Research Article Bioactive Flavonoids, Antioxidant Behaviour, and Cytoprotective Effects of Dried Grapefruit Peels (Citrus paradisi Macf.
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1 Oxidative Mediine and Cellular Longevity Volume 216, Artile ID , 12 pages Researh Artile Bioative Flavonoids, Antioxidant Behaviour, and Cytoprotetive Effets of Dried Grapefruit Peels (Citrus paradisi Maf.) Luia Castro-Vazquez, 1 María Elena Alañón, 2 Virginia Rodríguez-Robledo, 1 María Soledad Pérez-Coello, 1,2 Isidro Hermosín-Gutierrez, 2 María Consuelo Díaz-Maroto, 1,2 Joaquín Jordán, 3 María Franisa Galindo, 1 and María del Mar Arroyo-Jiménez 1 1 Analytial Chemistry and Food Tehnology Area, Faulty of Pharmay, University of Castilla-La Manha, 271 Albaete, Spain 2 Food Tehnology Area, Faulty of Chemistry, University of Castilla-La Manha, 271 Ciudad Real, Spain 3 Medial Sienes Department, Faulty of Mediine, University of Castilla-La Manha, 271 Albaete, Spain Correspondene should be addressed to Luia Castro-Vazquez; luiaisabel.astro@ulm.es Reeived 11 Otober 215; Revised 3 November 215; Aepted 1 Deember 215 Aademi Editor: Denis Deli Copyright 216 Luia Castro-Vazquez et al. This is an open aess artile distributed under the Creative Commons Attribution Liense, whih permits unrestrited use, distribution, and reprodution in any medium, provided the original work is properly ited. Grapefruit (Citrus paradisi Maf.) is an important ultivar of the Citrus genus whih ontains a number of nutrients benefiial to human health. The objetive of the present study was to evaluate hanges in bioative flavonoids, antioxidant behaviour, and in vitro ytoprotetive effet of proessed white and pink peels after oven-drying (45 C 6 C) and freeze-drying treatments. Comparison with fresh grapefruit peels was also assessed. Signifiant inreases in DPPH, FRAPS, and ABTS values were observed in dried grapefruit peel samples in omparison with fresh peels, indiating the suitability of the treatments for use as tools to greatly enhane the antioxidant potential of these natural byproduts. A total of thirteen flavonoids were quantified in grapefruit peel extrats by HPLC-MS/MS. It was found that naringin, followed by isonaringin, was the main flavonoid ourring in fresh, oven-dried, and freeze-dried grapefruit peels. In vivo assay revealed that fresh and oven-dried grapefruit peel extrats (45 C) exerted a strong ytoprotetive effet on SH-SY5Y neuroblastoma ell lines at onentrations ranging within.1.25 mg/ml. Our data suggest that grapefruit (Citrus paradisi Maf.) peel has onsiderable potential as a soure of natural bioative flavonoids with outstanding antioxidant ativity whih an be used as agents in several therapeuti strategies. 1. Introdution Today, there is inreasing demand for natural bioative ompounds as people express more onern about their health, espeially in onnetion with health-giving diets. Epidemiologial studies suggest that high dietary intake of phytohemials, in partiular of polyphenols, is assoiated with a redued risk of a multitude of hroni diseases. In this onnetion, fruits of the Citrus genus are reognized as being a healthful soure of bioative ompounds suh as vitamins, arotenoids, fibre, and phenoli ompounds [1 3]. Worldwide agriultural itrus prodution, inluding oranges, mandarins, lemons, bergamots, limes, pummelos, and grapefruits, has been inreasing strongly in the last deades, reahing over 1 million metri tons per year [4]. About a third of itrus fruits go to produe fresh juie or itrus-based drinks. The juie yield of itrus fruits aounts for half of the fruit weight, and hene a very large amount of pulp and peel waste is produed worldwide every year [5]. It has been found that peels are the main soures of polyphenols in itrus fruits [6]. Peel residues from sweet and bitter oranges, lemons, and mandarins have proved to
2 2 Oxidative Mediine and Cellular Longevity be an important soure of phenoli aids and flavonoids, hiefly polymethoxyflavones (PMFs), flavanones, and glyosylated flavanones [7 1]. These bioative ompounds are strongly assoiated with therapeuti properties inluding antiallergeni, antiatherogeni, anti-inflammatory, antimirobial, antiarinogeni, antithromboti, ardioprotetive, and vasodilatory effets [11 18]. Many of these pharmaologial ativities of itrus polyphenols are a onsequene of their ability to savenge reative oxygen speies (ROS) and reative nitrogen speies (RNS) [19]. Sine oxidative stress is involved in all the abovementioned pathologial onditions, the outstanding antioxidant role of natural polyphenols has reeived muh attention from many researhers. In this regard, Citrus flavonoids have reently attrated onsiderable interest as potential therapeuti agents in numerous in vitro and in vivo studies. Naringin, high levels of whih our in several varieties of itrus fruits and itrus byproduts, has demonstrated antiinflammatory, antiarinogeni, lipid-lowering, and antioxidant ativities [2 23]. Hesperidin, one of the main flavanone glyosides, whih ours in oranges, has been shown to exert a wide range of therapeuti effets suh as antioxidant, antiinflammatory, and antiarinogeni properties [2]. Moreover, it