The multifunctionality of berries toward blood platelets and the role of berry phenolics in cardiovascular disorders

References

• Allender S, Scarboraugh P, Peto V, Rayner M. European Cardiovascular Disease Statistics 2008. 3rd ed. London, European Heart Network.
   Google Scholar
• Blockmans D, Deckmyn H, Vermylen J. Platelet activation. Blood Rev 1995;9:143–156.
   PubMed Web of Science ®Google Scholar
• Olas B, Wachowicz B. Role of reactive nitrogen species in blood platelet functions. Platelets 2007;18:555–565.
   PubMed Web of Science ®Google Scholar
• McEwen BJ. The influence of diet and nutrients on platelet function. Semin Thromb Hemost 2014;40:214–226.
   PubMed Web of Science ®Google Scholar
• Kallio H, Yang B, Halttunen T. Flavonol glycosides of berries of three major sea buckthorn subspecies, Hippophae rhamnoides ssp. rhamnoides, ssp. sinensis, and ssp. mongolica. Proc Invited Speeches Second Int Seabuckthorn Assoc. Conf. 2005;29–35.
   Google Scholar
• Kumar R, Kumar GP, Chaurasia OP, Singh S. Phytochemical and pharmacological profile of Sea buckthorn oil: a review. Res J Med Planta 2011;5:491–499.
   Google Scholar
• Suryakumar G, Gupta A. Medicinal and therapeutic potential of Sea buckthorn (Hippophae rhamnoides L.). J Ethnopharmacol 2011;138:268–278.
   PubMed Web of Science ®Google Scholar
• Christaki E. Hippophae Rhamnoides L. (Sea Buckthorn): a potential source of nutraceuticals. Food Public Health 2012;2:69–72.
   Google Scholar
• Malinowska P, Olas B. Sea buckthorn – valuable plant for health. Kosmos 2016;2:285–292.
   Google Scholar
• Sneader W. The discovery of aspirin: a reappraisal. BMJ 2000;321:1591–1594.
   PubMed Web of Science ®Google Scholar
• Kulling SE, Rawel HM. Chokeberry (Aronia melanocarpa) – A review on the characteristic components and potential health effects. Planta Med 2008;74:1625–1634.
   PubMed Web of Science ®Google Scholar
• MFF Chong, Macdonald R, Lovegrove JA. Fruit polyphenols and CDV risk: a review of human intervention studies. Br J Nutr 2010;104:S28–S39.
   PubMed Web of Science ®Google Scholar
• Chrubasik C, Li G, Chrubasik S. The clinical effeciveness of chokeberry: a systematic review. Phytother Res 2010;24:1107–1114.
   PubMed Web of Science ®Google Scholar
• Wightman JLD, Henberger RA. Effect of grape and other berries on cardiovascular health. J Sci Food Agric 2015;95:1584–1597.
   PubMed Web of Science ®Google Scholar
• Szajdek A, Borowska EJ. Bioactive compounds and health-promoting properties of berry fruits: a review. Plant Foods Hum Nutr 2008;63:147–156.
   PubMed Web of Science ®Google Scholar
• Nile SH, Park SW. Edible berries: bioactive components and their effect of human health. Nutrition 2014;30:134–144.
   PubMed Web of Science ®Google Scholar
• Teleszko M, Wojdylo A, Rudzinska M, Oszmianski J, Golis T. Analysis of lipophilic and hydrophilic bioactive compounds content in sea buckthorn (Hippophae rhamnoids L.) berries. J Agric Food Chem 2015;63:4120–4129.
   PubMed Web of Science ®Google Scholar
• Dyduch-Sieminska M, Najda A, Dyduch J, Gantner M, Klimek K. The content of secondary metabolites and antioxidant activity of wild strawberry fruit (Fragaria vesca L.). J Anal Methods Chem 2015;1–8.
   Web of Science ®Google Scholar
• Giampieri F, Tulipani S, Alvarez-Suarez JM, Quiles JL, Mezzetti B, Battino M. The strawberry: composition, nutritional quality, and impact on human health. Nutr 2012;28:9–19.
