Abstract
Objective
The mechanism action of the polyphenol-rich extracts from berries of Aronia melanocarpa (black chokeberry) and from grape seeds in the defence against homocysteine (Hcy) and its derivatives action in blood platelets is still unknown. In this study, the influence of the aronia extract and grape seeds extract (GSE) on the platelet adhesion to collagen and fibrinogen and the platelet aggregation during a model of hyperhomocysteinemia was investigated. The aim of our study in vitro was also to investigate superoxide anion radicals (O −•2 ) production after incubation of platelets with Hcy, HTL and the aronia extract and GSE during a model of hyperhomocysteinemia (induced by reduced form of homocysteine at final dose of 100 μM) and the most reactive form of Hcy—its cyclic thioester, homocysteine thiolactone (HTL, 1 μM). Moreover, the additional aim of our study was also to establish and compare the influence of the aronia extract, GSE and resveratrol (3,4′,5-trihydroxystilben), a phenolic compound, which has been supposed to be beneficial for the prevention of cardiovascular events, on selected steps of platelet activation.
Methods
The effects of tested extracts on adhesion of blood platelets to collagen and fibrinogen were determined according to Tuszynski and Murphy. The platelet aggregation was determined by turbidimetry method using a Chrono-log Lumi-aggregometer.
Results
We have observed that HTL, like its precursor—Hcy stimulated the generation of O −•2 (measured by the superoxide dismutase—inhibitable reduction of cytochrome c) in platelets and caused an augmentation of the platelet adhesion and aggregation induced by the strong physiological agonist—thrombin. Our present results in vitro also demonstrated that the aronia extract and grape seeds extract reduced the toxicity action of Hcy and HTL on blood platelet adhesion to collagen and fibrinogen, the platelet aggregation and superoxide anion radicals production in platelets, suggesting its potential protective effects on hemostasis during hyperhomocysteinemia.
Conclusion
In the comparative studies, the aronia extract was found to be more effective antiplatelet factors, than GSE or resveratrol during a model of hyperhomocysteinemia. It gives hopes for development of diet supplements, which may be important during hyperhomocysteinemia.
Similar content being viewed by others
References
Kahkonen MP, Hopia AI, Vuorela HJ, Rauha JP, Pihlaja K, Kujala TS, Heinonen M (1999) Antioxidant activity of plant extracts containing phenolics compounds. J Agric Food Chem 47:3954–3962
Valcheva-Kuzmanova SV, Belcheva A (2006) Current knowledge of Aronia melanocarpa as a medicinal plant. Folia Med 48:11–17
Kulling SE, Rawel HM (2008) Chokeberry (Aronia melanocarpa)—a review on the characteristic components and potential health effects. Planta Med 74:1625–1634
Kokotkiewicz A, Jeremicz Z, Luczkiewicz M (2010) Aronia plants: a review of traditional use, biological activities, and perspectives for modern medicine. J Med Food 13:255–269
Olas B, Kedzierska M, Wachowicz B, Stochmal A, Oleszek W (2010) Effects of polyphenol-rich extract from berries of Aronia melanocarpa on the markers of oxidative stress and blood platelet activation. Platelets 21:274–281
Olas B, Wachowicz B, Nowak P, Kedzierska M, Tomczak A, Stochmal A, Oleszek W, Jeziorski A, Piekarski J (2008) Studies on antioxidant properties of polyphenol-rich extract from berries of Aronia melanocarpa in blood platelets. J Physiol Pharmacol 59:823–835
Chrubasik C, Li G, Chrubasik S (2010) The clinical effectiveness of chokeberry: a systematic review. Phytother Res 24:1107–1114
Olas B, Kędzierska M, Wachowicz B, Stochmal A, Oleszek W, Jeziorski A, Piekarski J, Głowacki R (2010) Effect of aronia on thiol levels in plasma of breast cancer patients. Cent Eur J Biol 5:38–46
Kedzierska M, Olas B, Wachowicz B, Stochmal A, Oleszek W, Jeziorski A, Piekarski J (2010) The nitrative and oxidative stress in blood platelets isolated from breast cancer patients; the protectory action of Aronia melanocarpa extract. Platelets 21:541–548
Kedzierska M, Olas B, Wachowicz B, Glowacki R, Bald E, Czernek U, Szydlowska-Pazera K, Potemski P, Piekarski J, Jeziorski A (2012) 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 83:310–317
Malinowska J, Babicz K, Olas B, Stochmal A, Oleszek W (2012) Aronia melanocarpa extract suppresses biotoxicity of homocysteine and its metabolite on hemostatic activity of fibrinogen and plasma. Nutrition 28:793–798
