Resveratrol and Naturally Occurring Analogues in Vaccinium Species
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1 Resveratrol and Naturally Occurring Analogues in Vaccinium Species Agnes M. Rimando Danny L. Barney USDA-ARS University of Idaho Natural Products Utilization Research Unit Sandpoint Research & Extension Center University, MS Sandpoint, ID USA USA Keywords: antioxidant activity, piceatannol, pterostilbene Abstract In a continuing study, seventeen samples of berries representing varieties and cultivars of nine Vaccinium species collected from Idaho, Washington, and Wyoming were analyzed for their content of resveratrol, pterostilbene and piceatannol. These naturally occurring stilbenes have been reported to have potential cancer chemopreventive and strong antioxidant activities. Analysis by GC/MS showed contents of and µg/g lyophilized berry for resveratrol and pterostilbene, respectively. Piceatannol was found in only three of the species studied at levels of µg/g lyophilized berries. Enzymatic hydrolysis of the extracts using β-d-glucosidase increased resveratrol levels up to 63-fold, suggesting and demonstrating for the first time, that resveratrol also occurs as a glycoside in Vaccinium berries. INTRODUCTION Resveratrol (Fig. 1) has been the subject of numerous studies having been linked to low incidence of fatal coronary heart disease among populations drinking wine moderately (Hegsted and Ausman, 1988; Renaud and De Lorgeril, 1992). It has also been shown to possess cancer chemopreventive property, demonstrated in assays representing three stages of carcinogenesis (Jang et al., 1997). The biological and pharmacological activities of resveratrol are thought to be due to strong antioxidant property, which has been investigated extensively (Arichi et al., 198; Fauconneau et al., 1997; Stivala et al., 21; Teguo et al., 1998). Recently, it was found that pterostilbene (Fig. 1), a naturally occurring analogue of resveratrol, has cancer chemopreventive activity similar to that of resveratrol in a mouse mammary gland culture assay (Rimando et al., 22). Pterostilbene was also shown to have antioxidant activity similar to that of resveratrol (Rimando et al., 22; Stivala et al., 21). Piceatannol (Fig. 1) is another naturally occurring resveratrol analogue that has been reported to have cancer chemopreventive as well, and stronger antioxidant activity than resveratrol (Hung et al., 21; Lee et al., 1998). Additionally, resveratrol was metabolized by cytochrome P45 enzyme CYP1B1 to piceatannol, reportedly known as an antileukemic agent (Potter et al., 22). Pterostilbene and piceatannol are both found in grapes. The reported activities of these analogues, which are similar to or greater than those of resveratrol, generated interest to investigate the presence of these compounds, as well as resveratrol, in other berries. The Vaccinium berries are of particular interest as fruits in this genus are one of the widely consumed small fruits. Blueberries recently have been drawing much attention due to their brain function enhancing activity (Joseph, 22; Youdim et al., 2). Results on the analysis of these three stilbenes in Vaccinium berries are presented. MATERIALS AND METHODS Vaccinium Berries Berries were collected in 21 (group I) and 22 (group II) from specific collection sites on specific dates (Table 1). Berries of domestic cultivars were frozen immediately after collection and stored at 4 C until transport on ice to the University of Idaho at Moscow, Idaho, where the fruits were freeze dried. Samples of V. uliginosum Proc. WOCMAP III, Vol.6: Traditional Medicine & Nutraceuticals Eds. U.R. Palaniswamy, L.E. Craker and Z.E. Gardner Acta Hort. 68, ISHS