   PubMed Web of Science ®Google Scholar
• Zanotti I, Dall’Asta M, Mena P, Mele L, Bruni R, Ray S, del Rio D. Atheroprotective effects of (poly)phenols: a focus on cell cholesterol metabolism. Food Funct 2005;6:13–31.
   Web of Science ®Google Scholar
• Wilczak J, Kamola D, Jank M. Bioavailability of polyphenolic compounds and their influence on antioxidant potential of rat plasma. Probl Hig Epidemiol 2013;94:532–535.
   Google Scholar
• Yang M, Koo SI, Song WO, Chun OK. Food matrix affecting anthocynanin bioavailability: review. Curr Med Chem 2011;18:291–300.
   PubMed Web of Science ®Google Scholar
• McGhie TK, Alton MC. The bioavailability and absorption of anthocyanins: towards a better understanding. Mol Nutr Food Res 2007;51:702–713.
   PubMed Web of Science ®Google Scholar
• Speciale A, Cimino F, Saija A, Canali R, Virgili F. Bioavailability and molecular activities of anthocyanins as modulators of endothelial function. Genes Nutr 2014;9:404.
   PubMed Web of Science ®Google Scholar
• Santhakumar AB, Stanley R, Singh I. The ex vivo antiplatelet activation potential of fruit phenolic metabolite hippuric acid. Food Funct 2015;6:2679–2683.
   PubMed Web of Science ®Google Scholar
• Scalbert A, Williamson G. Dietary intake and bioavailability of polyphenols. J Nutr 2000;130:2073–2085.
   PubMed Web of Science ®Google Scholar
• Kuntz S, Rudloff S, Asseburg H, Brsch C, Frohling B, Unger F, Dold S, Spengler B. Uptake and biovailability of anthocyanins and phenolic acids from grape/blueberry juice and smoothie in vitro and in vivo. Br J Nutr 2015;113:1044–1055.
   PubMed Web of Science ®Google Scholar
• Del Bo C, Riso P, Brambill A, Gardana C, Rizzolo A, Simonetti P, Bertolo G, Klimis-Zacas D, Porrini M. Blanching improves anthocyanin absorption from highbush blueberry (Vaccinium corymbosum L.) puree in healthy human volunteers: a pilot study. J Agric Food Chem 2012;60:9298–9304.
   PubMed Web of Science ®Google Scholar
• Vitaglione P, Donnrumma G, Napolitno A, Galvano F, Gallo A, Scalfi L, Fogliano V. Protocatechuic acid is the major human metabolite of cyaniding-glucosides. J Nutr 2007;137:2043–2048.
   PubMed Web of Science ®Google Scholar
• Toromanovic J, Kovac-Besovic E, Sapcainin A, Tahirovic I, Rimpapa Z, Kroyer G, Sofic E. Urinary hippuric acid after ingestion of edible fruits. Bosn J Basic Med Sci 2008;8:38–43.
   PubMed Web of Science ®Google Scholar
• Terahara N. Flavonoids in foods: a review. Nat Prod Commun 2015;10:521–528.
   PubMed Web of Science ®Google Scholar
• Cheng J, Kondo K, Suzuki Y, Ikeda Y, Meng X, Umemura K. Inhibitory effects of total flavones of Hippophae rhamnoides L. on thrombosis in mouse femoral artery and in vitro platelet aggregation. Life Sci 2003;72:2263–2271.
   PubMed Web of Science ®Google Scholar
• Sayegh M, Miglio C, Ray S. Potential cardiovascular implications of sea buckthorn berry consumption in humans. Int J Food Sci Nutr 2014;65:521–528.
   PubMed Web of Science ®Google Scholar
• Koyama T, Taka A, Togashi H. Effects of a herbal medicine, Hippophae rhamnoides, on cardiovascular functions and coronary microvessels in the spontaneously hypertensive stroke-prone rat. Clin Hemorheol Microcirc 2009;41:17–26.
   PubMed Web of Science ®Google Scholar
• Parzonko A, Naruszewicz M. Cardioprotective effects of aronia melanocarpa anthocyanins. From laboratory experiments to clinical practice. Curr Pharm Des 2015;22:174–179.
