Acute Consumption of Bordo Grape Juice and Wine Improves Serum Antioxidant Status in Healthy Individuals and Inhibits Reactive Oxygen Species Production in Human Neuron-Like Cells

Cristiane Copetti; Fernanda Wouters Franco; Eduarda da Rosa Machado; Marcela Bromberger Soquetta; Andréia Quatrin; Vitor de Miranda Ramos; José Cláudio Fonseca Moreira; Tatiana Emanuelli; Cláudia Kaehler Sautter; Neidi Garcia Penna

doi:10.1155/2018/4384012

Acute Consumption of Bordo Grape Juice and Wine Improves Serum Antioxidant Status in Healthy Individuals and Inhibits Reactive Oxygen Species Production in Human Neuron-Like Cells

Copetti, Cristiane;Franco, Fernanda Wouters;Machado, Eduarda da Rosa;Soquetta, Marcela Bromberger;Quatrin, Andréia;Ramos, Vitor de Miranda;Moreira, José Cláudio Fonseca;Emanuelli, Tatiana;Sautter, Cláudia Kaehler;Penna, Neidi Garcia 2018-03-01 00:00:00 Hindawi Journal of Nutrition and Metabolism Volume 2018, Article ID 4384012, 11 pages https://doi.org/10.1155/2018/4384012 Research Article Acute Consumption of Bordo Grape Juice and Wine Improves Serum Antioxidant Status in Healthy Individuals and Inhibits Reactive Oxygen Species Production in Human Neuron-Like Cells 1 1 1 Cristiane Copetti , Fernanda Wouters Franco , Eduarda da Rosa Machado , 2 1 3 Marcela Bromberger Soquetta, Andre´ia Quatrin , Vitor de Miranda Ramos , 3 1 1 Jose´ Cla´udio Fonseca Moreira, Tatiana Emanuelli , Cla´udia Kaehler Sautter, and Neidi Garcia Penna Department of Food Technology and Science, Center of Rural Sciences, Federal University of Santa Maria (UFSM), 1000 Roraima Avenue, 97105-900 Santa Maria, RS, Brazil Department of Chemical Engineering, Center of Technology, Federal University of Santa Maria (UFSM), 1000 Roraima Avenue, 97105-900 Santa Maria, RS, Brazil Department of Biochemistry, Center of Oxidative Stress Research (CEEO), Federal University of Rio Grande do Sul (UFRGS), 2600 Ramiro Barcelos Street–Annex, 90035-003 Porto Alegre, RS, Brazil Correspondence should be addressed to Cristiane Copetti; copetti.cris@gmail.com Received 4 September 2017; Accepted 30 November 2017; Published 1 March 2018 Academic Editor: Michael B. Zemel Copyright © 2018 Cristiane Copetti et al. )is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Few studies investigated the biological eﬀects of American grape cultivars. We investigated the metabolic response after acute consumption of grape juice or wine fromBordo grapes (Vitis labrusca) ina placebo-controlledcrossover study with ﬁfteen healthy volunteers. Blood samples were collected 1 hour after the intake of 100mL of water, juice, or wine to measure TBARS, ABTS, FRAP, glucose, and uric acid levels. To evaluate diﬀerences in cellular response, intracellular reactive species production (DCFH-DA) and metabolic mitochondrial viability (MTT) were assessed after exposure of human neuron-like cells (SH-SY5Y) to juice or wine. Glycemia was reduced after juice or wine consumption, whereas blood levels of uric acid were reduced after juice consumption but increased after wine consumption. Juice and wine consumption reduced plasma lipid peroxidation and increased plasma antioxidant capacity (ABTS and FRAP assays). Furthermore, juice inhibited H O -induced intracellular 2 2 production of reactive species (RS) and increased the viability of SH-SY5Y cells. In contrast, wine (dealcoholized) exhibited a per se eﬀect by inducing the production of RS and reducing cell viability. )ese results indicate a positive impact of acute consumption of Bordo juice and wine on human oxidative status, whereas only juice had protective eﬀects against oxidative stress-induced cytotoxicity. mitochondria in brain cells increases the generation of re- 1. Introduction active species [2]. Oxidative stress is caused by the insuﬃcient capacity of Fruits and vegetables have many bioactive compounds biological systems to neutralize the excessive production of such as polyphenols, which have antioxidant properties with reactive species [1], which leads to oxidative damage in cells. a role in the protection of cellular macromolecules against Neuronal cells are particularly susceptible to reactive oxygen oxidative damage induced by ROS and RNS [3–5]. )ere is species (ROS) and reactive nitrogen species (RNS) due to increasing evidence that polyphenols may protect cell their high metabolic activity, low antioxidant capacity, and constituents against oxidative damage and, therefore, limit their nonreplicative nature. Furthermore, the abundance of the risk of various degenerative diseases associated with 2 Journal of Nutrition and Metabolism oxidative stress [6]. Studies have repeatedly shown an which grape is crushed and then heated to at least 65 C in inverse association between the risk of several chronic a hot macerator. Next, commercial pectolytic enzymes are ° ° human diseases and the consumption of polyphenol-rich added and must be kept between55 C and 60 C during 1-2h. diet [7]. )e phenolic group of polyphenols can accept an )e extracted juice is then clariﬁed, pasteurized, and bottled electron to form relatively stable phenoxyl radicals, [23]. Bordo wine was obtained from viniﬁcation process by thereby disrupting chain oxidative reactions in cellular the coupled dispositive to the crushing machine that is called components. It is well established that polyphenol-rich dewaxing. In winemaking of red wine, grape skin remains foods and beverages may increase plasma antioxidant inside tanks during fermentation for extraction of antho- capacity [8, 9]. cyanin pigments [24]. Grapes contain high levels of polyphenols, which have been demonstrated to reduce oxidative stress, inﬂammatory 2.2. Determination of Bioactive Compounds in Bordo Juice and response, and the oxidation of low density lipoprotein Wine. )e total phenolic content was determined at 760nm cholesterol (LDL-c), while inhibiting platelet aggregation using the Folin–Ciocalteumethodand gallicacidasstandard and improving protection against atherothrombotic epi- [25]. Total anthocyanin content was assessed at 520nm as sodes. Such actions promote beneﬁcial eﬀects on coronary the diﬀerence of absorbance before and after sample heart disease (CHD) and atherosclerosis [10–12]. Red wines decoloration using sodium bisulﬁte at pH 0.8 and was are rich in polyphenols, such as phenolic acids (gallic acid, expressed as mg of malvidin-3-glucoside/L [26]. )e total caﬀeic acid, p-coumaric acid, and others), stilbenes (trans- ﬂavonoid content was estimated at 510nm using a standard resveratrol), and ﬂavonoids (catechin, epicatechin, querce- curve of catechin (0–200mg/L) [27]. tin, rutin, myricetin, and others) [13]. )erefore, a regular consumption of red wine has been linked with the “French paradox,” which explains the apparent compatibility of 2.3. Antioxidant Capacity of Bordo Juice and Wine. )e a high-fat diet with a low mortality from CHD. Also, current antioxidant capacity of grape juice and red wine were de- evidence suggests that wine consumption is correlated with termined using the 2,2′-azino-bis (3-ethylbenzothiazoline- a reduction in the incidence of neurodegenerative diseases 6-sulphonic acid) (ABTS) and ferric reducing antioxidant associated to oxidative stress such as Alzheimer’s and power (FRAP) methods as described by Re et al. [28] and Parkinson’s disease [14]. Grape juice is a natural and Benzie and Strain [29], respectively. )e ABTS assay is nonalcoholic beverage that contains sugars, minerals, assessed at 764nm and is based on the ability of the sample ·+ and phenolic compounds like anthocyanins, among which to scavenge the cation radical ABTS . )e FRAP assay is malvidin 3,5-diglucoside is the major one [15]. )is beverage assessed at 620nm and is based on the reduction of ferric- has been shown to exert antioxidant activity in vitro and tripyridyltriazine (Fe III-TPTZ) by antioxidants present in in vivo, as well as hypolipidemic and anti-inﬂammatory the samples forming ferrous-tripyridyltriazine (Fe II-TPTZ), eﬀects in rats and humans [16–18]. a blue-colored product. Trolox was used in the calibration However, few studies have compared the eﬀects of curve. wine and juice consumption in biological parameters of humans, and these studies used European grape species 2.4. In Vivo Study (Vitis vinifera) [19–21]. In contrast, the biological eﬀects of wine and juice from American grape species 2.4.1. Participants. )e study design was approved by the (Vitis labrusca) have not been compared. )is investigation is Ethics Committee of Federal University of Santa Maria particularly interesting as the red grape cultivar “Bordo” (CAAE 39197614.3.0000.5346), and all subjects signed (V. labrusca), which is the most important grape cultivated in a written agreement before participating. Fifteen healthy Brazil [15], has been recently demonstrated to exhibit volunteers, with mean age 24.0 ±3.6, were recruitedfrom the higher content of phenolic compounds and in vitro anti- University staﬀ. )e health status and medical history of oxidant capacity than V. vinifera species [22]. In the present volunteers were examined by a structured interview for study, we compared the biological eﬀects of juice and wine inclusion or exclusion according to the criteria shown in from “Bordo” grapes (V. labrusca L) by assessing blood Table 1. antioxidant response after human consumption and the oxidative cellular response in human neuron-like cells (SH-SY5Y). 