has been found to signifiantly redue ROS generation in ells [23, 24] and to restore mitohondrial enzyme ativity [25]. Citrus flavonoids may also exert neuroprotetive effets sine they are involved in the modulation of neuronal ativities and mental health inluding brain plastiity, behaviour, mood, depression, and ognition [2, 22]. In this regard, it has been demonstrated that hesperidin an protet neurons against various types of insults assoiated with many neurodegenerative diseases [26]. Also, naringin has proven to exert neuroprotetive effets through anti-inflammatory ativity on the survival of dopaminergi neurons and on the integrity of the nigrostriatal pathway in animal models of Parkinson s disease [27 29]. Natural flavonoids would therefore seem to have important potential as mediaments in the field of mental health, although their use in linial pratie is still a long way off [3]. The peel from Citrus fruits is also a soure of Polymethoxylated Flavones (PMFs), flavonoids substituted by methoxygroups,whihrarelyourinotherplants[31]. PMFsaremorephysiologiallyativethantheirmethylated derivatives. For instane, researh data have demonstrated that nobiletin possesses a wide range of therapeuti appliations inluding antioxidant, antitumor properties, in both in vitro and in vivo models [32 36]. Moreover, it has reently been reported that a novel itrus tangeretin derivative, 5- aetyl-6,7,8,4 -tetramethylnortangeretin, an inhibit MCF-7 breast aner ell proliferation [37]. These data provide new insights into the role that itrus polyphenols an play in the prevention of diseases. In reent years, white and pink grapefruits (Citrus paradisi Maf.) have attrated muh attention beause of their nutritional and antioxidant properties [38]. High levels of bioative flavanones glyosides, namely, naringin and narirutin, have been reported in seed and peel residues released after grapefruit juie extration [38, 39], although further researh is required to explore the omposition of this fruit variety and its byproduts in more detail. Several treatments, inluding far-infrared radiation, ultrasound-assisted alkaline hydrolysis, enzyme treatment, and heat treatment, have been proposed to release more bioative glyosylated flavonoids and low moleular weight phenoli ompounds from several speies of itrus genus [1,4,4].Inthisonnetionithasbeenfoundthatdried orange, mandarin, and lemon peel extrats ontained muh higher onentrations of phenoli ompounds than fresh ones and hene exhibited greater antioxidant ativity [14, 41, 42]. However, little is known about the bioative flavonoids in treated grapefruit (Citrus paradisi Maf.) peel as a soure of health-promoting phytohemials. To our knowledge, only Xu et al. 27 [42] have disussed the extratable phenoli fration of grapefruit (Citrus paradisi Changshanhuyou), in a ultivar loated in southern China, showing inreases in the individual phenoli ompounds and enhanements of antioxidant apaity after heat treatment. Based on these results, then, it is easy to understand the interest of new omprehensive studies to determine the potential of treated grapefruit (Citrus paradisi Maf.) peel as a natural produt that an serve as an outstanding low-ost antioxidant soure. Treated grapefruit peel residues ould play an important role in the development of nutraeutial produts or as therapeuti agents for use in various pharmaologialin vitro or in vitro approahes. For all these reasons, the objetives of this researh were as follows: (i) to desribe and quantify the flavonoid profiles and antioxidant ativities of proessed white and pink grapefruit peels (Citrus paradise Maf.) after oven-drying and freeze-drying; (ii) to study the in vitro ytoprotetive effetiveness of grapefruit peel extrats on SH-SY5Y neuroblastoma ell lines. 2. Material and Methods 2.1. Fruit Peel Materials. White and pink grapefruits (Citrus paradise) were grown in several Valenia areas (Spain) orresponding with the ropping areas. They were purhased at Corte Ingles supermarket and possess ertified geographial origin Oven-Dried and Freeze-Dried Grapefruit Peels Treatment. Grapefruits were leaned with distilled water in the laboratory and they were immediately peeled. White and pink grapefruits peels were ut into piees (sized from approximately.5.5 m thik). Slied peel was divided into four portions: (i) one fresh peel portion to be diretly analyzed; (ii) two frations whih were dried in an oven at 45 Cand6 C, respetively, until their water ontent was within 9 12%; (iii) one grapefruit peel fration that was freeze-dried Extration of Phenoli Compounds. Extration of grapefruits peels was arried out by means of an aelerated solvent extrator ASE 2 (Dionex Corp, Sunnyvale, CA, USA). Extrations were performed using 5 g of grapefruits peel whih was plaed into inox extration ells of 22 ml. Every