2 were stored on ice following collection and treated as described above. Freeze-dried samples were sent to Mississippi and stored in a cold room at 4 C until extraction. Three cultivars of V. corymbosum (highbush ) were harvested from research field plots at the University of Idaho Sandpoint Research and Extension Center. These were (1) Bluecrop, pedigree: GM-37 (Jersey x Pioneer) x CU-5 (Stanley x June); Bluejay, pedrigree: Berkeley x Michigan highbush sel. 241 (Pioneer x Taylor); and (3) Jersey, pedigree: Rubel x Grover. Three cultivars of V. corymbosum x V. angustifolium (half-highbush ) were also collected from this site. These were (1) Northblue, pedigree: (G65 x Ashworth) x U53; Northcountry, pedigree: (G65 x Ashworth) x R2P4; and (3) Northsky, pedigree: (G65 x Ashworth) x R2P4. Two wild genotypes of V. uliginosum were harvested from two separate, naturally occurring stands in Fremont County, Wyoming. Extraction of Group I Berries Berries were extracted using an ASE apparatus (Dionex Corp., Sunnyvale, CA). Five grams of lyophilized berry mixed with 25 g purified sand (Catalog no. S23-3; Fisher Scientific, Pittsburgh, PA) was loaded in the extraction cartridge. Extraction method was set at: heat 5 min, static 1 min, flush volume 1 ml, purge 9 sec, pressure 1 psi, temperature 4 C, extraction solvent methanol:acetone:water:acetic acid (4:4:2:.1), four cycles. Extract was concentrated under vacuum using a rotary evaporator to remove the organic solvents. The resulting aqueous solution was extracted 3 times with 5 ml of ethyl acetate. The combined ethyl acetate extract was evaporated to dryness in a rotavap. Extraction of Group II Berries Lyophilized berries (2 g) were homogenized in 5 ml of extraction solvent (methanol:water:formic acid, 8:2:.1) in a blender (Waring blender model 31BL91; Waring Products Division, Dynamics Corp., New Hartford, CT). The homogenate was transferred to a beaker. The blender was rinsed with 5 ml of the solvent and added to the homogenate in the beaker, which was then placed in an oven at 6 C for 3 min. The sample was allowed to cool to room temperature and vacuum filtered. The residue was washed with 2 ml of extraction solvent, and the combined filtrates (extracts) were concentrated under vacuum in a rotavap to remove methanol. The resulting aqueous solution was divided into two parts of equal volumes. The first portion was extracted 3 times with 15 ml of ethyl acetate and the combined extracts evaporated to dryness in a rotavap. The ph of the other portion was adjusted to 6 using.1m NaOH and then subjected to enzymatic hydrolysis by incubating with 18 mg of β-d-glucosidase (Catalog no. G395-5KU; 4. units/mg; Sigma-Aldrich, Inc., St. Louis, MO) at 37 C for 18 h. After incubation, this solution was extracted with ethyl acetate as was done with the first portion. Analysis of Resveratrol and Analogues To 1 mg of ethyl acetate extract in a GC vial 1 µl of derivatizing reagent [bis(trimethylsilyl)trifluoroacetamide:dimethyl formamide:methanol, 3.5:1:.5] was added. The vial was capped and heated at 7 C in a heating block for 1 h. After cooling to room temperature, the sample was analyzed by gas chromatography/mass spectrometry (GC/MS) on a JEOL (JEOL USA, Inc., Peabody, MA) GCMate II system. The GC temperature program was: initial 15 C, increased to 26 C at a rate of 25 C/min, increased to 27 C at a rate of 1 C/min, increased to 32 C at a rate of 6 C/min, and held at this temperature for 2 min. The GC capillary column used was ZB-5 (.25 mm i.d.,.25 mm film thickness, 3 m length; Phenomenex, Torrance, CA). The carrier gas was ultra high purity helium (nexair, Batesville, MS), 1 ml/min flow rate. The inlet (splitless), GC interface and ion chamber temperatures were 25, 25 and 2 C, respectively. The volume of sample injected was 2 µl. Resveratrol, piceatannol and pterostilbene (retention times 8 min 41 sec, 9 min 29 sec and 1 min 8 sec, respectively) were analyzed in a selected ion monitoring mode. 138