   Web of Science ®Google Scholar
• Zeb A. Chemical and nutritional constituents of sea buckthorn juice. Pak J Nutr 2004;3:99–106.
   Google Scholar
• Fatima T, Snyder CL, Schroeder W, Cram D, Datla R, Wishart D, Weselake RJ, Krishna P. Fatty acid composition of developing sea buckthorn (Hippophae rhamnoides L.) berry and the transcriptome of the mature seed. Plos One 2012;7:1–18.
   Web of Science ®Google Scholar
• Rissanen TH, Voutilainen S, Virtanen JK, Venho B, Vanharanta M, Mursu J, Salonen JT. Low intake of fruits, berries and vegetables is associated with excess mortality in men: the Kuopio Ischaemic Heart Disease Risk Factor (KIHD) study. J Nutr 2003;133:199–204.
   PubMed Web of Science ®Google Scholar
• Ellingse I, Hjerkinn E, Seljeflot I, Arnesen H, Tonstad S. Consumption of fruit and berries is inversely associated with carotid atherosclerosis in elderly men. Br J Nutr 2008;99:674–681.
   PubMed Web of Science ®Google Scholar
• Eccleston C, Baoru Y, Tahvonem R, Kallio H, Rimbach GH, Minihane AM. Effects of an antioxidant-rich juice (sea buckthorn) on risk factors for coronary heart disease in humans. J Nutr Biochem 2002:13:346–354.
   PubMed Web of Science ®Google Scholar
• Negi B, Kaur R, Dey G. Protective effects of a novel sea buckthorn wine on oxidative stress and hypercholesterolemia. Food Funct 2013;4:240–248.
   PubMed Web of Science ®Google Scholar
• Xu XY, Kaur M, Dhillon RS, Tappia PS, Dhalla NS. Health benefits of sea buckthorn for the prevention of cardiovascular diseases. J Funct Foods 2011;3:2–12.
   Web of Science ®Google Scholar
• Erlund I, Koli R, Alfthan G, Marniemi J, Puukka P, Mustonen P, Mattila P, Jula A. Favorable effects of berry consumption of platelet function, blood pressure, and HDL cholesterol. Am J Clin Nutr 2008;87:323–331.
   PubMed Web of Science ®Google Scholar
• Sikora J, Markowicz-Piasecka M, Broncel M, Mikiciuk-Olasik E. Extract of Aronia melanocarpa-modified hemostasis: in vitro studies. Eur J Nutr 2014;53:1493–1502.
   PubMed Web of Science ®Google Scholar
• Olas B, Kontek B, Malinowska P, Żuchowski J, Stochmal A. Hippophae rhamnoides L. fruits reduce the oxidative stress in human blood platelets and plasma. Oxid Med Cell Longev 2016;1–8.
   Web of Science ®Google Scholar
• Daskalova E, Delchev S, Peeva Y, Vladimirova-Kitova L, Kratchanova M, Kratchanov C, Denev P. Antiatherogenic and cardioprotective effects of black chokeberry (Aronia melanocarpa) juice in aging rats. Evidence-Based Complem Alter Med 2015;1–10.
   Google Scholar
• Olas B, Wachowicz B, Tomczak A, Erler J, Stochmal A, Oleszek W. Comparative anti-platelet and antioxidant properties of polyphenol-rich extracts from: berries of Aronia melanocarpa, seeds of grape, bark of Yucca schidigera in vitro. Platelets 2008;19:70–77.
   PubMed Web of Science ®Google Scholar
• Kontek B, Szczęsna M, Żuchowski J, Stochmal A, Olas B. Effects of Hippophae rhamnoides L. fruits on different steps of blood platelet activation. AJPM (sub.).
   Google Scholar
• Żbikowska HM, Olas B, Wachowicz B, Krajewski T. Response of blood platelets to resveratrol. Platelets 1999;10:247–252.
   PubMed Web of Science ®Google Scholar
• Żbikowska HM, Olas B. Antioxidants with carcinostatic activity (resveratrol, vitamin E and selenium) in modulation of blood platelet adhesion. J Physiol Pharmacol 2000;3:513–520.