2.4.2. Study Design. In this crossover-controlled clinical study, 15 volunteers were included, 10 women (67%) and 5 men (33%). All participants received the three treatments, 2. Materials and Methods namely, Bordo grape juice, Bordo wine, and water (control) 2.1. Bordo Grape Juice and Wine. )e commercial samples of with a washout period of 1 week between treatments. )e Bordo grape juice and Bordo wine were produced by sequence of the treatments was randomized among the a winemaker (Casa Perini, Farroupilha, RS, Brazil). )e participants as depicted in Figure 1. grape fruits used to prepare juice and wine were harvested in Participants were oriented to follow a low-antioxidant ° ° Farroupilha (29 13′ 30″ S, 51 20′ 52″ W, altitude 783m), in diet for 48h prior to the day of intervention, avoiding some the State of Rio Grande do Sul, Brazil, on January 2014. fruits, vegetables, and juices, mainly rich in anthocyanins, Bordo grape juice was prepared by the enzymatic method, in tea, coﬀee, cocoa foodstuﬀs, and alcoholic beverages. )is Journal of Nutrition and Metabolism 3 Table 1: Selection criteria of study participants. Inclusion criteria Exclusion criteria Apparently healthy individuals Pregnant and lactating women Age 18–35 years old Alcoholic and smokers BMI between 18.5 and 29.9kg/m Vegetarian diet Regular use of antioxidants or vitamin supplements Chronic diseases (cardiovascular diseases, hypertension, diabetes, liver diseases, SBP<140mmHg and DBP≤90mmHg cancer, or allergy); gastrointestinal disorders or known metabolic diseases; infections or inﬂammatory processes visible or known in the three months prior to the study BMI �body mass index, SBP �systolic blood pressure, and DBP �diastolic blood pressure. analysis. Blood collected in tubes without additives was Volunteers screened for eligibility (n= 30) centrifuged (1500 ×g, 10min) to yield serum for analysis of Excluded (n= 4) uric acid and glucose. Serum and plasma samples were Declined (n= 11) stored at −80 C until analysis. Uric acid and glucose were determined in serum using Subjects entered the study (n= 15) commercially available enzymatic kits (Bioclin, Belo Hori- Randomization 1-week washout zonte, Brazil). Lipid peroxidation was determined by measurement of TBARS at 535nm in plasma [31]. )e antioxidant capacity of plasma was assessed by the ABTS Bordo grape juice Bordo grape juice Bordo grape juice [28] and FRAP assays [29]. (n= 5) (n= 5) (n= 5) Bordo wine Bordo wine Bordo wine (n= 5) (n= 5) (n= 5) 2.5. Cell Culture Assays. Human neuron-like cell line SH- SY5Y obtained from the European Collection of Authenticated Water Water Water (n= 5) (n= 5) (n= 5) Cell Cultures (ECACC) were maintained in 75cm ﬂasks containing DMEM/F12 medium (1:1) supplemented with 10% fetal bovine serum (FBS) and 1× antibiotic/antimycotic solu- tion (Sigma-Aldrich). Cells were cultured in a humidiﬁed incubator set at 37 Subjects completed the study (n= 15) C with 5% CO . When cultures reached conﬂuence, cells were trypsinized and seeded at a density of 3 2 Figure 1: Flowchart of the selection of subjects in the controlled 30 ×10 cells/cm in 96-well culture plates. Treatments started intervention study. 24hoursafterseeding.Alltreatmentswereperformedusing1% FBS supplemented medium. Bordo juice and wine were freeze- dietary restriction was aimed to reduce dietary phenolic driedtoremovewaterandalcoholandthendissolvedinculture compounds from blood as these compounds are typically medium at the desired concentration (w/v). Cells were exposed cleared within 48h of consumption [30]. )e intake of to these juice and wine solutions or vehicle (culture medium). energy, macronutrients, dietary ﬁber, and antioxidants be- fore the intervention was monitored using a prospective 48h 2.5.1. Determination of Intracellular ROS Production. In- dietary record. Each participant served as his own control tracellular ROS production was detected using the 2′,7′- because we compared data obtained after either juice, wine, or water consumption with the respective baseline values dichloroﬂuorescein diacetate (DCFH-DA, Sigma) as de- scribed [32]. Cellswere pretreated with Bordo juice or wine before consumption. In the day of intervention, baseline blood samples were collected after overnight fasting (12h), (solutions in culture medium, Section 2.3) or vehicle (culture medium) during 2h and then incubated in the then subjects consumed 100mL of Bordo grape juice, Bordo wine, or water. One hour after drinking, test blood samples absence (control) or presence of H O (100 µM) for 3 h 2 2 before monitoring DCF ﬂuorescence. H O was used as were collected. )is protocol was chosen based on a previous 2 2 study that revealed maximal antioxidant capacity and a positive control to induce ROS generation [33]. DCFH- DA stock solution was dissolved in DMSO at a ﬁnal phenolic concentration in serum 1h after the intake of the fruit or beverage [30]. No food was provided during this concentration of 10mM and stored at −20 C protected from light. Before cells were treated, DCFH-DA was di- period. luted to 100 μM using 1% FBS-supplemented medium solution. After addition of DCFH-DA, cells were in- 2.4.3. Blood Collection and Analyses. Fasting venous blood cubated at 37 C, with 5% CO , and protected from light samples were collected through aseptic venipuncture into exposure for 1h. After DCFH internalization, the medium heparinized tubes and EDTA-containing tubes that were was replaced by fresh 1% FBS-supplemented medium centrifuged (1500 ×g, 10min) to yield plasma for thio- solution. When internalized, ROS cause DCFH oxidation, barbituric acid reactive species (TBARS), ABTS, and FRAP and it becomes a ﬂuorophore (DCF), which was quantiﬁed 4 Journal of Nutrition and Metabolism Table 2: Baseline characteristics of subjects enrolled in the study. Participants (n �15) Male (n �5) Female (n �10) 23.8 ±4.0 24.3 ±4.0 Age (years) (19–30) (22–33) 79.0 ±14.7 61.0 ±5.8 Weight (kg) (65–95) (54–70) 180.6 ±0.1 160.0 ±0.1 Height (cm) (169–191) (154–172) 24.3 ±4.5 23.4 ±2.5 BMI (kg/m ) (20.1–30.3) (20.2–28.7) 117.2 ±13.6 115.8 ±9.8 SBP (mmHg) (110–132) (100–130) 81.6 ±8.2 76.9 ±4.7 DBP (mmHg) (70–90) (70–80) Practice of physical activity at least once a week (%) 2 (40%) 3 (30%) Physical inactivity (%) 3 (60%) 7 (70%) Data are expressed as means±SEM (minimum–maximum), except for the physical activity/inactivity that was expressed as the number of participants (%). BMI �body mass index, SBP �systolic blood pressure, and DBP �diastolic blood pressure. using a SpectraMAX i3 (Molecular Devices) ﬂuorescence healthy individuals, 5 men and 10 women, respectively, with plate reader (Ex/Em � 485/532nm). Fluorescence was mean age 24.1±3.7 and body mass index of 23.7±3.2kg/m monitored, and the area under the curve (AUC) of were included. )e systolic and diastolic blood pressures of ﬂuorescence versus time was calculated. participants were within the intervals of optimal and normal blood pressures according to the Brazilian Society of Hy- pertension, Brazilian Society of Cardiology, and Brazilian 2.5.2. Metabolic Mitochondrial Viability. Metabolic mito- Society of Nephrology [36] and according to US-American chondrial viability was assessed by the MTT (3-(4,5- Hypertension Guideline [37]. dimethylthiazol-2-yl)-2,5-diphenyl tetrazolium bromide) assay as previously described [34]. SH-SY5Y cells were 3.2. Bordo Grape Juice and Wine Antioxidant Activity In plated onto 96-well plates and exposed to Bordo juice or wine (solutions in culture medium, see Section 2.3) or Vitro. )e chemical composition of Bordo grape juice and wine in the same serving size (portion) administered to vehicle (culture medium) during 24h. Parallel sets of wells healthy individuals in this study is shown in Table 3. Grape were run in the absence or presence of H O (100 µM) (co- 2 2 juice and wine showed high amounts of total phenolic exposure scheme with juice/wine), which was used as content, but wine had higher amount than grape juice (Table 3, a positive control to induce cell death [35]. )en, cells p <0.05). )e concentration of total monomeric anthocyanins were incubated with MTT for 45min at 37 C in a hu- and total ﬂavonols was also higher in wine compared with midiﬁed 5% CO atmosphere. )e medium was then grape juice (Table 3, p <0.05). removed, and plates were shaken with DMSO for 30min. )e antioxidant activities were elevated in the two grape )e optical density of each well was measured at 550nm beverages used in this study. Bordo wine showed higher (test) and 690nm. antioxidant capacity by the ABTS method, determined by ·+ the decolorization of the ABTS , through measuring the 2.6. Statistical Analysis. All the analyses were performed in reductionofthe radicalcation asthepercentageinhibition of triplicate. Results were analyzed using the Statistica software absorbance at 734nm, when compared with grape juice package (StatSoft Inc., Tulsa, Okla, USA) and