3 Oxidative Mediine and Cellular Longevity 3 ell was filled with methanol and raised to 6 C. Then, two stati extration phases lasting for 1 min were arried out under 15 psi. Between extrations, a rinse of the omplete system was performed to avoid any arry-over. Extrats were evaporated using a rotavapor with a vauum ontroller (Heidolph, Shwabah, Germany) at 4 C. Samples were redissolved with 5 ml of methanol and they were filtered through a Whatman Number 1 filter paper. Samples were kept at 2 C prior to being used to determine antioxidant ativity and phenoli ompounds HPLC-DAD-ESI-MS Analysis. HPLC separation and identifiation and quantifiation of phenoli ompounds were performed on an Agilent 11 series system (Agilent, Waldbronn, Germany), equipped with a DAD photodiode detetor (G1315B) and a LC/MSD Trap VL (G2445C VL) eletrospray ionization mass spetrometry (ESI/MSn) system, bothoupledtoanagilentchemstation(versionb.1.3) for data proessing. The samples, after filtration (.2 μm, polyester membrane, Chromafil PET 2/25, Maherey-Nagel, Düren, Germany), were injeted in dupliate on a reversed-phase narrow-bore olumn Zorbax Elipse XDB-C18 ( mm; 3.5 μmpartile;agilent)protetedbyaguardolumnzorbax Elipse XDB-C8 ( mm; 5μm partile; Agilent), both thermostated at 4 C. The solvents were as follows: solvent A (aetonitrile/ water/formi aid, 3 : 88.5 : 8.5, v/v/v), solvent B (aetonitrile/water/formi aid, 5 : 41.5 : 8.5, v/v/v), and solvent C (methanol/water/formi aid, 9 : 1.5 : 8.5, v/v/v). The flow rate was.19 ml/min. The linear solvents gradient was as follows: min, 99% A and 1% B; 8 min, 97% A and 3% B; 37 min, 7% A, 17% B, and 13% C; 4 min, 5% A, 3% B, and 2%C;51min,1%A,4%B,and5%C;56min,5%Band 5%C;59min,5%Band5%C;and65min,99%Aand1% B. For identifiation, ESI-MSn was used in both positive and negative modes, setting the following parameters: dry gas, N2, 11 ml/min; drying temperature, 35 C; nebulizer, 65 psi; apillary, 25V (positive ionization mode) up to 42 minutes and +25 V (negative ionization mode) until the end of the hromatogram; target mass, 6 m/z; ompound stability, 4% (negative ionization mode) and 1% (positive ionization mode); trap drive level, 1%; and san range, 5 12 m/z. The identifiation of flavonoid ompounds was arried out by omparing their retention times and mass spetra provided with those of authenti standard (from Sigma St. Louis, MO) when available and spilling the samples with standard solutions. This was the ase of hesperidin, neohesperidin, naringin, naringenin, nobiletin, and tangeretin. The identifiation of ompounds where the standards were not available was performed by omparing the UV spetra and the [M + H] +, [M H] m/z with those reported in the literature. Quantifiation was made by means of external standard alibration lines and was expressed as milligrams of ompounds per gram of dry weight (DW). Quantitative results for ompounds without hemial standard were expressed in mg g 1 naringin equivalents DPPH Radial Savenging Assay. The DPPH assay was arried out aording to the method proposed by [43] where 1,1-diphenyl-2-pirylhydrazyl radial was used as a stable radial. One hundred miroliters of different dilutions of extrats was added to 2.9 ml of a.6 mm methanol DPPH radial solution. Methanol was used to adjust the zero and the derease in absorbane was measured at 515 nm every minute for 25 min in a UV-vis spetrophotometer (Helios, Thermo Spetroni, Cambridge, UK). Only values between 2% and 8%oftheinitialabsorbaneoftheradialDPPHweretaken into onsideration. Conentrations were alulated from a alibration urve in the range between.1 and.8 mm trolox. Results were expressed in milligrams of trolox per gram of dry weight ABTS + Radial Savenging Assay. The method used was the ABTS + (radial ation azino-bis[3-ethylbenzthiazoline- 6-sulfoni aid]) deolourisation assay aording to [44]. The assay is based on the ability of an antioxidant ompound to quenh the ABTS + relative to that of a referene antioxidant suh as trolox. A stok solution of ABTS + radial ation was prepared by mixing ABTS solution and potassium persulfate solution at 7 mm and 2.45 mm final onentration, respetively.themixturewasmaintainedinthedarkatroomtemperaturefor12 16hbeforeuse.TheworkingABTS + solution was produed by dilution in ethanol (1 : 9 v/v) of the stok solution to ahieve an absorbane value of.7 (±.2) at 734 nm. An aliquot of 2 μl of diluted extrat was added to ABTS + working solution (3 ml). For the blank and standard urve, 2 μl of ethanol or trolox solution was used, respetively. Absorbane was measured by means of a UVvis spetrophotometer at 734 nm immediately after addition and rapid mixing (At = ) and then every minute for 5 min. Readings at t = min (At = ) andt = 5min (At = 5) of reation were used to alulate the perentage inhibition value for eah extrat. A standard referene urve was onstruted by plotting % inhibition value against trolox onentration (.1.8 mm). The radial savenging apaity of extrats was quantified as milligrams of trolox per gram of dry weight FRAP Assay. The FRAP assay (Ferri Reduing Ability of Plasma) was performed as previously desribed by Alañón et al. (211a) and Benzie and Strain, 1999 [43, 45], with some modifiations. This spetrophotometri assay measures the ferri reduing ability of antioxidants. The experiment was onduted at 37 C and ph 3.6. In the FRAP assay, antioxidants present in the extrat redue Fe (III)-tripyridyltriazine omplex to the blue ferrous form, with an absorption maximum at 593 nm. The assay was performed by means of an automated miroplate reader (Tean GENios Pro (Tean Ltd., Dorset, UK)) with 96-well plates. Reagents inluded 3 mm aetate buffer ph 3.6, 4 mm hydrohlori aid, 1 mm TPTZ solution, and 2 mm ferri hloride solution. The working FRAP reagent was prepared fresh on the day of analysis by mixing aetate buffer, TPTZ solution, and ferri hloride solutions in the ratio 1 : 1 : 1 and the mixture was inubated at 37 C. Diluted extrat (3 μl) and prewarmed FRAP reagent (225 μl) were put into eah well. The absorbane at time