3 Resveratrol was monitored for m/z 444 (and 429, 371, 355 as qualifier ions). Piceatannol was monitored for m/z 532 (and 517, 444, 429 as qualifier ions). Pterostilbene was monitored for m/z 328 (and 313, 297, 281 as qualifier ions). Quantitation was done using external standards of commercial samples of resveratrol (Catalog no. R-51; Sigma- Aldrich, Inc., St. Louis, MO) and piceatannol (Catalog no ; Calbiochem- Novabiochem Corp., San Diego, CA), and a synthetic sample of pterostilbene (see Rimando et al., 22 for method of synthesis). RESULTS AND DISCUSSION Varying amounts of resveratrol, piceatannol and pterostilbene were found in Vaccinium sp. randomly collected from the states of Idaho, Washington and Wyoming (Table 2). The highest resveratrol content (4.668 µg/g) was found in V. ovatum collected in 21 from Webb Hill Rd, Olympic National Forest, Mason County, WA. In a study of three grapevine berry varieties, resveratrol was shown to be absent in variety Pinot Noir uninfected with Botrytis bunch rot (Botrytis cinerea), and only low levels were found in varieties Gamay and Chardonnay (5.7 and 6.7 µg/g fresh weight of skins, respectively; Adrian et al., 2). Resveratrol content as high as 1 µg/g fresh weight of grape skins has been reported (Jang et al., 1997). Levels of resveratrol in grapes vary with times of harvest, environmental and climatic conditions, and plant developmental stage (Bais et al., 2; Eder et al., 21; Keller et al., 2; Moriarty et al., 21). B. cinerea infection as well as UV irradiation induce resveratrol synthesis in grapes (Adrian et al., 2). It is possible that these factors also affect levels of resveratrol in Vaccinium sp. and may account for the variability of resveratrol content of the samples in this study. In this study, piceatannol was found in four samples in group I berries in small quantities (Table 2). Piceatannol was not detected in any berry collected in 22. Pterostilbene was found in relatively high quantities, as high as 1-2 µg/g lyophilized berry (Tables 2 and 3). In grapes, these levels of pterostilbene are found only in fungus-infected berries (Adrian et al., 2). Piceatannol and pterostilbene are generally found in very minute quantities and may be completely absent in grapes. The 3-O-β-glycoside of piceatannol (astringin) has been reported in wine (Ribeiro de Lima et al., 1999) but pterostilbene, glycosylated or not, has not been found in wine. Between the two groups, Group I samples (those collected in 21) appear to have higher contents of the stilbenes. This may be due to difference in extraction. Group I berries were extracted in an automated machine under pressurized condition and a slightly elevated (4 C) temperature conditions, which improve extraction efficiency. With group II samples it was decided to investigate if resveratrol occurs as a glycoside in the berries; thus, milder extraction conditions were used. Results showed that after treatment of the extracts with β-d-glucosidase, resveratrol content increased up to 63 times that found in extract not treated with the enzyme (V. membranaceum, Table 3). Data obtained indicate that resveratrol, as in grapes, also occurs as a glycoside (piceid) in Vaccinium berries. This is significant because it has been shown that resveratrol is absorbed in the small intestines in the form of a glucuronide conjugate (Kuhnle et al., 2). Furthermore, piceid has been shown to also exhibit antioxidant activity (Mérillon et al., 1997). CONCLUSION The highest level of resveratrol found in this study (4.67 µg/g lyophilized berry) is comparable to some reported values found in grapes. Pterostilbene levels ( µg/g lyophilized berry) are relatively higher than those reported in grapevine berries. Piceatannol was detected in only three species (V. membranaceum, and V. ovatum), at levels of µg/g lyophilized berry. Enzymatic hydrolysis of samples collected in 22 yielded an increase in resveratrol content indicating that it is also present in glycosidic form in Vaccinium berries. This is the first report of sequestration of resveratrol as a glucoside in Vaccinium berries. The different amounts of stilbenes in Vaccinium berries could produce varying levels of antioxidant activity and provide cancer chemoprevention, further adding to health benefits derived from consumption of 139