expressed as (Table 3, p <0.05). On the other hand, the wine antioxidant mean ±SEM. )e parameters of the juice and wine were capacity assessed by the FRAP method, based on the ferric ion compared by the Student’s t-test. )e eﬀects of wine, juice, +3 reduction (Fe ) capacity, did not diﬀer from juice (Table 3, and water intake on blood parameters were evaluated by the p <0.05). paired t-test to compare baseline versus test data (intragroup comparison) and by analyses of variance followed by Tukey’s 3.3. Acute Consumption of Bordo Juice and Wine. After the test for intergroup comparison. Signiﬁcance was set at consumption of Bordo grape juice and wine, serum levels of p <0.05. TBARS were, respectively, decreased by 22.3% and 25.7% compared with baseline values (p <0.001), but no signiﬁcant 3. Results diﬀerences were observed between Bordo juice and wine 3.1. Characteristics of the Subjects. General characteristics of (Figure 2(a)). Changes in TBARS levels after juice and wine the study group are presented in Table 2. Fifteen apparently intake were signiﬁcantly diﬀerent from changes observed Journal of Nutrition and Metabolism 5 Table 3: Phenolic composition and in vitro antioxidant activity of the Bordo grape juice and wine. Parameter Bordo juice Bordo wine b a Total polyphenol index (µmol GAE/100mL) 184.2 ±13.1 371.3 ±9.6 Total anthocyanins (µmol malvidin-3- b a 17.5 ±22.5 66.74 ±10.2 glucoside/100mL) b a Total ﬂavonols (µmol catechin/100mL) 84.5 ±9.7 93.6 ±4.6 Total antioxidant activity b a ABTS (µmol TEAC/100mL) 316.5 ±14.6 448.7 ±12.1 a a FRAP (µmol TEAC/100mL) 234.6 ±9.5 234.9 ±7.1 a,b Values are means ±SEM of determinations in triplicate. Diﬀerent superscript letters denote signiﬁcant diﬀerences (Tukey’s test, p <0.05). GAE �gallic acid equivalent; TEAC �Trolox equivalent antioxidant capacity. after water intake (p <0.05), which increased (13.6%) combination with Bordo grape juice, we observed that all TBARS levels compared with baseline values (p <0.001). tested concentrations (250–1000 μg/mL) of grape juice A signiﬁcant increase in the antioxidant capacity levels, protected against H O -induced cell death (Figure 3(c); 2 2 measured by ABTS and FRAP assays, was found 1h after the p <0.001). However, Bordo wine at 1000 μg/mL signiﬁcantly consumption of Bordo juice (9.1% and 14.1%, resp.) and (p <0.001) reduced cell viability in the absence of H O 2 2 wine (7.8% and 12.5%, resp.), compared with baseline values (Figure 3(d)). In the presence of H O , only 250–500 μg/mL 2 2 (Figures 2(b) and 2(c); p <0.05). Changes in ABTS and of Bordo wine protected against cytotoxicity (p <0.01 and FRAP levels after juice and wine intake were signiﬁcantly p <0.05), whereas 1000 μg/mL of Bordo grape wine induced (p <0.05) diﬀerent from changes observed after water in- further cytotoxicity compared with vehicle-H O (Figure 2 2 take, which decreased ABTS (9.7%; p <0.001) and FRAP 3(d), p <0.001). values (9.8%; p <0.05) compared with baseline values. Signiﬁcant changes were detected in the mean values of 4. Discussion serum glucose and uric acid after the intake of the Bordo grape juice and wine (Table 4). Blood glucose was reduced Polyphenols, which have high antioxidant capacity and exhibit strong protective eﬀect against cellular oxidative after consumption of Bordo juice and wine compared with baseline values (p <0.01). Furthermore, wine triggered damage, are the most abundant secondary metabolites in plants and antioxidants in human diet [38]. Grapes and a greater decrease in blood glucose levels compared with water intake (−8.8% versus −2.0%; p <0.05). Consumption derivatives contain high amounts of phenolic compounds, mainly ﬂavonoids. In fact, high levels of phenolic com- of wine had a diﬀerent eﬀect in blood uric acid levels compared with water and juice (p <0.05; Table 4). Com- pounds were found in samples ofBordo grape juice and wine used in the present study, which may contribute to the high pared with baseline values, blood uric acid levels were in- creased after the consumption of Bordo grape wine antioxidant potential of those beverages. Furthermore, many of these compounds exhibit multiple biological activities, (p <0.05) but decreased after the consumption of water and Bordo grape juice (p <0.01). and these functions are mainly attributed to their antioxi- dant and antiradical activity [39, 40]. )e main ﬁnding of our study is that the consumption of Bordo grape juice and 3.4. Neuroprotective Eﬀects of Bordo Juice and Wine. We wine yielded similar antioxidant eﬀects by increasing total investigated whether Bordo grape juice and wine could antioxidant capacity and reducing lipid oxidation, despite prevent H O -induced intracellular ROS production in the higher content of phenolic compounds and in vitro 2 2 SH-SY5Y cells and promote neuroprotective actions (Figure 3). antioxidant activity of Bordo wine compared with juice. Our results showed that exposure to H O increased the Concerning the study of antioxidant eﬀectiveness, the 2 2 intracellular ROS production (Figures 3(a) and 3(b)). use of diﬀerent in vitro models has been recommended, due However, 500 and 1000 µg/mL of Bordo grape juice sig- to the diﬀerences betweenthe various free radical scavenging niﬁcantly (p <0.05 and p <0.001) reduced H O -induced assays [41, 42]. )us, antioxidant activity of Bordo juice and 2 2 wine were assessed using the ABTS method, which measures production of ROS (Figure 3(a)), whereas 1000 µg/mL of Bordo grape wine had a prooxidant eﬀect per se by in- the scavenging of the ABTS radical cation, and the FRAP method, which measures the ability to reduce the ferric- creasing the DCF levels in the absence of H O (p <0.001; 2 2 Figure 3(b)). Bordo grape wine was unable to prevent the tripyridyl triazine complex (Fe III-TPX) to ferrous complex increase in ROS induced by H O and only 1000 µg/mL of (FeII-TPZ) under acidic conditions. In our study, the ABTS 2 2 Bordo grape wine induced further increase in ROS levels assay showed signiﬁcantly higher values compared with compared with H O (Figure 3(b), p<0.05). FRAP values, mainly for wine. However, the reaction of 2 2 To determine whether Bordo grape juice and wine could FRAP method may not be complete even several hours after protect against oxidative stress-induced cell death, the SH- the initiation of the reaction, mainly because of subsequent SY5Y cell line was used as an in vitro model and H O as dimerizations and polymerizations [43]. Drawbacks of this 2 2 prooxidant insult. After 24h of H O exposure in method are concerned with compounds that have low redox 2 2 6 Journal of Nutrition and Metabolism 25.0 15.0 ∗∗∗ 20.0 ∗∗∗ ∗∗∗ 10.0 15.0 10.0 5.0 5.0 0.0 0.0 −5.0 −10.0 −5.0 −15.0 −20.0 −10.0 −25.0 ∗∗∗ ∗∗∗ b ∗∗∗ −30.0 −15.0 Control Control Bordo juice Bordo juice Bordo wine Bordo wine (a) (b) 20.0 ∗∗∗ ∗∗∗ 15.0 10.0 5.0 0.0 −5.0 −10.0 −15.0 Control Bordo juice Bordo wine (c) Figure 2: Changes in serum TBARS levels (a) and plasma antioxidant capacity assessed by the ABTS (b) and FRAP (c) assays in humans after consumption of Bordo juice, Bordo wine, or water (control). Results are expressed as percentage of baseline values for each group ∗ ∗ ∗∗ ∗∗∗ a,b (means ±SEM, n �15). Signiﬁcantly diﬀerent from baseline (paired Student’s t-test; p <0.05, p <0.01, and p <0.001). Diﬀerent letters indicate signiﬁcant diﬀerence among interventions (Tukey’s test, p <0.05). potential and can reduce the Fe III even though they do not showed a signiﬁcant (p <0.05) decrease in serum lipid behave as antioxidants in vivo [44, 45], interfering com- peroxidation after the intake of both Bordo juice and wine pounds that can absorb at the same wavelength and the assay compared with baseline values, and this eﬀect was not being performed at a nonphysiological pH. observed after water intake. Similar eﬀects were previously Numerous indices and methods have been used to assess reported in human serum or plasma after the intake of oxidative stress, deﬁned as an imbalance between the pro- polyphenol-rich foods, and according to these studies, the duction of ROS and their removal by antioxidants. Among decrease in lipid peroxidation probably occurred due to the various indices, products of lipid peroxidation are the most quick absorption of polyphenols into the bloodstream common group used to evaluate the individual oxidative [15, 48,49].)ese phytochemicals areknownto prevent lipid (antioxidant/prooxidant) status [5, 45]. Lipid peroxidation is peroxidation by scavenging peroxyl radicals [15, 49, 50]. a result of complex reactions which yield compounds that Moreover, evidence from in vitro studies indicates that can be determined as TBARS [46]. According to Garc´ıa- resveratrol, which is among the most important grape Alonso et al. [47] a reduction in the lipid oxidation might be polyphenols [51], can be accumulated into erythrocytes and associated with the intake of phenolic beverages. Our results activates the erythrocyte plasma membrane redox system TBARS (% change versus baseline) FRAP (% change versus baseline) ABTS (% change versus baseline) Journal of Nutrition and Metabolism 7 Table 4: Glucose and uric acid