   Google Scholar
• Malinowska J, Oleszek W, Stochmal A, Olas B. The polyphenol-rich extracts from black chokeberry and grape seeds impair changes in the platelet adhesion and aggregation induced by hyperhomocysteinemia. Eur J Nutr 2013;52:1049–1057.
   PubMed Web of Science ®Google Scholar
• Pace-Asciak CR, Rounova O, Hahn SE, Diamandis EP, Goldberg DM. Wines and grape juices as modulators of platelet aggregation in healthy subjects. Clin Chim Acta 1996;246:163–182.
   PubMed Web of Science ®Google Scholar
• Keevil JG, Osman HE, Reed JD, Folt JD. Grape juice, but not orange juice or grapefruit juice, inhibits human platelet aggregation. J Nutr 2000;130:53–56.
   PubMed Web of Science ®Google Scholar
• Freedman JE, Parker C, Li L, Perlan JA, Frei B, Ivanov V, Deak LR, Iafrati MD, Folts JD. Select flavonoids and whole juice from purple grapes inhibit platelet function and enhance nitric oxide release. Circul 2001;103:2792–2798.
   PubMed Web of Science ®Google Scholar
• Polagruto JA, Gross HB, Kamangar F, Kosuna K, Sun B, Fujii H, Keen CL, Hackman RM. Platelet reactivity in male smokers following the acute consumption of a flavanol-rich grape seed extract. J Med Food 2007;10:725–730.
   PubMed Web of Science ®Google Scholar
• Ostertag LM, O’Kennedy N, Horgan GW, Kroon PA, Duthie GG, de Roos B. In vitro anti-platelet effects of simple plant-derived phenolic compounds are only found at high, non-physiological concentrations. Mol Nutr Food Res 2011;55:1624–1636.
   PubMed Web of Science ®Google Scholar
• Rotondo S, Rotilio D, Cerletti CH, De Gaetano G. Red wine, aspirin and platelet function. Thromb Haemostas 1996;76:813–821.
   PubMed Web of Science ®Google Scholar
• Malinowska J, Olas B. Response of blood platelets to resveratrol during model of hyperhomocysteinemia. Platelets 2011;22:277–283.
   PubMed Web of Science ®Google Scholar
• Shanmuganayagam D, Beahm MR, Osman HE, Krueger CG, Reed JD, Folts JD. Grape seed and grape skin extracts elicit a greater antiplatelet effect when used in combination than when used individually in dogs and humans. J Nutr 2002;132:3592–3598.
   PubMed Web of Science ®Google Scholar
• Sikora J, Broncel M, Markowicz M, Chalubinski M, Wojdan K, Mikiciuk-Olasik E. Short-term supplementation with Aronia melanocarpa extract improves platelet aggregation, clotting, and fibrinolytsis in patients with metabolic syndrome. Eur J Nutr 2012;51:549–556.
   PubMed Web of Science ®Google Scholar
• Wilson T, Bauer BA. Advising consumers about dietary supplements: lessons from cranberry products. J Diet Suppl 2009;6:377–384.
   PubMedGoogle Scholar
• Alarcon M, Fuentes E, Olate N, Navarrete S, Carrasco G, Palomo I. Strawberry extract presents antiplatelet activity by inhibition of inflammatory mediator of atherosclerosis (sP-selectin, sCD40L, RANTES, and IL-1β) and thrombus formation. Platelets 2015;26:224–229.
   PubMed Web of Science ®Google Scholar
• Watkins TR, Bierenbaum ML. Grape juice attenuates cardiovascular risk factors in the hyperlipemic subject. Pharmaceut Biol 1998;36:75–80.
   Web of Science ®Google Scholar
• Shanmuanayagam D, Warner TF, Krueger CG, Reed JD, Folts JD. Concord grape juice attenuates platelet aggregation, serum cholesterol and development of atheroma in hypercholesterolemic rabbits. Atherosclerosis 2007;190:135–142.