4 Vaccinium fruits (Joseph, 22; Youdim et al., 2), which has been attributed to other classes of polyphenols (e.g. flavonoids and anthocyanins) in the berries. ACKNOWLEDGEMENT The technical help of Ms. Gloria Hervey is gratefully acknowledged. Literature Cited Adrian, M., Jeandet, P., Douillet-Breuil, A.C. and Bessis, R. 2. Stilbene content of mature Vitis vinifera berries in response to UV-C elicitation. J. Agric. Food Chem. 48: Arichi, H., Kimura, Y., Okuda, H., Baba, K., Kosawa, M. and Arichi, S Effects of stilbene components of the roots of Polygonum cuspidatum Sieb. et Zucc. on lipid metabolism. Chem. Pharm. Bull. 3: Bais, A.J., Murphy, P.J. and Dry, I.B. 2. The molecular regulation of stilbene phytoalexin biosynthesis in Vitis vinifera during grape berry development. Aus. J. Plant Physiol. 27: Eder, R., Wendelin, S. and Vrhovsek, U. 21. Resveratrol contents of grapes and red wines in dependency on vintage year and harvest date. Mitteilungen Klosterneuburg 51: Fauconneau, B., Waffo-Teguo, P., Huguet, F., Barrier, L., Decendit, A. and Merillon, J.- M Comparative study of radical scavenger and antioxidant properties of phenolic compounds from Vitis vinifera cell cultures using in vitro tests. Life Sci. 61: Hegsted, D.M and Ausman, L.M Diet, alcohol and coronary heart disease in man. J. Nutr. 118: Hung, L.M., Chen, J.-K., Lee, R.-S., Liang, H.-C. and Su, M.-J. 21. Beneficial effects of astringinin, a resveratrol analogue, on the ischemia and reperfusion damage in rat heart. Free Radical Biol. Med. 3: Keller, M., Steel, C.C. and Creasy, G.L. 2. Stilbene accumulation in grapevine tissues: Developmental and environmental effects. Acta Hort. 514: Jang, M., Cai, L., Udeani, G.O., Slowing, K.V., Thomas, C.F., Beecher, C.W.W., Fong, H.H.S., Farnsworth, N.R., Kinghorn, A.D., Mehta, R.G., Moon, R.C. and Pezzuto, J.M Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science 275: Joseph, J.A. 22. Successful brain aging and polyphenolic intake. Abstracts of Papers, 224 th ACS National Meeting, Boston, MA, United States, August 18-22, 22, AGFD-42. Kuhnle, G., Spencer, J.P.E., Chowromootoo, G., Schroeter, H., Debnam, E.S., Srai, S.K.S., Rice-Evans, C. and Hahn, U. 2. Resveratrol is absorbed in the small intestine as resveratrol glucuronide. Biochem. Biophys. Res. Comm. 272: Lee, S.K., Mbwambo, Z.H., Chung, H., Luyengi, L., Gamez, E.J.C., Mehta, R.G., Kinghorn, A.D. and Pezzuto, J.M Evaluation of the antioxidant potential of natural products. Combinat. Chem. and High Throughput Screen. 1: Mérillon, J.-M., Fauconneau, B., Waffo-Téguo, P., Barrier, L., Vercauteren, J. and Huguet, F Antioxidant activity of the stilbene astringin, newly extracted from Vitis vinifera cell cultures. Clinical Chemistry 43 (Pt. 1): Moriarty, J.M., Harmon, R., Weston, L.A., Bessis, R., Breuil, A.-C., Adrian, M. and Jeandet, P. 21. Resveratrol content of two Californian table grape cultivars. Vitis 4: Potter, G.A., Patterson, L.H., Wanogho, E., Perry, P.J., Butler, P.C., Ijaz, T., Ruparelia, K.C., Lamb, J.H., Farmer, P.B., Stanley, L.A. and Burke, M.D. 22. The cancer chemopreventive agent resveratrol is converted to the anticancer agent piceatannol by the cytochrome P 45 enzyme CYP1B1. British J. Cancer 86: Ribeiro de Lima, M.T., Waffo-Téguo, P., Teissedre, P.L., Pujolas, A., Vercauteren, J., Cabanis, J.C. and Mérillon, J.-M Determination of stilbenes (trans-astringin, 14