levels in healthy individuals at baseline and after the interventions with Bordo grape juice, Bordo wine, and water (control). Intervention samples Bordo grapes Biochemical parameters Control Bordo juice Bordo wine Serum glucose (mg/dL) Baseline 84.1 ±5.8 74.4 ±5.5 82.2 ±7.1 1h after intervention 82.3 ±5.5 69.3 ±6.2 74.8 ±7.4 b ab a ∗∗ ∗∗ Change versus baseline (%) −2.0 ±1.5 −6.7 ±1.7 −8.8 ±2.0 Uric acid (mg/dL) Baseline 4.8 ±1.9 4.8 ±1.6 4.4 ±1.2 1h after intervention 4.6 ±1.8 4.6 ±1.5 4.6 ±1.2 b b a ∗∗ ∗∗ ∗ Change versus baseline (%) −4.6 ±1.4 −4.1 ±1.1 4.2 ±1.2 a,b ∗ ∗ ∗∗ Results are expressed as means ±SEM (n �15). Signiﬁcantly diﬀerent from baseline (paired Student’s t-test; p <0.05 and p<0.01). Diﬀerent letters indicate signiﬁcant diﬀerence among interventions (Tukey’s test, p<0.05). [52]. Resveratrol may function as an electron donor for this an eﬀect could be a consequence of increased uric acid levels enzymatic system, which reduces extracellular oxidants and [57]. Uric acid has been demonstrated to be one of the major recycles oxidized ascorbate, thereby contributing to coun- contributors to the antioxidant capacity in human serum teract extracellular oxidative processes [52]. In addition, in [48] and particularly contributes to the antioxidant capacity of serum assessed by the FRAP assay [18, 29]. Fructose from silico studies revealed that other grape polyphenols, namely, quercetin, epigallocatechin gallate, catechin, and epi- ﬂavonoid-rich fruits has been demonstrated to be re- catechin, are able to interact and donate protons to the sponsible for increasing plasma uric acid levels [57]. human NADH-cytochrome b5 reductase, which is a com- However, in the present study, the consumption of 100mL ponent of the erythrocyte plasma membrane redox system of Bordo juice or wine did not increase glycemia. Moreover, [53]. )ese mechanisms may underline the antioxidant ef- we demonstrated that Bordo grape juice decreased blood fect of Bordo juice and wine in serum as observed in the uric acid levels, indicating that the increase in antioxidant present study. capacity of serum was promoted by grape juice antioxidants Short-term studies involving the consumption of poly- and not by urate. Similar results were recently found after acute consumption of grape juices [18]. On the other hand, phenol beverages have reported acute increases in the an- tioxidant capacity of plasma or serum, which have usually we found an increase in serum levels of uric acid after Bordo wine consumption that was parallel to the increase in plasma been attributed to the high levels of polyphenolic antioxi- dants provided by plants [5, 18, 54, 55]. Our ﬁndings showed antioxidant capacity (FRAP and ABTS assays) and to the signiﬁcant (p <0.05) improvement in antioxidant status decrease in plasma lipid oxidation. Similar results were after the consumption of Bordo grape juice and wine, in found for port wine consumption [58]. opposite to the ingestion of control beverage (water), Assays using living cells have proven to be useful for therefore conﬁrming our hypothesis that polyphenols routine testing of various products, producing reliable re- present in the Bordo juice and wine favorably inﬂuence the sults for the identiﬁcation of biological activities, including antioxidant capacity in vivo. Malvidin-3-glucoside (M-3-G), antioxidant capacity [59]. Excessive ROS production is as- which is the most abundant anthocyanin in grapes and grape sociated with disruptionof cell cycleregulatory mechanisms. In the present study, we used the human neuron-like cells products, has similar bioavailability after the ingestion of red wine or dealcoholized red wine, indicating that ethanol in SH-SY5Y, which were challenged with H O that is among 2 2 red wine does not seem to aﬀect the absolute uptake and the major physiologically relevant ROS species [60, 61]. plasma concentrations of M-3-G [56]. Furthermore, in- Bordo juice inhibited the production of RS and the loss of creases in plasma anthocyanin concentrations after the cell viability induced by H O . In contrast, Bordo wine had 2 2 consumption of either red wine or dealcoholized red wine only a small protective eﬀect against the loss of cell viability were about two times lower than those measured after at intermediate concentrations but increased RS production consumption of red grape juice. )ese authors did not and promoted loss of cell viability per se at the highest measure the antioxidant capacity after beverage intake. We concentration. Such an eﬀect was not related to the ethanol found that anthocyanin concentration in Bordo wine was 3 content of wine as ethanol was removed by freeze-drying times higher than in Bordo grape juice, but both beverages before the experiment. were similarly eﬀective to increase blood antioxidant ca- )e direct radical scavenging action of polyphenols pacity and reduce lipid oxidation in humans after requires the presence of the antioxidant at the exact place consumption. where such radicals are formed. Polyphenols protect bi- )e hypothesis that ﬂavonoids are responsible for the ological membranes from oxidation as they interact with the increase in plasma antioxidant capacity after the intake of lipid phase of the membrane with a tendency to incorporate ﬂavonoid-richfoods has been disputed by evidence that such into the outer hydrophilic portion of the phospholipid 8 Journal of Nutrition and Metabolism ∗∗∗ ∗∗∗ 0 0 Control H O Control H O 2 2 2 0 500 0 500 250 1000 250 1000 (a) (b) 150 150 100 100 ∗∗∗ ∗∗∗ ∗∗ 50 50 ∗∗∗ 0 0 Control H O Control H O 2 2 2 0 500 0 500 250 1000 1000 (c) (d) Figure 3: Eﬀect of Bordo grape juice and wine on H O -induced cytotoxicity in SH-SY5Y cells. (a) DCF ﬂuorescence of cells treated 2 2 with Bordo grape juice. (b) DCF ﬂuorescence of cells treated with Bordo grape wine. (c) Cell viability of cells treated with Bordo grape juice. (d) Cell viability of cells treated with Bordo grape wine. Cells were exposed to 0 (vehicle), 250, 500, and 1000 µg/mL of Bordo juice or Bordo ∗ ∗∗ wine during 5h (panels (a) and (b)) or 24h (panels (c) and (d)). Two-way ANOVA was applied to all data. p <0.05, p <0.01, and ∗∗∗ p <0.001 versus the respective vehicle group. bilayer [60]. )e antioxidant components of fruits and may be attributed to diﬀerences in the cultivars used to vegetables, such as polyphenols, have been found to possess prepare the wines. Another explanation for the diﬀerent properties which play a role in protecting cellular macro- eﬀect of Bordo wine and juice in the culture assays could be molecules from ROS-induced damage [3, 4]. Many grape the higher concentration of phenolic compounds in Bordo compounds could be responsible for the grape juice anti- wine compared with Bordo juice, which could exert oxidant activity against H O -induced damage in SH-SY5Y a prooxidant eﬀect. In fact, Long et al. [63] showed that 2 2 cells. Polyphenol composition of wines shows higher addition of phenolic compounds, especially epigallocatechin complexity when compared with their corresponding juice and epigallocatechin gallate, to the cell culture media rapidly generates substantial amounts of H berries because during the winemaking and maturation O . )is eﬀect was dose- 2 2 processes, there are numerous reactions involving phenolic dependent and signiﬁcant amounts of H O (200–400 µM) 2 2 compounds (enzymatic and chemical oxidation reactions, have beenshowntobe formedafterthe addition ofphenolics condensation reactions, hydrolysis, etc.). We propose that at concentrations ≥100 µM. wine fermentation process generates compounds that ex- )e small number of individuals studied may be con- hibit prooxidant eﬀects at high concentrations and would be sidered a limitation of the present study. However, it should responsible for the overproduction of RS induced by the be noted that all the analyses were paired comparisons, highest wine concentration (1mg/mL) in SH-SY5Y cells. which has strong statistical power. In conclusion, the high Conversely, commercial red wine from China exhibited amount of phenolic compounds found in samples of Bordo neuroprotective eﬀects against H O -induced oxidative grape juice and wine used in the present study may con- 2 2 stress in SH-SY5Y cells upto 4mg/mL [62]. )is discrepancy tribute to the high in vitro antioxidant potential of those Cell viability (% of control) DUF ﬂuorescence (% of control AUC) Cell viability (% of control) DUF ﬂuorescence (% of control AUC) Journal of Nutrition and Metabolism 9 [9] K. B. Pandey and S. I. Rizvi, “Markers of oxidative stress in beverages. 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Publisher: Hindawi Publishing Corporation
Copyright: Copyright © 2018 Cristiane Copetti et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
ISSN: 2090-0724
eISSN: 2090-0732
DOI: 10.1155/2018/4384012
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Abstract

