room tempera- tral data from all peaks were collected in the range of 200– ture, in the dark, until analysis. 400 nm and chromatograms were recorded at 330 nm. The data were processed on Unipoint System software (Gilson Medical Elec- 2.4. HPLC–DAD–ESI/MSn qualitative analysis of phenolic compounds tronics, Villiers le Bel, France). The compounds were identified by comparing their elution order and UV–vis spectra with those of G.
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