Skip to main content

Advertisement

Log in

The polyphenol-rich extracts from black chokeberry and grape seeds impair changes in the platelet adhesion and aggregation induced by a model of hyperhomocysteinemia

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. 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

    Article  CAS  Google Scholar 

  2. Valcheva-Kuzmanova SV, Belcheva A (2006) Current knowledge of Aronia melanocarpa as a medicinal plant. Folia Med 48:11–17

    Google Scholar 

  3. Kulling SE, Rawel HM (2008) Chokeberry (Aronia melanocarpa)—a review on the characteristic components and potential health effects. Planta Med 74:1625–1634

    Article  CAS  Google Scholar 

  4. 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

    Article  CAS  Google Scholar 

  5. 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

    Article  CAS  Google Scholar 

  6. 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

    CAS  Google Scholar 

  7. Chrubasik C, Li G, Chrubasik S (2010) The clinical effectiveness of chokeberry: a systematic review. Phytother Res 24:1107–1114

    CAS  Google Scholar 

  8. 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

    Article  Google Scholar 

  9. 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

    Article  CAS  Google Scholar 

  10. 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

    Article  CAS  Google Scholar 

  11. 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

    Google Scholar 

  12. 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

    Article  CAS  Google Scholar 

  13. 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

    Google Scholar 

  14. 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

    Article  CAS  Google Scholar 

  15. Das S, Das DK (2006) Wine and the heart: a journey from grapes to resveratrol. S Afr J Enol Vitic 27:127–132

    Google Scholar 

  16. Halliwell B (2000) Lipid peroxidation, antioxidants and cardiovascular disease: how should we move forward? Cardiovasc Res 47:410–418

    Article  CAS  Google Scholar 

  17. Visioli F, Borsani L, Galli C (2000) Diet and prevention of coronary heart disease: the potential role of phytochemicals. Cardiovasc Res 47:419–425

    Article  CAS  Google Scholar 

  18. Olas B, Wachowicz B (2005) Resveratrol, a phenolic antioxidant with effects on blood platelet functions. Platelets 16:251–260

    Article  CAS  Google Scholar 

  19. Wu K (1996) Platelet activation mechanisms and marker in arterial thrombosis. J Inter Med 239:17–34

    Article  CAS  Google Scholar 

  20. 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

    Google Scholar 

  21. Iuliano L, Colavita AR, Leo R, Practico D, Violi F (1997) Oxygen free radicals and platelet activation. Free Rad Biol Med 22:999–1006

    Article  CAS  Google Scholar 

  22. Wachowicz B, Olas B, Zbikowska HM, Buczynski A (2002) Generation of reactive oxygen species in blood platelets. Platelets 13:175–182

    Article  CAS  Google Scholar 

  23. 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

    Article  CAS  Google Scholar 

  24. 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

    Article  CAS  Google Scholar 

  25. 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

    Article  CAS  Google Scholar 

  26. 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

    Article  CAS  Google Scholar 

  27. Wachowicz B, Kustron J (1992) Effect of cisplatin on lipid peroxidation in pig blood platelets. Cytobios 70:41–47

    CAS  Google Scholar 

  28. 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

    Article  CAS  Google Scholar 

  29. Tuszynski GP, Murphy A (1990) Spectrophotometric quantitation of anchorage—dependent cell numbers using the bicinchoninic acid protein assay reagent. Anal Biochem 184:189–191

    Article  CAS  Google Scholar 

  30. Olas B, Mielicki W, Wachowicz B, Krajewski T (1999) Cancer procoagulant (CP) stimulates platelet adhesion. Thromb Res 94:199–203

    Article  CAS  Google Scholar 

  31. 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

    CAS  Google Scholar 

  32. 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

    Article  CAS  Google Scholar 

  33. 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

    Article  CAS  Google Scholar 

  34. Perla-Kajan J, Twardowski T, Jakubowski H (2007) Mechanisms of homocysteine toxicity in humans. Amino Acids 32:561–572

    Article  CAS  Google Scholar 

  35. 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

    Article  CAS  Google Scholar 

  36. 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

    Article  CAS  Google Scholar 

  37. 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

    Article  CAS  Google Scholar 

  38. 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

    Article  CAS  Google Scholar 

  39. 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

    Article  CAS  Google Scholar 

  40. Malinowska J, Olas B (2011) Response of blood platelets to resveratrol during model of hyperhomocysteinemia. Platelets 22:277–283

    Article  CAS  Google Scholar 

  41. Olas B, Malinowska J, Rywaniak J (2010) Homocysteine and its thiolactone may promote apoptotic events in blood platelets in vitro. Platelets 21:533–540

    Article  CAS  Google Scholar 

  42. 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

    Article  CAS  Google Scholar 

  43. 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

    Google Scholar 

  44. 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

    CAS  Google Scholar 

  45. 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

    Article  CAS  Google Scholar 

  46. 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

    Article  CAS  Google Scholar 

  47. 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

    Article  CAS  Google Scholar 

  48. 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

    Google Scholar 

  49. Signorello MG, Pascale R, Leoncini G (2002) Effect of homocysteine on arachidonic acid release in human platelets. Eur J Clin Invest 32:279–284

    Article  CAS  Google Scholar 

  50. 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

    Article  CAS  Google Scholar 

  51. Leoncini G, Bruzzese D, Signorello MG (2007) A role for PLCγ2 in platelet activation by homocysteine. J Cell Biochem 100:1255–1265

    Article  CAS  Google Scholar 

  52. Leoncini G, Bruzzese D, Signorello MG (2006) Activation of p38MAPKinase/cPLA2 pathway in homocysteine treated platelets. J Thromb Haemos 4:209–216

    Article  CAS  Google Scholar 

  53. 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

    Article  CAS  Google Scholar 

  54. Karolczak K, Olas B (2009) Mechanism action of homocysteine and its thiolactone in haemostasis system. Physiol Res 58:623–633

    CAS  Google Scholar 

  55. 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

    Article  CAS  Google Scholar 

  56. 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

    Article  Google Scholar 

  57. 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)

Download references

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

Authors

Corresponding author

Correspondence to Joanna Malinowska.

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-012-0411-8

Keywords

Navigation