Hindawi Journal of Nutrition and Metabolism Volume 2018, Article ID 4384012, 11 pages https://doi.org/10.1155/2018/4384012 Research Article Acute Consumption of Bordo Grape Juice and Wine Improves Serum Antioxidant Status in Healthy Individuals and Inhibits Reactive Oxygen Species Production in Human Neuron-Like Cells 1 1 1 Cristiane Copetti , Fernanda Wouters Franco , Eduarda da Rosa Machado , 2 1 3 Marcela Bromberger Soquetta, Andre´ia Quatrin , Vitor de Miranda Ramos , 3 1 1 Jose´ Cla´udio Fonseca Moreira, Tatiana Emanuelli , Cla´udia Kaehler Sautter, and Neidi Garcia Penna Department of Food Technology and Science, Center of Rural Sciences, Federal University of Santa Maria (UFSM), 1000 Roraima Avenue, 97105-900 Santa Maria, RS, Brazil Department of Chemical Engineering, Center of Technology, Federal University of Santa Maria (UFSM), 1000 Roraima Avenue, 97105-900 Santa Maria, RS, Brazil Department of Biochemistry, Center of Oxidative Stress Research (CEEO), Federal University of Rio Grande do Sul (UFRGS), 2600 Ramiro Barcelos Street–Annex, 90035-003 Porto Alegre, RS, Brazil Correspondence should be addressed to Cristiane Copetti; copetti.cris@gmail.com Received 4 September 2017; Accepted 30 November 2017; Published 1 March 2018 Academic Editor: Michael B. Zemel Copyright © 2018 Cristiane Copetti et al. )is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Few studies investigated the biological eﬀects of American grape cultivars. We investigated the metabolic response after acute consumption of grape juice or wine fromBordo grapes (Vitis labrusca) ina placebo-controlledcrossover study with ﬁfteen healthy volunteers. Blood samples were collected 1 hour after the intake of 100mL of water, juice, or wine to measure TBARS, ABTS, FRAP, glucose, and uric acid levels. To evaluate diﬀerences in cellular response, intracellular reactive species production (DCFH-DA) and metabolic mitochondrial viability (MTT) were assessed after exposure of human neuron-like cells (SH-SY5Y) to juice or wine. Glycemia was reduced after juice or wine consumption, whereas blood levels of uric acid were reduced after juice consumption but increased after wine consumption. Juice and wine consumption reduced plasma lipid peroxidation and increased plasma antioxidant capacity (ABTS and FRAP assays). Furthermore, juice inhibited H O -induced intracellular 2 2 production of reactive species (RS) and increased the viability of SH-SY5Y cells. In contrast, wine (dealcoholized) exhibited a per se eﬀect by inducing the production of RS and reducing cell viability. )ese results indicate a positive impact of acute consumption of Bordo juice and wine on human oxidative status, whereas only juice had protective eﬀects against oxidative stress-induced cytotoxicity. mitochondria in brain cells increases the generation of re- 1. Introduction active species [2]. Oxidative stress is caused by the insuﬃcient capacity of Fruits and vegetables have many bioactive compounds biological systems to neutralize the excessive production of such as polyphenols, which have antioxidant properties with reactive species [1], which leads to oxidative damage in cells. a role in the protection of cellular macromolecules against Neuronal cells are particularly susceptible to reactive oxygen oxidative damage induced by ROS and RNS [3–5]. )ere is species (ROS) and reactive nitrogen species (RNS) due to increasing evidence that polyphenols may protect cell their high metabolic activity, low antioxidant capacity, and constituents against oxidative damage and, therefore, limit their nonreplicative nature. Furthermore, the abundance of the risk of various degenerative diseases associated with 2 Journal of Nutrition and Metabolism oxidative stress [6]. Studies have repeatedly shown an which grape is crushed and then heated to at least 65 C in inverse association between the risk of several chronic a hot macerator. Next, commercial pectolytic enzymes are ° ° human diseases and the consumption of polyphenol-rich added and must be kept between55 C and 60 C during 1-2h. diet [7]. )e phenolic group of polyphenols can accept an )e extracted juice is then clariﬁed, pasteurized, and bottled electron to form relatively stable phenoxyl radicals, [23]. Bordo wine was obtained from viniﬁcation process by thereby disrupting chain oxidative reactions in cellular the coupled dispositive to the crushing machine that is called components. It is well established that polyphenol-rich dewaxing. In winemaking of red wine, grape skin remains foods and beverages may increase plasma antioxidant inside tanks during fermentation for extraction of antho- capacity [8, 9]. cyanin pigments [24]. Grapes contain high levels of polyphenols, which have been demonstrated to reduce oxidative stress, inﬂammatory 2.2. Determination of Bioactive Compounds in Bordo Juice and response, and the oxidation of low density lipoprotein Wine. )e total phenolic content was determined at 760nm cholesterol (LDL-c), while inhibiting platelet aggregation using the Folin–Ciocalteumethodand gallicacidasstandard and improving protection against atherothrombotic epi- [25]. Total anthocyanin content was assessed at 520nm as sodes. Such actions promote beneﬁcial eﬀects on coronary the diﬀerence of absorbance before and after sample heart disease (CHD) and atherosclerosis [10–12]. Red wines decoloration using sodium bisulﬁte at pH 0.8 and was are rich in polyphenols, such as phenolic acids (gallic acid, expressed as mg of malvidin-3-glucoside/L [26]. )e total caﬀeic acid, p-coumaric acid, and others), stilbenes (trans- ﬂavonoid content was estimated at 510nm using a standard resveratrol), and ﬂavonoids (catechin, epicatechin, querce- curve of catechin (0–200mg/L) [27]. tin, rutin, myricetin, and others) [13]. )erefore, a regular consumption of red wine has been linked with the “French paradox,” which explains the apparent compatibility of 2.3. Antioxidant Capacity of Bordo Juice and Wine. )e a high-fat diet with a low mortality from CHD. Also, current antioxidant capacity of grape juice and red wine were de- evidence suggests that wine consumption is correlated with termined using the 2,2′-azino-bis (3-ethylbenzothiazoline- a reduction in the incidence of neurodegenerative diseases 6-sulphonic acid) (ABTS) and ferric reducing antioxidant associated to oxidative stress such as Alzheimer’s and power (FRAP) methods as described by Re et al. [28] and Parkinson’s disease [14]. Grape juice is a natural and Benzie and Strain [29], respectively. )e ABTS assay is nonalcoholic beverage that contains sugars, minerals, assessed at 764nm and is based on the ability of the sample ·+ and phenolic compounds like anthocyanins, among which to scavenge the cation radical ABTS . )e FRAP assay is malvidin 3,5-diglucoside is the major one [15]. )is beverage assessed at 620nm and is based on the reduction of ferric- has been shown to exert antioxidant activity in vitro and tripyridyltriazine (Fe III-TPTZ) by antioxidants present in in vivo, as well as hypolipidemic and anti-inﬂammatory the samples forming ferrous-tripyridyltriazine (Fe II-TPTZ), eﬀects in rats and humans [16–18]. a blue-colored product. Trolox was used in the calibration However, few studies have compared the eﬀects of curve. wine and juice consumption in biological parameters of humans, and these studies used European grape species 2.4. In Vivo Study (Vitis vinifera) [19–21]. In contrast, the biological eﬀects of wine and juice from American grape species 2.4.1. Participants. )e study design was approved by the (Vitis labrusca) have not been compared. )is investigation is Ethics Committee of Federal University of Santa Maria particularly interesting as the red grape cultivar “Bordo” (CAAE 39197614.3.0000.5346), and all subjects signed (V. labrusca), which is the most important grape cultivated in a written agreement before participating. Fifteen healthy Brazil [15], has been recently demonstrated to exhibit volunteers, with mean age 24.0 ±3.6, were recruitedfrom the higher content of phenolic compounds and in vitro anti- University staﬀ. )e health status and medical history of oxidant capacity than V. vinifera species [22]. In the present volunteers were examined by a structured interview for study, we compared the biological eﬀects of juice and wine inclusion or exclusion according to the criteria shown in from “Bordo” grapes (V. labrusca L) by assessing blood Table 1. antioxidant response after human consumption and the oxidative cellular response in human neuron-like cells (SH-SY5Y). 