4 4 Oxidative Mediine and Cellular Longevity Table 1: Total Polyphenol Index (TPI), DPPH, FRAP, and ABTS assays mean values and standard deviation (SD) of untreated, oven-dried, and freeze-dried grapefruit peel extrats. TPI DPPH FRAP ABTS Mean ± SD Mean ± SD Mean ± SD Mean ± SD Fresh white grapefruit a ± a ± a ± a ± 6.22 Fresh pink grapefruit b ± a ± b ± a ± 12.9 White grapefruit dried at 45 C a ± b ± a ± b ± 3.8 Pink grapefruit dried at 45 C a ± a ± a ± b ± 5.64 White grapefruit dried at 6 C ± ± ± ± Pink grapefruit dried at 6 C a ± b ± a ± b ± 2.19 Freeze-dried white grapefruit 84.6 d ± d ± d ± d ± 36.1 Freeze-dried pink grapefruit 66.7 e ± d ± d ± e ± 1.95 TPI are expressed as mg galli aid equivalents per gram of dry weight. DPPH, FRAP, and ABTS assays are expressed as mg trolox per gram of dry weight. a,b,,d,e Different letters in the same olumn denote a signifiant differene aording to the Student-Newman-Keuls test, at p <.5. zero and after 4 min was reorded at 593 nm. The alulated differeneinabsorbaneisproportionaltotheferrireduing/antioxidant power of the extrat. For quantifiation, a alibration urve of trolox was prepared with dilutions within 1.5 mm. The final results were expressed as milligrams of trolox per gram of dried grapefruit peel. 2.8.TotalPhenolIndex(TPI).The total phenol ontent of extrats was determined aording to the Folin-Cioalteu proedure desribed by Singleton and Rossi [46]. Deionized water (1.8 ml) was added to.2 ml of eah extrat. Folin- Cioalteu reagent (.2 ml) was then added and tubes were shakenvigorously.after3min,.4mlsodiumarbonate solution (35% w/v) was added, along with 1.4 ml of deionized water. Samples were well mixed and left in the dark for 1 h. The absorbane was measured at 725 nm using a UV-vis spetrophotometer (Lambda 5, Perkin-Elmer, Seer Green, UK) and the results were expressed in galli aid equivalents, GAE, using a galli aid standard urve (.2 mg ml 1 ). Extrats werefurtherdilutediftheabsorbanevaluemeasuredwas above the linear range of the standard urve Cell Culture and Drug Treatment Proedures. SH-SY5Y ultures were grown as desribed previously by Jordán et al., 24 [47], in Dulbeo s modified Eagle s medium (DMEM) supplemented with 2 mm L-glutamine, 2 units ml 1 peniillin, 5 mg ml 1 streptomyin, and 15% (v/v) fetal bovine serum (Invitrogen, Carlsbad, CA, USA). The SH-SY5Y ells (1 1 6 /ml) were seeded 24 h before the experiments in a 96- wellplateandtheyweregrowninahumidifiedellinubator at 37 C under a 5% CO 2 atmosphere. For treatments, extrats from white and pink grapefruit peels (fresh, dried, and freeze-dried) were diretly added to the ulture medium at different onentrations (.1,.25,.5,.75, and 1 mg/ml) for 24 h. The orresponding ontrols were treated with the same onentration of ethanol, whih was always below.1% (final onentration) Viability Assay: 3-(4,5-Dimethylthiazol-2-yl)-2,5-diphenyltetrazolium Bromide (MTT) Assay. Cell viability was measured by the ability to redue 3-(-4,5-dimethylthiazol-2-yl)- 2,5-diphenyltetrazolium bromide (MTT) to the blue formazan produt. The ulture medium was removed after 24 h of treatment. 15 μl ofmtt(1mg ml 1 in normal ulture medium) was added to the plates, and the ells (ontrol and treated) were inubated for 2 h at 37 C. The medium was then replaed with DMSO, and MTT absorption was measured in a VERSAmax tunable miroplate reader (Moleular Devies, Sunnyvale, CA, USA). Results were expressed as the perentage of MTT redution, assuming that the absorbane of the ontrol SH-SY5Y ells was 1% Statistial Analysis. Analysis of variane and multivariate analysis were performed using SPSS 15. for Windows statistial pakage. Differenes among means were determined for signifianeat p.5 using the Student-Newman-Keuls test. Prinipal Component Analysis was performed to lassify the samples into groups aording to phenoli omposition and antioxidant ativity. 3. Results and Disussion 3.1. Effet of Proessing on the Antioxidant Ativities and Total Polyphenol Index of Grapefruit Peel Extrats. The effets of oven-drying and freeze-drying treatments on the antioxidant ativity of grapefruit peels extrats were determined by DPPH, ABTS +, and FRAPS tests (see Table 1). It is interesting to note that freeze-drying enhaned antioxidant ativity in all ases. The DPPH assay showed signifiantly higher levels of antioxidant apaity (p <.5) in freeze-dried than in fresh grapefruit peels. Freeze-dried white and pink grapefruit peels registered and mg trolox/g DW, while extrats from fresh peels registered values of and mg trolox/g DW, respetively. This effet is probably a onsequene of the freeze-drying proess. This proess