Olas B, Wachowicz B, Tomczak A, Erler J, Stochmal A, Oleszek W (2008) 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 19:70–77
Olas B, Wachowicz B, Stochmal A, Oleszek W (2012) The polyphenol-rich extract from grape seeds inhibits platelet signaling pathway triggered by both proteolytic and non-proteolytic agonists. Platelets 23:282–289
Kolodziejczyk J, Malinowska J, Olas B, Stochmal A, Oleszek W, Erler J (2011) The polyphenol-rich extract from grape seeds suppresses toxicity of homocysteine and its thiolactone on the fibrinolytic system. Thromb Res 127:489–491
Das S, Das DK (2006) Wine and the heart: a journey from grapes to resveratrol. S Afr J Enol Vitic 27:127–132
Halliwell B (2000) Lipid peroxidation, antioxidants and cardiovascular disease: how should we move forward? Cardiovasc Res 47:410–418
Visioli F, Borsani L, Galli C (2000) Diet and prevention of coronary heart disease: the potential role of phytochemicals. Cardiovasc Res 47:419–425
Olas B, Wachowicz B (2005) Resveratrol, a phenolic antioxidant with effects on blood platelet functions. Platelets 16:251–260
Wu K (1996) Platelet activation mechanisms and marker in arterial thrombosis. J Inter Med 239:17–34
Alexandru N, Jardin I, Popov D, Simionescu M, Garcia-Estan J, Salido GM, Rosado JA (2007) Effect of homocysteine on calcium mobilization and platelet function in type 2 diabetes mellitus. J Cell Mol Med 14:111–117
Iuliano L, Colavita AR, Leo R, Practico D, Violi F (1997) Oxygen free radicals and platelet activation. Free Rad Biol Med 22:999–1006
Wachowicz B, Olas B, Zbikowska HM, Buczynski A (2002) Generation of reactive oxygen species in blood platelets. Platelets 13:175–182
Doolittle RF, Schubert D, Schwartz SA (1967) Amino acid sequence studies on artiodactyl fibrinopeptides I Dromedary camel, mule deer, and cape buffalo. Arch Biochem Biophys 118:456–467
Kedzierska M, Olas B, Wachowicz B, Stochmal A, Oleszek W, Jeziorski A, Piekarski J, Glowacki R (2009) An extract from berries of Aronia melanocarpa modulates the generation of superoxide anion radicals in blood platelets from breast cancer patients. Planta Med 75:1405–1409
Bald E, Chwatko G, Glowacki R, Kusmierek K (2004) Analysis of plasma thiols by high-performance liquid chromatography with ultraviolet detection. J Chromatogr 1032:109–115
Glowacki R, Bald E, Jakubowski H (2011) An on-column derivatization method for the determination of homocysteine-thiolactone and protein N-linked homocysteine. Amino Acids 41:187–194
Wachowicz B, Kustron J (1992) Effect of cisplatin on lipid peroxidation in pig blood platelets. Cytobios 70:41–47
Walkowiak B, Michalak E, Koziolkiewicz W, Cierniewski CS (1989) Rapid photometric method for estimation of platelet count in blood plasma or platelet suspension. Thromb Res 56:763–766
Tuszynski GP, Murphy A (1990) Spectrophotometric quantitation of anchorage—dependent cell numbers using the bicinchoninic acid protein assay reagent. Anal Biochem 184:189–191
Olas B, Mielicki W, Wachowicz B, Krajewski T (1999) Cancer procoagulant (CP) stimulates platelet adhesion. Thromb Res 94:199–203
Olas B, Zbikowska HM, Wachowicz B, Krajewski T, Buczynski A, Magnuszewska A (1999) Inhibitory effect of resveratrol on free radical generation in blood platelets. Acta Biochim Polon 46:961–966
Jahn B, Hansch GM (1990) Oxygen radical generation in human platelets: depended of 12-lipoxygenase activity and on the glutathione cycle. Int Arch Allergy Appl Immunol 93:73–79
Carluccio MA, Ancora MA, Massaro M, Carluccio M, Scoditti E, Distante A, Storelli C, De Caterina R (2007) Homocysteine induces VCAM-1 gene expression through NF-kappaB and NAD(P)H oxidase activation: protective role of Mediterranean diet polyphenolic antioxidants. Am J Physiol Heart Circ Physiol 293:H2344–H2354
Perla-Kajan J, Twardowski T, Jakubowski H (2007) Mechanisms of homocysteine toxicity in humans. Amino Acids 32:561–572
Olas B, Kedzierska M, Wachowicz B (2008) Comparative studies on homocysteine and its metabolite—homocysteine thiolactone action in blood platelets in vitro. Platelets 19:520–527
Sibrian-Vazquez M, Escobedo JO, Lim S, Samoei GK, Strongin RM (2010) Homocystamides promote free-radical and oxidative damage to proteins. Proc Natl Acad Sci USA 107:551–554
Kolling J, Scherer EB, da Cunha AA, da Cunha MJ, Wyse AT (2011) Homocysteine induces oxidative-nitrative stress in heart of rats: prevention by folic acid. Cardiovasc Toxicol 11:67–73