2.4.2. Study Design. In this crossover-controlled clinical study, 15 volunteers were included, 10 women (67%) and 5 men (33%). All participants received the three treatments, 2. Materials and Methods namely, Bordo grape juice, Bordo wine, and water (control) 2.1. Bordo Grape Juice and Wine. )e commercial samples of with a washout period of 1 week between treatments. )e Bordo grape juice and Bordo wine were produced by sequence of the treatments was randomized among the a winemaker (Casa Perini, Farroupilha, RS, Brazil). )e participants as depicted in Figure 1. grape fruits used to prepare juice and wine were harvested in Participants were oriented to follow a low-antioxidant ° ° Farroupilha (29 13′ 30″ S, 51 20′ 52″ W, altitude 783m), in diet for 48h prior to the day of intervention, avoiding some the State of Rio Grande do Sul, Brazil, on January 2014. fruits, vegetables, and juices, mainly rich in anthocyanins, Bordo grape juice was prepared by the enzymatic method, in tea, coﬀee, cocoa foodstuﬀs, and alcoholic beverages. )is Journal of Nutrition and Metabolism 3 Table 1: Selection criteria of study participants. Inclusion criteria Exclusion criteria Apparently healthy individuals Pregnant and lactating women Age 18–35 years old Alcoholic and smokers BMI between 18.5 and 29.9kg/m Vegetarian diet Regular use of antioxidants or vitamin supplements Chronic diseases (cardiovascular diseases, hypertension, diabetes, liver diseases, SBP<140mmHg and DBP≤90mmHg cancer, or allergy); gastrointestinal disorders or known metabolic diseases; infections or inﬂammatory processes visible or known in the three months prior to the study BMI �body mass index, SBP �systolic blood pressure, and DBP �diastolic blood pressure. analysis. Blood collected in tubes without additives was Volunteers screened for eligibility (n= 30) centrifuged (1500 ×g, 10min) to yield serum for analysis of Excluded (n= 4) uric acid and glucose. Serum and plasma samples were Declined (n= 11) stored at −80 C until analysis. Uric acid and glucose were determined in serum using Subjects entered the study (n= 15) commercially available enzymatic kits (Bioclin, Belo Hori- Randomization 1-week washout zonte, Brazil). Lipid peroxidation was determined by measurement of TBARS at 535nm in plasma [31]. )e antioxidant capacity of plasma was assessed by the ABTS Bordo grape juice Bordo grape juice Bordo grape juice [28] and FRAP assays [29]. (n= 5) (n= 5) (n= 5) Bordo wine Bordo wine Bordo wine (n= 5) (n= 5) (n= 5) 2.5. Cell Culture Assays. Human neuron-like cell line SH- SY5Y obtained from the European Collection of Authenticated Water Water Water (n= 5) (n= 5) (n= 5) Cell Cultures (ECACC) were maintained in 75cm ﬂasks containing DMEM/F12 medium (1:1) supplemented with 10% fetal bovine serum (FBS) and 1× antibiotic/antimycotic solu- tion (Sigma-Aldrich). Cells were cultured in a humidiﬁed incubator set at 37 Subjects completed the study (n= 15) C with 5% CO . When cultures reached conﬂuence, cells were trypsinized and seeded at a density of 3 2 Figure 1: Flowchart of the selection of subjects in the controlled 30 ×10 cells/cm in 96-well culture plates. Treatments started intervention study. 24hoursafterseeding.Alltreatmentswereperformedusing1% FBS supplemented medium. Bordo juice and wine were freeze- dietary restriction was aimed to reduce dietary phenolic driedtoremovewaterandalcoholandthendissolvedinculture compounds from blood as these compounds are typically medium at the desired concentration (w/v). Cells were exposed cleared within 48h of consumption [30]. )e intake of to these juice and wine solutions or vehicle (culture medium). energy, macronutrients, dietary ﬁber, and antioxidants be- fore the intervention was monitored using a prospective 48h 2.5.1. Determination of Intracellular ROS Production. In- dietary record. Each participant served as his own control tracellular ROS production was detected using the 2′,7′- because we compared data obtained after either juice, wine, or water consumption with the respective baseline values dichloroﬂuorescein diacetate (DCFH-DA, Sigma) as de- scribed [32]. Cellswere pretreated with Bordo juice or wine before consumption. In the day of intervention, baseline blood samples were collected after overnight fasting (12h), (solutions in culture medium, Section 2.3) or vehicle (culture medium) during 2h and then incubated in the then subjects consumed 100mL of Bordo grape juice, Bordo wine, or water. One hour after drinking, test blood samples absence (control) or presence of H O (100 µM) for 3 h 2 2 before monitoring DCF ﬂuorescence. H O was used as were collected. )is protocol was chosen based on a previous 2 2 study that revealed maximal antioxidant capacity and a positive control to induce ROS generation [33]. DCFH- DA stock solution was dissolved in DMSO at a ﬁnal phenolic concentration in serum 1h after the intake of the fruit or beverage [30]. No food was provided during this concentration of 10mM and stored at −20 C protected from light. Before cells were treated, DCFH-DA was di- period. luted to 100 μM using 1% FBS-supplemented medium solution. After addition of DCFH-DA, cells were in- 2.4.3. Blood Collection and Analyses. Fasting venous blood cubated at 37 C, with 5% CO , and protected from light samples were collected through aseptic venipuncture into exposure for 1h. After DCFH internalization, the medium heparinized tubes and EDTA-containing tubes that were was replaced by fresh 1% FBS-supplemented medium centrifuged (1500 ×g, 10min) to yield plasma for thio- solution. When internalized, ROS cause DCFH oxidation, barbituric acid reactive species (TBARS), ABTS, and FRAP and it becomes a ﬂuorophore (DCF), which was quantiﬁed 4 Journal of Nutrition and Metabolism Table 2: Baseline characteristics of subjects enrolled in the study. Participants (n �15) Male (n �5) Female (n �10) 23.8 ±4.0 24.3 ±4.0 Age (years) (19–30) (22–33) 79.0 ±14.7 61.0 ±5.8 Weight (kg) (65–95) (54–70) 180.6 ±0.1 160.0 ±0.1 Height (cm) (169–191) (154–172) 24.3 ±4.5 23.4 ±2.5 BMI (kg/m ) (20.1–30.3) (20.2–28.7) 117.2 ±13.6 115.8 ±9.8 SBP (mmHg) (110–132) (100–130) 81.6 ±8.2 76.9 ±4.7 DBP (mmHg) (70–90) (70–80) Practice of physical activity at least once a week (%) 2 (40%) 3 (30%) Physical inactivity (%) 3 (60%) 7 (70%) Data are expressed as means±SEM (minimum–maximum), except for the physical activity/inactivity that was expressed as the number of participants (%). BMI �body mass index, SBP �systolic blood pressure, and DBP �diastolic blood pressure. using a SpectraMAX i3 (Molecular Devices) ﬂuorescence healthy individuals, 5 men and 10 women, respectively, with plate reader (Ex/Em � 485/532nm). Fluorescence was mean age 24.1±3.7 and body mass index of 23.7±3.2kg/m monitored, and the area under the curve (AUC) of were included. )e systolic and diastolic blood pressures of ﬂuorescence versus time was calculated. participants were within the intervals of optimal and normal blood pressures according to the Brazilian Society of Hy- pertension, Brazilian Society of Cardiology, and Brazilian 2.5.2. Metabolic Mitochondrial Viability. Metabolic mito- Society of Nephrology [36] and according to US-American chondrial viability was assessed by the MTT (3-(4,5- Hypertension Guideline [37]. dimethylthiazol-2-yl)-2,5-diphenyl tetrazolium bromide) assay as previously described [34]. SH-SY5Y cells were 3.2. Bordo Grape Juice and Wine Antioxidant Activity In plated onto 96-well plates and exposed to Bordo juice or wine (solutions in culture medium, see Section 2.3) or Vitro. )e chemical composition of Bordo grape juice and wine in the same serving size (portion) administered to vehicle (culture medium) during 24h. Parallel sets of wells healthy individuals in this study is shown in Table 3. Grape were run in the absence or presence of H O (100 µM) (co- 2 2 juice and wine showed high amounts of total phenolic exposure scheme with juice/wine), which was used as content, but wine had higher amount than grape juice (Table 3, a positive control to induce cell death [35]. )en, cells p <0.05). )e concentration of total monomeric anthocyanins were incubated with MTT for 45min at 37 C in a hu- and total ﬂavonols was also higher in wine compared with midiﬁed 5% CO atmosphere. )e medium was then grape juice (Table 3, p <0.05). removed, and plates were shaken with DMSO for 30min. )e antioxidant activities were elevated in the two grape )e optical density of each well was measured at 550nm beverages used in this study. Bordo wine showed higher (test) and 690nm. antioxidant capacity by the ABTS method, determined by ·+ the decolorization of the ABTS , through measuring the 2.6. Statistical Analysis. All the analyses were performed in reductionofthe radicalcation asthepercentageinhibition of triplicate. Results were analyzed using the Statistica software absorbance at 734nm, when compared with grape juice package (StatSoft Inc., Tulsa, Okla, USA) and expressed as (Table 3, p <0.05). On the other hand, the wine antioxidant mean ±SEM. )e parameters of the juice and wine were capacity assessed by the FRAP method, based on the ferric ion compared by the Student’s t-test. )e eﬀects of wine, juice, +3 reduction (Fe ) capacity, did not diﬀer from juice (Table 3, and water intake on blood parameters were evaluated by the p <0.05). paired t-test to compare baseline versus test data (intragroup comparison) and by analyses of variance followed by Tukey’s 3.3. Acute Consumption of Bordo Juice and Wine. After the test for intergroup comparison. Signiﬁcance was set at consumption of Bordo grape juice and wine, serum levels of p <0.05. TBARS were, respectively, decreased by 22.3% and 25.7% compared with baseline values (p <0.001), but no signiﬁcant 3. Results diﬀerences were observed between Bordo juice and wine 3.1. Characteristics of the Subjects. General characteristics of (Figure 2(a)). Changes in TBARS levels after juice and wine the study group are presented in Table 2. Fifteen apparently intake were signiﬁcantly diﬀerent from changes observed Journal of