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Anthocyanins and Proanthocyanidins from Blueberry–Blackberry

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Anthocyanins and Proanthocyanidins from Blueberry–Blackberry 1182 DOI 10.1002/mnfr.201200678 Mol. Nutr. Food Res. 2013, 57, 1182–1197 RESEARCH ARTICLE Anthocyanins and proanthocyanidins from blueberry–blackberry fermented beverages inhibit markers of inflammation in macrophages and carbohydrate-utilizing enzymes in vitro Michelle H. Johnson1, Elvira Gonzalez de Mejia1,2, Junfeng Fan3, Mary Ann Lila4 and Gad G. Yousef4 1 Division of Nutritional Sciences, University of Illinois, Urbana, IL, USA 2 Department of Food Science and Human Nutrition, University of Illinois, Urbana, IL, USA 3 College of Bioscience and Biotechnology, Beijing Forestry University, Beijing, P. R. China 4 Plants for Human Health Institute, NC Research Campus, North Carolina State University, Kannapolis, NC, USA Scope: Berries are an excellent source of dietary flavonoids which have several health benefits. Received: October 14, 2012 Methods and results: We evaluated well-characterized anthocyanins (ANCs) and proantho- Revised: January 14, 2013 cyanidins (PACs) from fermented blueberry–blackberry beverages. Wines were produced from Accepted: January 23, 2013 highbush blueberries and blackberries grown in Illinois and blended to create ratios rang- ing from 100% blueberry to 100% blackberry. Total ANCs of the wine were strongly corre- lated to total phenolics (r = 0.99, p < 0.05) and to antioxidant capacity (r = 0.77, p < 0.05). ANC- and PAC-enriched fractions were purified from each wine blend and a phenolic profile was generated. ANCs increased with more blackberries from 1114 to 1550 mg cyanidin-3-O- glucoside (C3G) equivalents/L. Hydrolysable tannins were identified in the PAC-enriched frac- tion. Both ANC- and PAC-enriched fractions inhibited starch-degrading enzyme ␣-glucosidase and dipeptidyl peptidase-IV activity. Computational docking demonstrated that delphinidin- 3-arabinoside effectively inactivated dipeptidyl peptidase-IV by binding with the lowest inter- action energy (−3228 kcal/mol). ANC and PAC (100 ␮M C3G and epicatechin equivalents, respectively) from blueberry–blackberry blends reduced LPS-induced inflammatory response in mouse macrophages via the nuclear factor kappa B-mediated pathway. Conclusion: ANC- and PAC- (including hydrolysable tannins in blackberry) enriched fractions from blueberry and blackberry fermented beverages are beneficial sources of antioxidants, inhibitors of carbohydrate-utilizing enzymes, and potential inhibitors of inflammation. Keywords: Anthocyanin / Berry / Diabetes / Hydrolysable tannins / Inflammation / Proantho- cyanidin 1 Introduction Correspondence: Professor Elvira Gonzalez de Mejia, Depart- Blueberries and blackberries are a rich source of anthocyanins ment of Food Science and Human Nutrition, University of Illi- (ANCs), the water-soluble pigments which give berries their nois at Urbana-Champaign, 228 ERML, 1201 W. Gregory Avenue, red, blue, and purple coloring [1]. Berries also contain poly- Urbana, IL 61801, USA merized phenolic compounds including hydrolysable tannins E-mail: [email protected] (HTs), such as ellagitannins and gallotannins, and condensed Fax: +1-217-265-0925 tannins known as proanthocyanidins (PACs) [2]. The con- Abbreviations: ANC, anthocyanin; C3G, cyanidin-3-O-glucoside; sumption of ANCs is among the highest of all flavonoids COX-2, cyclooxygenase-2; DPP-IV, dipeptidyl peptidase-IV; EAE, ellagic acid equivalents; HT, hydrolysable tannin; iNOS, inducible nitric oxide synthase; MTS, 3-(4,5-dimethylthiazol-2-yl)- PAC, proanthocyanidin; PES, phenazine ethosulfate; p-p65 NF␬B, 5-(3-carboxymethoxyphenyl)-2-(4-sulfophenyl)-2H-tetrazolium; phosphorylated p-65 subunit of nuclear factor kappa B; TE,trolox NO,nitricoxide;ORAC, oxygen radical absorbance capacity; equivalents C 2013 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.mnf-journal.com Mol. Nutr. Food Res. 2013, 57, 1182–1197 1183 due to their wide distribution in foods [3]. Positive health tioxidant capacity, the ability to reduce carbohydrate-utilizing effects have been attributed to the high antioxidant capacity enzymes activity, and reduce inflammation. of these phytochemicals. ANCs have been established as hav- ing a high antioxidant capacity by scavenging free radicals and reducing oxidative stress [4]. PACs may also reduce oxidative 2 Materials and methods stress and inflammation [5]. Increased phenolic intake has been seen to correlate with health benefits and is linked with 2.1 Materials decreased incidence of several diseases, including metabolic syndrome [6] and diabetes [4]. Wines used were produced from highbush blueberries Fermentation is known to increase the phenolic content of (Vaccinium corymbosum) and blackberries (Rubus spp.) grown berry juice products by increasing extraction from the skins, at