   PubMed Web of Science ®Google Scholar
• Ryszawa N, Kawczynska-Drodz A, Pryjma J, Czesnikiewicz-Guzik M, Adamek-Guzik T, Naruszewicz M, Korbut R, Guzik TJ. Effects of novel plant antioxidants on platelet superoxide production and aggregation in atherosclerosis. J Physiol Pharmacol 2006;57:611–626.
   PubMed Web of Science ®Google Scholar
• Naruszewicz M, Laniewska I, Millo B, Dluzniewski M. Combination therapy of statin with flavonoids rich extract from chokeberry fruits enhanced reduction in cardiovascular risk markers in patients after myocardial infraction (MI). Atherosclerosis 2007;194:179–184.
   PubMed Web of Science ®Google Scholar
• Luzak B, Golanski J, Różalski M, Krajewska U, Olas B, Watała C. Extract from Aronia melanocarpa fruits potentiates the inhibition of platelet aggregation in the presence of endothelial cells. Arch Med Sci 2010;2:141–144.
   Web of Science ®Google Scholar
• Olas B, Wachowicz B, Stochmal A, Oleszek W. The polyphenol-rich extract from grape seeds inhibits platelet signaling pathways triggered by both proteolytic and non-proteolytic agonists. Platelets 2012;23:282–289.
   PubMed Web of Science ®Google Scholar
• Olas B, Wachowicz B, Szewczuk J, Saluk-Juszczak J, Kaca W. The effect of resveratrol on the platelet secretory process induced by endotoxin and thrombin. Microbios 2011;105:7–13.
   Google Scholar
• Olas B, Żbikowska HM, Wachowicz B, Krajewski T, Buczyński A, Magnuszewska A. Inhibitory effect of resveratrol on free radical generation in blood platelets. Acta Bioch Pol 1999;46:961–966.
   PubMed Web of Science ®Google Scholar
• Olas B, Wachowicz B, Saluk-Juszczak J, Zieliński T, Kaca W, Buczyński A. Antioxidant activity of resveratrol in endotoxin – stimulated blood platelets. Cell Biol Toxicol 2001;17:117–125.
   PubMed Web of Science ®Google Scholar
• Olas B, Wachowicz B, Saluk-Juszczak J, Zieliński T. Effect of resveratrol, a natural polyphenolic compound, on platelet activation induced by endotoxin or thrombin. Thromb Res 2002;107:141–145.
   PubMed Web of Science ®Google Scholar
• Olas B, Nowak P, Kołodziejczyk J, Wachowicz B. The effects of antioxidants on peroxynitrite-induced changes in platelet proteins. Thromb Res 2004;113:399–406.
   PubMed Web of Science ®Google Scholar
• Olas B, Nowak P, Wachowicz B. Resveratrol protects against peroxynitrite – induced thiol oxidation in blood platelets. Cell Mol Biol Let 2004;9:577–587.
   PubMed Web of Science ®Google Scholar
• Olas B, Nowak P, Ponczek M, Wachowicz B. Natural phenolic compound - resveratrol may reduce carbonylation of proteins induced by peroxynitrite in blood platelets. General Physiol Biophys 2006;25:215–222.
   PubMed Web of Science ®Google Scholar
• Olas B, Nowak P, Kolodziejczyk J, Ponczek M, Wachowicz B. Protective effects of resveratrol against oxidative/nitrative modifications of plasma proteins and lipids exposed to peroxynitrite. J Nutr Biochem 2006;17:96–102.
   PubMed Web of Science ®Google Scholar
• Subbaramaiah K, Chung WJ, Michaluart P, Telang N, Tanabe T, Inoue H, Jang M, Pezzuto JM, Dannenberg AJ. Resveratrol inhibits cyclooxygenase-2 transcription and activity in phorbol ester-treated human mammary epithelial cells. J Biol Chem 1998;273:21875–21882.
   PubMed Web of Science ®Google Scholar
• Olas B, Wachowicz B, Holmsen H, Fukami M. Resveratrol inhibits polyphosphoinositide cycle in activated platelets. BBA-Biomembranes 2005;1714:125–133.