5 Oxidative Mediine and Cellular Longevity 5 Table 2: Spetral data of flavonoids in grapefruit peel extrats. Tentative identifiation RT UVmax MS [M H] MS [M + H] + Produts ions (min) λ (nm) (m/z) (m/z) (m/z) Isonaringin[32,41] ,284, ,151 Naringin [32, 41] , 283, , 271 Hesperidin [32, 41] , 284, Neohesperidin [41] , 283, , 489 Unknown , ,33 Unknown ,257, ,287 Naringenin[42] ,284, Hesperetin [4] , 285, Isosinensetin [4] , 27, , 343, 327 Sinensetin[32,4,43] ,264, ,343,312 Unknown , 272, , 373 Nobiletin[4,43] ,268, ,373 Tangeretin [32, 4] , , 343, 325, 297 Referenes given in brakets are taken from papers with mathing spetral data: Angeloni et al. 212 [32]; Rivas et al. 28 [4]; Jeong et al. 24 [41]; Xu et al. 27 [42]; Alañón et al. 211 [43]. hasbeenassoiatedwithhighprodutionofredox-ative metabolites whih play an important role in adsorbing and neutralizing free radials or deomposing peroxides, as previously reported by other researhers [48]. After oven-drying at 45 Cand6 C, DPPH values of both white and pink grapefruit peels were signifiantly greater than those of fresh peel extrats (Table 1). These inreases denote inreased antioxidant ativity, partiularly in the ase of white grapefruit peel heated at 6 C. They are presumably a onsequene of the relationship between the generation of breakdown antioxidant produts and the inreasing temperatures to whih the grapefruit peels were subjeted, and they are onsistent with data reported for other itrus varieties subjeted to omparable heat treatments [41, 42, 49]. The ABTS + assay showed the same tendeny, revealing a signifiant inrease of free radial savenging ativity in white and pink freeze-dried grapefruit peel extrats (p <.5), whih reahed and mg trolox/g DW, versus and mg trolox/g DW in the ase of fresh samples. ABTS + ativity was also greater in grapefruit peel dried at 45 Cand6 C than in fresh extrats, although the rise was less pronouned than in the ase of freeze-dried peel. For instane, savenging ability was signifiantly (p <.5) greater in white grapefruit peel extrats than in fresh extrats (from to and mgtrolox/g DW) as a result of treatment at 45 Cand6 C, respetively. ABTS also inreased in the ase of pink grapefruit peel but did not differ signifiantly between 45 Cand6 C. This behaviour is onsistent with reports for extrats of dried itrus peel of other varieties [42, 49]. FRAP helating values for white and pink grapefruit peels oven-dried at 6 C reahed and mg trolox/g DW, respetively, that is, 1.7 times the values for fresh peels extrats (Table 1). In the ase of freeze-dried samples, results varied from 6.3 and for white and pink fresh grapefruit peel extrats to and mg trolox/g DW for freeze-dried grapefruit peels, respetively. In general, the sale of the antioxidant ativity observed in freeze-dried white and pink grapefruit peels suggested that this treatment might produe not only dissoiation or liberation of some phenoli ompounds from biologial strutures but also hemial hanges enabling the onversion of insoluble phenols into more soluble and free forms, as indiated by the data from other freeze-dried vegetable extrats [5, 51]. The results of the Folin-Cioalteu Total Phenol Index (TPI), a preliminary sreening fator to establish the antioxidant apaities of treated grapefruit peels, are shown in Table 1. Total phenols in white and pink grapefruit peels dried at 45 C, and partiularly at 6 C (63.35 and mg GAE/g dry weight, resp.), were signifiantly higher than in fresh samples (49.14 and mg GAE/g dry weight), most probably due to the leaving of glyosylated bonds in various phenoli ompounds. Note also that TPI values from white and pink freezedried grapefruit peel extrats were 58% and 42% higher, respetively, than in fresh samples. This trend is onsistent with reports in previous works arried out on lyophilized fruits, tubers, vegetables, and fungi [5, 52, 53]. The same trend was observed in the behaviour of TPI, ABTS,FRAP,andDPPHvalues,whihweresignifiantly enhaned after oven-drying (45 C, 6 C) and espeially freeze-drying treatments. This suggests that both proesses ould be suessfully used to enhane antioxidant ativity in grapefruits peels for use as natural soures of antioxidants, with major attendant environmental and eonomi benefits. As natural produts, with outstanding antioxidant power, proessed grapefruit look very promising for use in the development of new therapeuti strategies Effet of Oven-Drying and Freeze-Drying on Flavanone and Polymethoxylated Flavones of Grapefruit Peels. Atotalof thirteen ompounds were quantified, based on their UV-data spetra and [M + H] +,[M H] m/z (Table 2), and were