Dixon Springs Agricultural Center in Simpson, Illinois. including ANCs [7], and therefore may increase the antioxi- Blueberry wine was fermented as previously described [14]. dant capacity [8] and potential for health benefits. Moderate Blueberry (V. corymbosum) cultivars Blue Chip, Bluecrop, wine consumption as part of a healthy diet may reduce the Blue Haven, Blue Jay, Blueray, Bluetta, Collins, Coville, Dar- risk of certain chronic diseases linked to inflammatory pro- row, Earliblue, Elliot, Jersey, Late Blue, and Spartan were cesses [6, 9]. The health benefits and sensory properties at- collected from Dixon Springs Agricultural Center during the tributed to fermented berry products may be due to the high ripening season of 2010. Blueberry juice from crushed frozen amounts of polyphenolic compounds present [10–12]. blueberries was fermented with Saccharomyces bayanus at Type 2 diabetes occurs when the body is unable to pro- 23ЊC until alcohol content reached 5–6%; finished wine was vide a proper insulin response to deal with glucose from the filtered through cheesecloth. Blackberry wine was prepared diet, leading to excessive blood glucose and insulin resistance. at the same time using a similar procedure [14]. Blackberries Several studies have been conducted to evaluate the reduction (Rubus fruticosus) cultivars A-1937, A-2215, A-2241 Natchez, of absorption of glucose by berries and berry compounds to A-2315, APF 27, APF 40, APF 41, and Prime Jan were col- inhibit ␣-glucosidase and ␣-amylase [13–15]. One potential lected from Dixon Springs Agricultural Center during the drug therapy for diabetics targets these carbohydrate-utilizing ripening season of 2010. Upon collection, the berries were enzymes; natural sources of inhibitors of these enzymes stored frozen at −18ЊC until use. Wine was prepared using would be beneficial to avoid undesirable side effects that oc- 90.7 kg blackberries, with roughly even mixtures of all culti- cur with drug therapy [16]. Dipeptidyl peptidase-IV (DPP-IV, vars listed above. To the blackberry lot, 180 mL SO2 solution EC.3.4.14.5) is another current pharmaceutical target for di- (50 ppm), 3 g pectic enzyme solution (dissolved in water), abetes treatment. Inhibitors of this enzyme are emerging as and 10 kg sucrose solution were added. Dry wine yeast Lavin antidiabetes therapy and allow for stimulation of insulin se- EC 1118 (S. bayanus) obtained from Presque Isle Wine Cel- cretion to consequently decrease blood glucose levels [17]. lars (North East, PA) was rehydrated at 40ЊC for 20 min with However, the inhibitory potential on DPP-IV by berry com- occasional gentle stirring to remove clumps prior to inocula- pounds needs to be further studied. tion of the juice. Per manufacturer’s recommendations, EC Chronic inflammation due to abnormal circulating lev- 1118 was inoculated at 40 or 50 mg dry yeast/100 mL, and els of pro-inflammatory cytokines is associated with the held at 21 ± 1ЊC during fermentation. Blends ranging from development of diabetes and other metabolic diseases. A 100% blueberry to 100% blackberry were made using room stimulated inflammatory cascade may be mediated by nu- temperature fermented wines. Blends are presented as a ra- clear factor kappa B (NF␬B) signaling pathway to upreg- tio of %blueberry : %blackberry. The ratios were 100:0, 70:30, ulate pro-inflammatory enzymes, such as inducible nitric 50:50, 30:70,and0:100 of blueberry:blackberry wine blends, oxide synthase (iNOS) and cyclooxygenase-2 (COX-2). Di- respectively. etary flavonoids have been linked to anti-inflammatory path- All solvents used for phenolic extraction were HPLC- ways [3], and many berries or berry compounds have been grade and were purchased from Fisher Scientific (Pittsburg, investigated for their anti-inflammatory properties and an- PA). Amberlite XAD-7 was purchased from Sigma-Aldrich tioxidant capacity or radical scavenging activity [4, 18–21]. (St. Louis, MO), Sephadex LH-20 was purchased from GE Life Fermented juices and wines from berries have been inves- Sciences (Buckinghamshire, UK). Murine macrophage RAW tigated [11, 22], and in several studies they were found to 264.7 cell line and DMEM with L-glutamine were purchased inhibit inflammatory protein production or expression more from American Type Culture Collection (ATCC) (Manassas, than their unfermented counterparts [12, 23–25]. VA). Fetal bovine serum was from Invitrogen (Grand Island, The objective of this study was to evaluate well- NY). CellTiter 96R AQueous One Solution Proliferation assay characterized ANCs-enriched fraction and PACs-enriched kit (3-(4,5-dimethylthiazol-2-yl)-5-(3-carboxymethoxyphenyl)- fraction present in blueberry–blackberry fermented bever- 2-(4-sulfophenyl)-2H-tetrazolium (MTS)/phenazine ethosul- ages for their effect on markers of inflammation in RAW fate (PES)) was purchased from Promega Corporation
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