   PubMed Web of Science ®Google Scholar
• Dobrydneva Y, Willimas RL, Blackmore PF. Trans-resveratrol inhibits calcium influx in thrombin- stimulated human platelets. Br J Pharmacol 1999;128;149–157.
   PubMed Web of Science ®Google Scholar
• Jagroop IA. Plant extracts inhibit ADP-induced platelet activation in humans: their potential therapeutic role as ADP antagonists. Purinergic Signal 2014;10:233–239.
   PubMed Web of Science ®Google Scholar
• Kędzierska M, Olas B, Wachowicz B, Stochmal A, Oleszek W, Jeziorski A, Piekarski J, Głowacki R. An extract from berries of Aronia melanocarpa modulates the generation of superoxide anion radicals in blood platelets from breast cancer patients. Planta Med 2009;75:1405–1409.
   PubMed Web of Science ®Google Scholar
• Kędzierska M, Olas B, Wachowicz B, Stochmal A, Oleszek W, Jeziorski A, Piekarski J. The nitrative and oxidative stress in blood platelets isolated from breast cancer patients; the protectory action of Aronia melanocarpa extract. Platelets 2010;21:541–548.
   PubMed Web of Science ®Google Scholar
• Kedzierska M, Olas B, Wachowicz B, Glowacki R, Bald E, Czernek U, Szydłowska-Pazera K, Potemski P, Piekarski J, Jeziorski A. Effects of the commercial extract of aronia on oxidative stress in blood platelets isolated from breast cancer patients after the surgery and various phases of the chemotherapy. Fitoterapia 2012;83:310–217.
   PubMed Web of Science ®Google Scholar
• Malinowska J, Olas B. Effect of resveratrol on hemostatic properties of human fibrinogen and plasma during model of hyperhomocysteinemia. Thromb Res 2010;126:379–382.
   PubMed Web of Science ®Google Scholar
• Malinowska J, Babicz K, Olas B, Stochmal A, Oleszek W. Aronia melanocarpa extract suppresses biotoxicity of homocysteine and its metabolite on hemostatic activity of fibrinogen and plasma. Nutrition 2012;28:793–798.
   PubMed Web of Science ®Google Scholar
• Torres-Urruita C, Guzman L, Schmeda-Hirschmann G, Moore-Carrasco R, Alarcon M, Astudillo L, Gutierrez M, Carrasco G, Yuri JA, Aranda E, I. Palomo Antiplatelet, anticoagulant, and fibrinolytic activity in vitro of extracts from selected fruits and vegetables. Blood Coagul Fibrinol 2011;22:197–205.
   PubMed Web of Science ®Google Scholar
• Kolodziejczyk J, Malinowska J, Olas B, Stochmal A, Oleszek W, Erler J. The polyphenol-rich extract from grape seeds suppresses toxicity of homocysteine and its thiolactone on the fibrinolytic system. Thromb Res 2011;127:489–491.
   PubMed Web of Science ®Google Scholar
• Wright B, Tindall MJ, Lovegrove JA, Gibbins JM. Investigating flavonoids as molecular templates fort he design of small-molecule inhibitors of cell signalling. J Food Sci 2013;78:N1921–N1928.
   PubMed Web of Science ®Google Scholar
• Stein JH, Keevil JG, Wiebe DA, Aeschlimann S, Folts JD. Purple grape juice improves endothelial function and reduces the susceptibility of LDL cholesterol to oxidation in patients with coronary artery disease. Circulation 1999;100:1050–1055.
   PubMed Web of Science ®Google Scholar
• Chou EJ, Keevil JG, Aeschlimann S, Wiebe DA, Folts JD, Stein JH. Effect of ingestion of purple grape juice on endothelial function in patients with coronary heart disease. Am J Cardiol 2001;88:553–555.
   PubMed Web of Science ®Google Scholar
• Reul G, Pomerleau S, Couture P, Lamarche B, Couillard C. Changes in plasma antioxidant capacity and oxidized low-density lipoprotein levels in men after short-term cranberry juice consumption. Metabolism 2005;54:856–861.
   PubMed Web of Science ®Google Scholar