5 cis- and trans-piceid, and cis- and trans-resveratrol) in Portuguese wines. J. Agric. Food Chem. 47: Renaud, S. and De Lorgeril, M Wine, alcohol, and the French paradox for coronary heart disease. Lancet 339:1523. Rimando, A.M., Cuendet, M., Desmarchelier, C., Mehta, R.G., Pezzuto, J.M. and Duke, S.O. 22. Cancer chemopreventive and antioxidant activities of pterostilbene, a naturally occurring analogue of resveratrol. J. Agric. Food Chem. 5: Stivala, L.A., Savio, M., Fedarico, C., Perucca, P., Bianchi, L., Magas, G., Forti, L., Pagnoni, U.M., Albini, A., Prosperi, E. and Vannini, V. 21. Specific structural determinants are responsible for the antioxidant activity and the cell cycle effects of resveratrol. J. Biol. Chem. 276: Teguo, P.W., Fauconneau, B., Deffieux, G., Huguet, F., Vercauteren, J. and Mérillon, J.- M Isolation, identification, and antioxidant activity of three stilbene glucosides newly extracted from Vitis vinifera cell cultures. J. Nat. Prod. 61: Youdim, K.A., Shukitt-Hale, B., Martin, A., Wang, H., Denisova, N., Bickford, P.C. and Joseph, J.A. 2. Short-term dietary supplementation of polyphenolics: beneficial effects on aging brain performance and peripheral tissue function. Nutritional Neurosci. 3: Tables Table 1. Site and date of collection of Vaccinium samples. Sample Collection Site Date Group I V. deliciosum Gifford Pinchot National Forest, Skamania County, WA 8/24/21 V. membranaceum (1) Kaniksu National Forest, ID 7/31/21 V. membranaceum V. ovatum (1) V. ovatum V. parvifolium Group II V. corymbosum V. corymbosum x V. angustifolium V. membranaceum V. uliginosum Gifford Pinchot National Forest, Skamania County, WA Wenatchee National Forest, Chelan County, WA Hatchery Lake, Olympic National Forest, Mason County, WA Webb Hill Rd, Olympic National Forest, Mason County, WA Olympic National Forest, Mason County, WA Sandpoint Res. & Ext. Center, Sandpoint, ID Sandpoint Res. & Ext. Center, Sandpoint, ID Bonner County, ID Bonner County, ID Fremont County, WY 8/23/21 8/17/21 11/15/21 11/15/21 8/19/21 7/29 through 8/1 22 7/29 through 8/1 22 7/29/22 7/29/22 8/2/22 141
6 Table 2. Resveratrol, piceatannol and pterostilbene content of group I Vaccinium berries a. Sample Common name Resveratrol Piceatannol Pterostilbene V. deliciosum Blue huckleberry.29 (.1) V. membranaceum (1) Black huckleberry Oval-leaved Evergreen huckleberry Red huckleberry (.22).258 b.68 (.5).331 (.6) V. ovatum (1) (.69).59 b (.29) V. parvifolium 3.56 (1.39) a Values are means of duplicate analysis expressed in µg/g lyophilized berry (± std. dev.). b Value from a single analysis, overlapping peaks prohibited accurate quantitation of the duplicate..315 (.6).753 (.4) b b (.46) Table 3. Resveratrol and pterostilbene content of group II Vaccinium berries a,b. Sample Common name Resveratrol c Resveratrol d Pterostilbene V. corymbosum (1) (3) V. corymbosum x V. angustifolium (1) Highbush Half-highbush.26 (.1).527 (.3) 1.53 (.2).672 (.1) 4.43 (.7) 7.49 (.25) (.29) (.33).128 (.1).124 (.1).475 (.2).32 (.8).945 (.2) (.7).142 (.5) (3) 1. (.3) (.7).353 (.6) V. membranaceum (.1) (.95).127 (.2) Black huckleberry Oval-leaved Alpine bilberry (.4) (1.9) V. uliginosum (1).789 (.3) 5.54 (1.3).512 (.1) e a Values are means of duplicate analysis expressed in µg/g lyophilized berry (± std. dev.). b No piceatannol was found in any of these samples. c Before enzymatic hydrolysis. d After enzymatic hydrolysis. e Value from a single analysis, overlapping peaks prohibited accurate quantitation of the duplicate..214 (.2).129 (.6).139 e 142
7 Figures 4' OH R 2 O 5 3' R 3 3 OR 1 R 1 R 2 R 3 Resveratrol H H H Piceatannol H H OH Pterostilbene CH 3 CH 3 H Fig. 1. Structures of stilbenes analyzed. 143
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