6 6 Oxidative Mediine and Cellular Longevity (mau) Fresh white grapefruit peel (min) (mau) White grapefruit peel oven-dried at 45 C (min) (a) (b) 3 Freeze-dried white grapefruit 2 25 (mau) (min) () Figure 1: HPLC hromatogram of white grapefruit peels. Peak assignments: (1) isonaringin; (2) naringin; (3) hesperidin; (4) neohesperidin; (5) unknown-1; (6) unknown-2; (7) naringenin; (8) hesperetin; (9) isosinensetin; (1) sinensetin; (11) unknown-3; (12) nobiletin; (13) tangeretin. quantified by HPLC-MS. These were as follows: four glyosylated flavanones (FGs), namely, isonaringin, naringin, hesperidin, and neohesperidin; four polymethoxylated flavones (PMFs), namely, isosinensetin, sinensetin, nobiletin, and tangeretin; two flavanone aglyones: hesperetin and naringenin; and three unknown ompounds. Typial MS total ion urrent hromatograms with numbered peaks are shown in Figure 1. Naringin and to a muh lesser extent isonaringin were the main FGs in all grapefruit peels extrats (Table 3). Naringin levels in fresh pink and white grapefruits varied within mg/g DW, respetively, while isonaringin ranged between and 13.42mg/g DW. Moreover, naringenin was the most abundant flavanone aglyone in fresh white and pink grapefruit peels (Table 3). Levels of polymethoxylated flavones, sinensetin, nobiletin, and tangeretin ranged from 1.3 to 3.45 mg/g DW in fresh grapefruit peels. Results were very similar to reports in the literature for peels of mandarin and thirteen itrus speies [53 56]. However, one of the most outstanding findings in this study was the flavonoid losses in proessed grapefruit peels. Oven-dried and freeze-dried grapefruit peels had similar flavonoid profiles, although onentrations were lower than in fresh samples. After oven-drying of grapefruit peels at 45 Cand6 C, the onentrations of most FGs, PMFs, and flavanone aglyones delined sharply, 3 6-fold with respet to fresh grapefruit peel extrats (Table 3). The same behaviour has been reported in dried itrus peels from other varieties [42, 49]. However, it is important to note that naringin onentrations in proessed grapefruit peels were between two and four times higher than reported in treated byproduts from other itrus speies [42, 57, 58]. The same downward trend was observed when omparing flavonoid ontents in freeze-dried grapefruit peels and fresh grapefruit peel extrats (Table 2). For instane, isonaringin dereased from mg/g DW in fresh white grapefruit peels to 7.17 mg/g DW in freeze-dried white grapefruit peels. The dereases were most pronouned (from to 4.57 and 4.2) after oven-drying at 45 Cand6 C, respetively. It is interesting to note that the effets of oven-drying and freeze-drying on FG and PMF levels were opposite to their effets on TPI values and free radial savenging ativities. This may be beause the TPI assay evaluates the totality of phenols, that is, all flavonoids and nonflavonoid phenoli ompounds, whih suggests that some phenoli ompounds other than flavones and flavanones are involved in the antioxidant ativities of grapefruit peel extrats. This tends to onfirm some reent studies whih desribed progressive inreases of innamis and benzois aids levels in orange peels dried from 6 Cto12 Cinomparison with untreated samples due to the leaving of esterified bond and glyosylated bond [42, 49]. By the other hand, our results are in a good agreement with dereases of naringin, hesperidin, and neohesperidin reported in dried orange peels in omparison with untreated samples [42]. Heat treatment of grapefruit peels is thus losely assoiated with releases of bound phenoli aids, inluding hydroxybenzoi and hydroxyinnami aids, produing higher levels of free
7 Oxidative Mediine and Cellular Longevity 7 Table 3: Flavanones glyosides, flavanones, and polymethoxylated flavones ontent (milligrams per gram of dry weight) and relative standard deviations (RSD) both for white and pink grapefruit peel extrats. Fresh white grapefruit White grapefruit oven-dried at 45 C White grapefruit oven-dried at 6 C Freeze-dried white grapefruit Fresh pink grapefruit Pink grapefruit oven-dried at 45 C Pink grapefruit oven-dried at 6 C Freeze-dried pink grapefruit Isonaringin a (13.92) 4.57 b (1.71) 4.2 b (.22) 7.17 (2.6) a (1.73) 3.72 b (5.65) 3.55 b (.32) 5.22 b (4.74) Naringin a (18.24) b (1.96) b (.25) 95.8 (5.39) a (16.81) b (6.39) 43.5 b (.34) 5.4 b (3.12) Hesperidin 3.23 a (15.81).51 d (2.2).37 d (5.82).65 d (1.9) 2.68 b (6.31).21 d (6.29).13 d (.26).95 (2.77) Neohesperidin 3.3 a (9.93).79 (2.34).67 d (.48) 1.39 e (5.45) 2.93 b (7.4).3 d (6.41).27 d (.39).79 (2.9) Unknown a (5.26).76 (2.17).76 (.8).74 (1.26) 3.88 b (4.83).93 (1.65).84 (.12).61 (5.59) Unknown a (6.71) 1.67 b (2.28) 1.46 b (1.8) 2.2 (7.1) 5.5 a (8.82) 1.6 b (4.7) 1.29 b (.8) 1.9 b (1.4) Naringenin 8.49 a (9.95) 5.5 b (2.16) 4.54 b (1.1) 7.83 a (4.78) 8.14 a (15.83) 2.87 (5.29) 2.49 (.29) 2.35 (.35) Hesperetin 2.93 a (2.24).54 (1.94).43 d (1.17).87 e (1.25) 2.55 b (3.3).42 d (5.57).39 d (1.4).47 d (6.99) Isosinensetin 3.2 a (3.71).56 b (3.44).45 b (.59).6 a (4.96) 3.12 a (1.67).41 b (1.34).43 b (2.7).24 b (6.16) Sinensetin 2.1 a (14.48) 1.82 a (.13) 1.78 a (.68) 1.74 a (2.68) 2.7 a (5.3).63 b (.77).63 b (.69).79 b (7.69) Unknown a (9.42) 1.14 b (4.56).99 b (.87) 1.46 b (3.69) 3.86 a (9.83).32 (5.5).32 (3.68).41 (8.13) Nobiletin 2.36 a (14.26) 1.22 (1.29) 1.35 (13.2) 2.9 a (12.63) 3.45 b (11.67).63 d (2.74).58 d (2.61) 1.24 (1.19) Tangeretin 2.45 a (1.48) 2.5 (1.11) 1.98 (5.29) 1.96 (2.51) 1.3 b (3.34).97 b (.38).97 b (.46) 1.6 b (8.32) Compounds tentatively identified. Data are expressed as naringin equivalents (mg/g). a,b,,d,e Different letters in the same olumn denote a signifiant differene aording to the Student-Newman-Keuls test, at p <.5.