Nutrition and Metabolism 5 Table 3: Phenolic composition and in vitro antioxidant activity of the Bordo grape juice and wine. Parameter Bordo juice Bordo wine b a Total polyphenol index (µmol GAE/100mL) 184.2 ±13.1 371.3 ±9.6 Total anthocyanins (µmol malvidin-3- b a 17.5 ±22.5 66.74 ±10.2 glucoside/100mL) b a Total ﬂavonols (µmol catechin/100mL) 84.5 ±9.7 93.6 ±4.6 Total antioxidant activity b a ABTS (µmol TEAC/100mL) 316.5 ±14.6 448.7 ±12.1 a a FRAP (µmol TEAC/100mL) 234.6 ±9.5 234.9 ±7.1 a,b Values are means ±SEM of determinations in triplicate. Diﬀerent superscript letters denote signiﬁcant diﬀerences (Tukey’s test, p <0.05). GAE �gallic acid equivalent; TEAC �Trolox equivalent antioxidant capacity. after water intake (p <0.05), which increased (13.6%) combination with Bordo grape juice, we observed that all TBARS levels compared with baseline values (p <0.001). tested concentrations (250–1000 μg/mL) of grape juice A signiﬁcant increase in the antioxidant capacity levels, protected against H O -induced cell death (Figure 3(c); 2 2 measured by ABTS and FRAP assays, was found 1h after the p <0.001). However, Bordo wine at 1000 μg/mL signiﬁcantly consumption of Bordo juice (9.1% and 14.1%, resp.) and (p <0.001) reduced cell viability in the absence of H O 2 2 wine (7.8% and 12.5%, resp.), compared with baseline values (Figure 3(d)). In the presence of H O , only 250–500 μg/mL 2 2 (Figures 2(b) and 2(c); p <0.05). Changes in ABTS and of Bordo wine protected against cytotoxicity (p <0.01 and FRAP levels after juice and wine intake were signiﬁcantly p <0.05), whereas 1000 μg/mL of Bordo grape wine induced (p <0.05) diﬀerent from changes observed after water in- further cytotoxicity compared with vehicle-H O (Figure 2 2 take, which decreased ABTS (9.7%; p <0.001) and FRAP 3(d), p <0.001). values (9.8%; p <0.05) compared with baseline values. Signiﬁcant changes were detected in the mean values of 4. Discussion serum glucose and uric acid after the intake of the Bordo grape juice and wine (Table 4). Blood glucose was reduced Polyphenols, which have high antioxidant capacity and exhibit strong protective eﬀect against cellular oxidative after consumption of Bordo juice and wine compared with baseline values (p <0.01). Furthermore, wine triggered damage, are the most abundant secondary metabolites in plants and antioxidants in human diet [38]. Grapes and a greater decrease in blood glucose levels compared with water intake (−8.8% versus −2.0%; p <0.05). Consumption derivatives contain high amounts of phenolic compounds, mainly ﬂavonoids. In fact, high levels of phenolic com- of wine had a diﬀerent eﬀect in blood uric acid levels compared with water and juice (p <0.05; Table 4). Com- pounds were found in samples ofBordo grape juice and wine used in the present study, which may contribute to the high pared with baseline values, blood uric acid levels were in- creased after the consumption of Bordo grape wine antioxidant potential of those beverages. Furthermore, many of these compounds exhibit multiple biological activities, (p <0.05) but decreased after the consumption of water and Bordo grape juice (p <0.01). and these functions are mainly attributed to their antioxi- dant and antiradical activity [39, 40]. )e main ﬁnding of our study is that the consumption of Bordo grape juice and 3.4. Neuroprotective Eﬀects of Bordo Juice and Wine. We wine yielded similar antioxidant eﬀects by increasing total investigated whether Bordo grape juice and wine could antioxidant capacity and reducing lipid oxidation, despite prevent H O -induced intracellular ROS production in the higher content of phenolic compounds and in vitro 2 2 SH-SY5Y cells and promote neuroprotective actions (Figure 3). antioxidant activity of Bordo wine compared with juice. Our results showed that exposure to H O increased the Concerning the study of antioxidant eﬀectiveness, the 2 2 intracellular ROS production (Figures 3(a) and 3(b)). use of diﬀerent in vitro models has been recommended, due However, 500 and 1000 µg/mL of Bordo grape juice sig- to the diﬀerences betweenthe various free radical scavenging niﬁcantly (p <0.05 and p <0.001) reduced H O -induced assays [41, 42]. )us, antioxidant activity of Bordo juice and 2 2 wine were assessed using the ABTS method, which measures production of ROS (Figure 3(a)), whereas 1000 µg/mL of Bordo grape wine had a prooxidant eﬀect per se by in- the scavenging of the ABTS radical cation, and the FRAP method, which measures the ability to reduce the ferric- creasing the DCF levels in the absence of H O (p <0.001; 2 2 Figure 3(b)). Bordo grape wine was unable to prevent the tripyridyl triazine complex (Fe III-TPX) to ferrous complex increase in ROS induced by H O and only 1000 µg/mL of (FeII-TPZ) under acidic conditions. In our study, the ABTS 2 2 Bordo grape wine induced further increase in ROS levels assay showed signiﬁcantly higher values compared with compared with H O (Figure 3(b), p<0.05). FRAP values, mainly for wine. However, the reaction of 2 2 To determine whether Bordo grape juice and wine could FRAP method may not be complete even several hours after protect against oxidative stress-induced cell death, the SH- the initiation of the reaction, mainly because of subsequent SY5Y cell line was used as an in vitro model and H O as dimerizations and polymerizations [43]. Drawbacks of this 2 2 prooxidant insult. After 24h of H O exposure in method are concerned with compounds that have low redox 2 2 6 Journal of Nutrition and Metabolism 25.0 15.0 ∗∗∗ 20.0 ∗∗∗ ∗∗∗ 10.0 15.0 10.0 5.0 5.0 0.0 0.0 −5.0 −10.0 −5.0 −15.0 −20.0 −10.0 −25.0 ∗∗∗ ∗∗∗ b ∗∗∗ −30.0 −15.0 Control Control Bordo juice Bordo juice Bordo wine Bordo wine (a) (b) 20.0 ∗∗∗ ∗∗∗ 15.0 10.0 5.0 0.0 −5.0 −10.0 −15.0 Control Bordo juice Bordo wine (c) Figure 2: Changes in serum TBARS levels (a) and plasma antioxidant capacity assessed by the ABTS (b) and FRAP (c) assays in humans after consumption of Bordo juice, Bordo wine, or water (control). Results are expressed as percentage of baseline values for each group ∗ ∗ ∗∗ ∗∗∗ a,b (means ±SEM, n �15). Signiﬁcantly diﬀerent from baseline (paired Student’s t-test; p <0.05, p <0.01, and p <0.001). Diﬀerent letters indicate signiﬁcant diﬀerence among interventions (Tukey’s test, p <0.05). potential and can reduce the Fe III even though they do not showed a signiﬁcant (p <0.05) decrease in serum lipid behave as antioxidants in vivo [44, 45], interfering com- peroxidation after the intake of both Bordo juice and wine pounds that can absorb at the same wavelength and the assay compared with baseline values, and this eﬀect was not being performed at a nonphysiological pH. observed after water intake. Similar eﬀects were previously Numerous indices and methods have been used to assess reported in human serum or plasma after the intake of oxidative stress, deﬁned as an imbalance between the pro- polyphenol-rich foods, and according to these studies, the duction of ROS and their removal by antioxidants. Among decrease in lipid peroxidation probably occurred due to the various indices, products of lipid peroxidation are the most quick absorption of polyphenols into the bloodstream common group used to evaluate the individual oxidative [15, 48,49].)ese phytochemicals areknownto prevent lipid (antioxidant/prooxidant) status [5, 45]. Lipid peroxidation is peroxidation by scavenging peroxyl radicals [15, 49, 50]. a result of complex reactions which yield compounds that Moreover, evidence from in vitro studies indicates that can be determined as TBARS [46]. According to Garc´ıa- resveratrol, which is among the most important grape Alonso et al. [47] a reduction in the lipid oxidation might be polyphenols [51], can be accumulated into erythrocytes and associated with the intake of phenolic beverages. Our results activates the erythrocyte plasma membrane redox system TBARS (% change versus baseline) FRAP (% change versus baseline) ABTS (% change versus baseline) Journal of Nutrition and Metabolism 7 Table 4: Glucose and uric acid levels in healthy individuals at baseline and after the interventions with Bordo grape juice, Bordo wine, and water (control). Intervention samples Bordo grapes Biochemical parameters Control Bordo juice Bordo wine Serum glucose (mg/dL) Baseline 84.1 ±5.8 74.4 ±5.5 82.2 ±7.1 1h after intervention 82.3 ±5.5 69.3 ±6.2 74.8 ±7.4 b ab a ∗∗ ∗∗ Change versus baseline (%) −2.0 ±1.5 −6.7 ±1.7 −8.8 ±2.0 Uric acid (mg/dL) Baseline 4.8 ±1.9 4.8 ±1.6 4.4 ±1.2 1h after intervention 4.6 ±1.8 4.6 ±1.5 4.6 ±1.2 b b a ∗∗ ∗∗ ∗ Change versus baseline (%) −4.6 ±1.4 −4.1 ±1.1 4.2 ±1.2 a,b ∗ ∗ ∗∗ Results are expressed as means ±SEM (n �15). Signiﬁcantly diﬀerent from baseline (paired Student’s t-test; p <0.05 and p<0.01). Diﬀerent letters indicate signiﬁcant diﬀerence among interventions (Tukey’s test, p<0.05). [52]. Resveratrol may function as an electron donor for this an eﬀect could be a consequence of increased uric acid levels enzymatic system, which reduces extracellular oxidants and [57]. Uric acid has been demonstrated to be one of the major recycles oxidized ascorbate, thereby contributing to coun- contributors to the antioxidant