Fu W, Conklin BS, Lin PH, Lumsden AB, Yao Q, Chen C (2003) Red wine prevents homocysteine-induced endothelial dysfunction in porcine coronary arteries. J Surg Res 115:82–91
Malinowska J, Olas B (2010) Effect of resveratrol on hemostatic properties of human fibrinogen and plasma during model of hyperhomocysteinemia. Thromb Res 126:e379–e382
Malinowska J, Olas B (2011) Response of blood platelets to resveratrol during model of hyperhomocysteinemia. Platelets 22:277–283
Olas B, Malinowska J, Rywaniak J (2010) Homocysteine and its thiolactone may promote apoptotic events in blood platelets in vitro. Platelets 21:533–540
Noll C, Hamelet J, Matulewicz E, Paul JL, Delabar JM, Janel N (2009) Effects of red wine polyphenolic compounds on paraoxonase-1 and lectin-like oxidized low-density lipoprotein receptor-1 in hyperhomocysteinemic mice. J Nutr Bichem 20:586–596
Kowalczyk E, Fijalkowski P, Kura M, Krzesinski P, Blaszczyk J, Kowalski J, Smigielski J, Rutkowski M, Kopff M (2005) The influence of anthocyanins from Aronia melanocarpa on selected parameters of oxidative stress and microelements contents in men with hypercholesterolemia. Pol Merkur Lekarski 19:651–653
Ryszawa N, Kawczynska-Drozdz A, Pryjma J, Czesnikiewicz-Guzik M, Adamek-Guzik T, Naruszewicz M et al (2006) Effects of novel plant antioxidants on platelet superoxide production and aggregation in arteriosclerosis. J Physiol Pharmacol 57:611–626
Brito O, Almeida LM, Dinis TCP (2002) The interaction of resveratrol with ferrylmyoglobin and peroxynitrite; protection against LDL oxidation. Free Radic Res 36:621–631
Houde V, Greinier D, Chandad F (2006) Protective effects of grape seed proanthocyanidins against oxidative stress induced by lipopolysaccharides of periodontopathogenes. J Periodontol 77:1371–1379
Bijak M, Bobrowski M, Borowiecka M, Podstedek A, Golanski J, Nowak P (2011) Anticoagulant effect of polyphenols-rich extracts from blac chokeberry and grape seeds. Fitoterapia 82:811–817
Zhang Y, Shi H, Wang W, Ke Z, Xu P, Zhong Z, Li X, Wang S (2010) Antithrombotic effect of grape seed proanthocyanidins extract in a rat model of deep vein thrombosis. J Vasc Surg 53:743–753
Signorello MG, Pascale R, Leoncini G (2002) Effect of homocysteine on arachidonic acid release in human platelets. Eur J Clin Invest 32:279–284
Signorello MG, Viviani GL, Armani U, Cerone R, Minniti G, Piana A, Leoncini G (2007) Homocysteine, reactive oxygen species and nitric oxide in type 2 diabetes mellitus. Thromb Res 120:607–613
Leoncini G, Bruzzese D, Signorello MG (2007) A role for PLCγ2 in platelet activation by homocysteine. J Cell Biochem 100:1255–1265
Leoncini G, Bruzzese D, Signorello MG (2006) Activation of p38MAPKinase/cPLA2 pathway in homocysteine treated platelets. J Thromb Haemos 4:209–216
Undas A, Stepien E, Plicner D, Zielinski L, Tracz W (2007) Elevated total homocysteine is associated with increased platelet activation at the site of microvascular injury. Effects of folic acid administration. J Thromb Haemost 5:1070–1072
Karolczak K, Olas B (2009) Mechanism action of homocysteine and its thiolactone in haemostasis system. Physiol Res 58:623–633
Olas B, Kolodziejczyk J, Kedzierska M, Rywaniak J, Wachowicz B (2009) Modification of blood platelet proteins induced by homocysteine and its thiolactone in vitro. Thromb Res 124:689–694
McGarrigle SA, O’Neill S, Walsh GM, Moran N, Groham IM, Cooney MT, Monavari A, Mayne P, Collins P (2011) Integrin αIIbβ3 exists in an activated state in subjects with elevated plasma homocysteine levels. Platelets 22:63–71
Malinowska J, Olas B, Oleszek W, Stochmal A. Extract from aronia as a modulator of adhesive properties of fibrinogen during hyperhomocysteinemia. Cent Eur J Biol (submitted)
Acknowledgments
This work was supported by grant (No 0365/B/PO1/2011/40) from National Science Centre (Poland) and statutory activities of Institute of Soil Science and Plant Cultivation, Pulawy (Poland).
Conflict of interest
None to declare.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Malinowska, J., Oleszek, W., Stochmal, A. et al. The polyphenol-rich extracts from black chokeberry and grape seeds impair changes in the platelet adhesion and aggregation induced by a model of hyperhomocysteinemia. Eur J Nutr 52, 1049–1057 (2013). https://doi.org/10.1007/s00394-012-0411-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00394-012-0411-8