8 8 Oxidative Mediine and Cellular Longevity PC PC-1 F-Wgf D-Wgf-45 C D-Wgf-6 C FD-Wgf F-Pgf D-Pgf-45 C D-Pgf-6 C FD-Pgf Figure 2: Prinipal Component Analysis performed onsidering dupliates of the flavanones glyosides, flavones, and polymethoxylated flavones ontents on fresh, oven-dried and freeze-dried, and white and pink grapefruit peel extrats. F-Wgp: fresh white grapefruit; F-Pgf: fresh pink grapefruit; D-Wgf-45 C: dried white grapefruit at 45 C; D-Pgf-45 C: dried pink grapefruit at 45 C; D- Wgf-6 C: dried white grapefruit at 6 C; D-Pgf-6 C: dried white grapefruit at 6 C; FD-Wgf: freeze-dried white grapefruit; FD-Pgf: freeze-dried pink grapefruit. phenoli aids. Therefore, the inrease in the total phenol index and DDP, FRAP, and ABTS values would appear to be aused by the free fration of phenoli aids. To obtain more detailed information on the individual flavanone glyosides, flavanones, and polymethoxylated flavones that our in proessed white and pink grapefruit peels, the data matrix was proessed by Prinipal Component Analysis (PCA). The two-dimensional projetion of variables is presented in Figure 2. The first prinipal omponent axis explains 83.47% of the total variation and learly isolated fresh grapefruit peel extrats whih were grouped on the right side of the plot, orrelating losely with higher levels of hesperidin, neohesperidin, isonaringin, naringin, nobiletin, and unknowns-1-2. PC-1 also exhibited orrelation with freeze-dried samples plotted on the negative area of PC-1 (Figure 2). The fat that amounts of isosinensetin, hesperetin, hesperidin, isonaringin, neohesperidin, unknown-3, naringin, and nobiletin in freeze-dried grapefruit peels were higher than in extrats from oven-dried peels indiates a good degree of disrimination and also suggests that freeze-drying is more effetive in preserving bioative ompounds than ovendrying. However, extrats from grapefruit peels dried at 45 C 2. and 6 C were loated too lose together on the x-axis for disrimination. PC-2 explains 1.4% of the total variation and is partiularly important in terms of differentiating grapefruit varieties. PC-2 showed positive loadings for tangeretin, sinensetin, and naringenin, grouping white grapefruit peel extrats at the top of the axis and pink grapefruit peel extrats at the bottom Viability. SH-SY5Y ell viability results were influened by two parameters; firstly the treatment of grapefruit peels (fresh, oven-drying, or freeze-drying) and seondly the onentration of bioative ompounds. Our results showed that the potential ell protetion and/or ell ytotoxiity of grapefruit peel extrats was determined by these two fators together. In general, ell viability dereased with inreasing onentrations of grapefruit peel extrats, whether they were fresh/proessed or white/pink. On the other hand, in the ase of SH-SY5Y ells viability perentages were higher in fresh than in treated grapefruit peel extrats. It is important to stress that fresh white grapefruit peel extrats at onentrations between.1 and.25 mg/ml learly exerted a protetive effet on the SH-SY5Y ell line, reahing viabilities of 1% (Figure 3). Similar effets were reported by Chen et al. 212 [59] on Hep G2 ells after ontat with fresh Citrus sinensis peel extrats at onentrations ranging within.1.5 mg/ml, whih signifiantly proteted against tertiary butyl hydroperoxides t-bhp. The ytoprotetive effet observed in the urrent is most probably attributable to the levels of bioative flavonoids (FGs and PMFs), mainly naringin, isonaringin, and naringenin, whih largely our in fresh white grapefruit peel extrats (Table 2). Similar finding have also been reported, revealing a relationship between naringin and naringenin and neuroprotetion and oxidative stress delay [6]. In the present ase, fresh white grapefruit peel extrats, whih registered the highest flavonoid ontents, also sored best for viability. On the other hand, freeze-dried peel extrats, ontaining less flavonoids (Table 2), registered the lowest ell viability ratios. Also, SH-SY5Y ell viability dereased to 75% after the following: (i) 24-hour inubation with fresh grapefruit peel extrats at.75 mg/ml; (ii) inubation with oven-dried grapefruit peels extrat (45 C and 6 C) at.25 mg/ml; and (iii) ontat with freeze-dried grapefruit peel extrat at onentrations ranging within.1.25 mg/ml (Figure 3). Finally, it was found that oven-dried grapefruit peels (45 Cand6 C), at onentrations ranging from.75 mg/ml to 1 mg/ml, indued ell death by 75 95% in both white and pink grapefruits. This effet was espeially pronouned after ell ontat with freeze-drying extrats (.75 mg/ml and 1 mg/ml) whih triggered 9% and 96%, respetively, of apoptosis in SH-SY5Y-ells. This suggests that ell ytoprotetion and/or apoptosis, expressed as ell viability, an be influened in a dose-dependent way by flavonoids. It should be noted that the results for SH-SY5Y ell viability after ontat with grapefruit peel extrats did not really math expetations in the light of the polyphenol index (TPI) and DPPH, FRAP, and ABTS here reported. There seemed to be an inverse orrelation between antioxidant