capacity in human serum teract extracellular oxidative processes [52]. In addition, in [48] and particularly contributes to the antioxidant capacity of serum assessed by the FRAP assay [18, 29]. Fructose from silico studies revealed that other grape polyphenols, namely, quercetin, epigallocatechin gallate, catechin, and epi- ﬂavonoid-rich fruits has been demonstrated to be re- catechin, are able to interact and donate protons to the sponsible for increasing plasma uric acid levels [57]. human NADH-cytochrome b5 reductase, which is a com- However, in the present study, the consumption of 100mL ponent of the erythrocyte plasma membrane redox system of Bordo juice or wine did not increase glycemia. Moreover, [53]. )ese mechanisms may underline the antioxidant ef- we demonstrated that Bordo grape juice decreased blood fect of Bordo juice and wine in serum as observed in the uric acid levels, indicating that the increase in antioxidant present study. capacity of serum was promoted by grape juice antioxidants Short-term studies involving the consumption of poly- and not by urate. Similar results were recently found after acute consumption of grape juices [18]. On the other hand, phenol beverages have reported acute increases in the an- tioxidant capacity of plasma or serum, which have usually we found an increase in serum levels of uric acid after Bordo wine consumption that was parallel to the increase in plasma been attributed to the high levels of polyphenolic antioxi- dants provided by plants [5, 18, 54, 55]. Our ﬁndings showed antioxidant capacity (FRAP and ABTS assays) and to the signiﬁcant (p <0.05) improvement in antioxidant status decrease in plasma lipid oxidation. Similar results were after the consumption of Bordo grape juice and wine, in found for port wine consumption [58]. opposite to the ingestion of control beverage (water), Assays using living cells have proven to be useful for therefore conﬁrming our hypothesis that polyphenols routine testing of various products, producing reliable re- present in the Bordo juice and wine favorably inﬂuence the sults for the identiﬁcation of biological activities, including antioxidant capacity in vivo. Malvidin-3-glucoside (M-3-G), antioxidant capacity [59]. Excessive ROS production is as- which is the most abundant anthocyanin in grapes and grape sociated with disruptionof cell cycleregulatory mechanisms. In the present study, we used the human neuron-like cells products, has similar bioavailability after the ingestion of red wine or dealcoholized red wine, indicating that ethanol in SH-SY5Y, which were challenged with H O that is among 2 2 red wine does not seem to aﬀect the absolute uptake and the major physiologically relevant ROS species [60, 61]. plasma concentrations of M-3-G [56]. Furthermore, in- Bordo juice inhibited the production of RS and the loss of creases in plasma anthocyanin concentrations after the cell viability induced by H O . In contrast, Bordo wine had 2 2 consumption of either red wine or dealcoholized red wine only a small protective eﬀect against the loss of cell viability were about two times lower than those measured after at intermediate concentrations but increased RS production consumption of red grape juice. )ese authors did not and promoted loss of cell viability per se at the highest measure the antioxidant capacity after beverage intake. We concentration. Such an eﬀect was not related to the ethanol found that anthocyanin concentration in Bordo wine was 3 content of wine as ethanol was removed by freeze-drying times higher than in Bordo grape juice, but both beverages before the experiment. were similarly eﬀective to increase blood antioxidant ca- )e direct radical scavenging action of polyphenols pacity and reduce lipid oxidation in humans after requires the presence of the antioxidant at the exact place consumption. where such radicals are formed. Polyphenols protect bi- )e hypothesis that ﬂavonoids are responsible for the ological membranes from oxidation as they interact with the increase in plasma antioxidant capacity after the intake of lipid phase of the membrane with a tendency to incorporate ﬂavonoid-richfoods has been disputed by evidence that such into the outer hydrophilic portion of the phospholipid 8 Journal of Nutrition and Metabolism ∗∗∗ ∗∗∗ 0 0 Control H O Control H O 2 2 2 0 500 0 500 250 1000 250 1000 (a) (b) 150 150 100 100 ∗∗∗ ∗∗∗ ∗∗ 50 50 ∗∗∗ 0 0 Control H O Control H O 2 2 2 0 500 0 500 250 1000 1000 (c) (d) Figure 3: Eﬀect of Bordo grape juice and wine on H O -induced cytotoxicity in SH-SY5Y cells. (a) DCF ﬂuorescence of cells treated 2 2 with Bordo grape juice. (b) DCF ﬂuorescence of cells treated with Bordo grape wine. (c) Cell viability of cells treated with Bordo grape juice. (d) Cell viability of cells treated with Bordo grape wine. Cells were exposed to 0 (vehicle), 250, 500, and 1000 µg/mL of Bordo juice or Bordo ∗ ∗∗ wine during 5h (panels (a) and (b)) or 24h (panels (c) and (d)). Two-way ANOVA was applied to all data. p <0.05, p <0.01, and ∗∗∗ p <0.001 versus the respective vehicle group. bilayer [60]. )e antioxidant components of fruits and may be attributed to diﬀerences in the cultivars used to vegetables, such as polyphenols, have been found to possess prepare the wines. Another explanation for the diﬀerent properties which play a role in protecting cellular macro- eﬀect of Bordo wine and juice in the culture assays could be molecules from ROS-induced damage [3, 4]. Many grape the higher concentration of phenolic compounds in Bordo compounds could be responsible for the grape juice anti- wine compared with Bordo juice, which could exert oxidant activity against H O -induced damage in SH-SY5Y a prooxidant eﬀect. In fact, Long et al. [63] showed that 2 2 cells. Polyphenol composition of wines shows higher addition of phenolic compounds, especially epigallocatechin complexity when compared with their corresponding juice and epigallocatechin gallate, to the cell culture media rapidly generates substantial amounts of H berries because during the winemaking and maturation O . )is eﬀect was dose- 2 2 processes, there are numerous reactions involving phenolic dependent and signiﬁcant amounts of H O (200–400 µM) 2 2 compounds (enzymatic and chemical oxidation reactions, have beenshowntobe formedafterthe addition ofphenolics condensation reactions, hydrolysis, etc.). We propose that at concentrations ≥100 µM. wine fermentation process generates compounds that ex- )e small number of individuals studied may be con- hibit prooxidant eﬀects at high concentrations and would be sidered a limitation of the present study. However, it should responsible for the overproduction of RS induced by the be noted that all the analyses were paired comparisons, highest wine concentration (1mg/mL) in SH-SY5Y cells. which has strong statistical power. In conclusion, the high Conversely, commercial red wine from China exhibited amount of phenolic compounds found in samples of Bordo neuroprotective eﬀects against H O -induced oxidative grape juice and wine used in the present study may con- 2 2 stress in SH-SY5Y cells upto 4mg/mL [62]. )is discrepancy tribute to the high in vitro antioxidant potential of those Cell viability (% of control) DUF ﬂuorescence (% of control AUC) Cell viability (% of control) DUF ﬂuorescence (% of control AUC) Journal of Nutrition and Metabolism 9 [9] K. B. Pandey and S. I. Rizvi, “Markers of oxidative stress in beverages. 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Saito et al., “Beneﬁcial eﬀects of grape antioxidant eﬀect in cell culture showing to be toxic at high seed extract on malondialdehyde-modiﬁed LDL,” Journal of concentration, whereas juice had antioxidant eﬀects against Nutritional Science and Vitaminology, vol. 53, no. 2, H O -induced cellular oxidative stress. Bordo grape juice 2 2 pp. 174–182, 2007. and wine can be used for improving health and as a pre- [12] I. C. Arts and P. C. Hollman, “Polyphenols and disease risk in ventive agent for oxidative stress-related diseases, but wine epidemiologic studies,” American Journal of Clinical Nutri- should be consumed in smaller doses due to the prooxidant tion, vol. 81, no. 1, pp. 317S–325S, 2005. eﬀect observed in cell culture. [13] D. Kammerer, A. Claus, R. Carle, and A. 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Acute Consumption of Bordo Grape Juice and Wine Improves Serum Antioxidant Status in Healthy Individuals and Inhibits Reactive Oxygen Species Production in Human Neuron-Like Cells

Acute Consumption of Bordo Grape Juice and Wine Improves Serum Antioxidant Status in Healthy Individuals and Inhibits Reactive Oxygen Species Production in Human Neuron-Like Cells

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Acute Consumption of Bordo Grape Juice and Wine Improves Serum Antioxidant Status in Healthy Individuals and Inhibits Reactive Oxygen Species Production in Human Neuron-Like Cells

Acute Consumption of Bordo Grape Juice and Wine Improves Serum Antioxidant Status in Healthy Individuals and Inhibits Reactive Oxygen Species Production in Human Neuron-Like Cells

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