9 Oxidative Mediine and Cellular Longevity 9 Cell viability (%) Control Fresh grapefruit peels a a a a ab a b ab F-Pgf.1 mg/ml F-Wgf.1 mg/ml F-Pgf.25 mg/ml F-Wgf.25 mg/ml F-Pgf.5 mg/ml F-Wgf.5 mg/ml F-Pgf.75 mg/ml F-Wgf.75 mg/ml F-Pgf 1 mg/ml F-Wgf 1 mg/ml Cell viability (%) Control a a D-Pgf-45 C-.1 mg/ml D-Wgf-45 C-.1 mg/ml Dried grapefruit peel at 45 C b b D-Pgf-45 C-.25 mg/ml D-Wgf-45 C-.25 mg/ml D-Pgf-45 C-.5 mg/ml D-Wgf-45 C-.5 mg/ml d d D-Pgf-45 C-.75 mg/ml D-Wgf-45 C-.75 mg/ml e e D-Pgf-45 C-1 mg/ml D-Wgf-45 C-1 mg/ml (a) (b) Cell viability (%) Control ab a D-Pgf-6 C-.1 mg/ml D-Wgf-6 C-.1 mg/ml b Dried grapefruit peels 6 C ab D-Pgf-6 C-.25 mg/ml D-Wgf-6 C-.25 mg/ml D-Pgf-6 C-.5 mg/ml D-Wgf-6 C-.5 mg/ml D-Pgf-6 C-.75 mg/ml d d e e D-Wgf-6 C-.75 mg/ml D-Pgf-6 C-1 mg/ml D-Wgf-6 C-1 mg/ml Cell viability (%) Control a a FD-WP.1 mg/ml FD-PP.1 mg/ml Freeze-dried grapefruit peels FD-WP.25 mg/ml b FD-PP.25 mg/ml e FD-WP.5 mg/ml d FD-PP.5 mg/ml e f f f FD-WP.75 mg/ml FD-PP.75 mg/ml FD-WP 1 mg/ml FD-PP 1 mg/ml () (d) Figure 3: Effets of different onentrations of red and white grapefruit extrats in ell viability of SH-SY5Y ell ultures for 24 h. Data were expressed as the perentage of live ells relative to total ells. Data are presented by means ± SD (n = 3). F-Wgp: fresh white grapefruit; F- Pgf: fresh pink grapefruit; D-Wgf-45 C: dried white grapefruit at 45 C; D-Pgf-45 C: dried pink grapefruit at 45 C; D-Wgf-6 C: dried white grapefruit at 6 C; D-Pgf-6 C: dried white grapefruit at 6 C; FD-Wgf: freeze-dried white grapefruit; FD-Pgf: freeze-dried pink grapefruit. a, b,, d, e, f: different letters in the same olumn denote a signifiant differene aording to the Student-Newman-Keuls test, at p <.5. ativity and ell viability sine the extrats with the highest antioxidant apaities were the most losely assoiated with ell ytotoxiity. The explanation of this singular behaviour probably lies in the amounts of phenoli aids, whih would surely inrease after drying at 45 Cand6 C and more so after freeze-drying, produing onsiderable inreases in the overall antioxidant ativity and TPI index. However, it has also been reported that phenoli aids, due to their hemial struture and depending on ertain onditions, are involved in prooxidant reations assoiated with damage to moleules suh as DNA [61, 62]. These last findings would seem to indiate that phenoli aid levels are strongly assoiated with ell ytotoxiity and apoptosis, whih supports the findings in the present work. 4. Conlusions Our results indiate that oven-drying (45 C, 6 C) and espeially freeze-drying an be used to signifiantly enhane the antioxidant power of grapefruit peels, thus realizing their outstanding potential for biomedial use. Fresh and proessed grapefruit peel wastes are a natural soure of valuable bioative flavonoids, mostly naringin, that ould be inorporated as food ingredients or as therapeuti agents as part of pharmaologial strategies. Finally, the in vitro ytoprotetion demonstrated by fresh and oven-dried (45 C) grapefruit peels opens up new possibilities for these natural extrats; however, further researh into ation mehanisms, animal models, linial trials, and dose-effet will be needed. Conflit of Interests The authors delare that there is no onflit of interests regarding the publiation of this paper. Aknowledgment The authors would like to thank the Junta de Comunidades de Castilla-La Manha (Consejería de Cienia y Tenología) for the finanial support under the Projet P II andalsothealfonsomartín Esudero Foundation. Referenes [1] A. Boo, M.-E. Cuvelier, H. Rihard, and C. Berset, Antioxidant ativity and phenoli omposition of itrus peel and seed extrats, JournalofAgriulturalandFoodChemistry, vol. 46, no. 6, pp , 1998.
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