Skip to main content
SpringerLink
Log in

Modulation of Oxidative Stress in Thrombin-Stimulated Platelets by Almond by-Product

  • Original Paper
  • Published:
Waste and Biomass Valorization Aims and scope Submit manuscript

Abstract

Almond (Al) green hulls are waste materials that are generated annually in the almond harvest and recently gained much attention due to their antioxidant properties. However, paucity information is in literature relevant to the modern pharmacological effects of Al green hulls. The aim of this study was to evaluate anti-platelet activity of Persian Al hull extract. The antioxidant activity of Al hull extract was investigated employing various established in vitro system including total antioxidant activity in linoleic acid emulsion system and DPPH assay. Platelet aggregation was monitored by spectrophotometer and intracellular ROS activity was evaluated by flow cytometry. Chemical composition of extract was determined by gas chromatography-mass spectrometry. In vitro study showed that Al hull extract at 100 μg/ml inhibited thrombin-induced platelet aggregation and protein secretion by 50%, without any cytotoxic effects on platelets. Moreover, based on different free radical trapping assay, it has been revealed that the examined extract had high antioxidant capacity and could suppress ROS generation in thrombin-stimulated platelets. GC-MS analyses revealed that Al hull extract contains a variety of phenolic and benzoic acid compounds dominated by ferulic acid, p-coumaric acid, quercetin, homovanilic acid, catechin and methoxysalsylic acid. Collectively high antioxidant capacity of Al hull extract and also its anti-platelet activity with lack of toxicity, give validity to this agricultural waste material as appropriate candidate for treatment of cardiovascular diseases and thrombosis.

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

Access this article

Log in via an institution

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

ACD:

Anticoagulant citrate dextrose

Al:

Almond

APA:

Anti-platelet aggregation

BSTFA:

N,O-bis(trimethylsilyl)trifluoroacetamide

DCFH-DA:

2,7- dichloroflourescin diacetate

GC-MS:

Gas chromatography-mass spectrometry

LDH:

Lactate dehydrogenase

MDA:

Malondialdehyde

NAC:

N-acetylcysteine

PBS:

Phosphate buffered saline

ROS:

Reactive oxygen species

RT:

Room temperature

TBA:

Thiobarbituric acid

TMCS:

Trimethylchlorosilane

TCA:

Trichloroacetic acid

References

  1. Takeoka, G.R., Dao, L.T.: Antioxidant constituents of almond [Prunus dulcis (Mill.) D.A. Webb] hulls. J. Agric. Food Chem. 51, 496–501 (2003)

    Article  Google Scholar 

  2. Takeoka, G., Dao, L., Teranishi, R., Wong, R., Flessa, S., Harden, L., et al.: Identification of three triterpenoids in almond hulls. J. Agric. Food Chem. 48, 3437–3439 (2000)

    Article  Google Scholar 

  3. Sang, S., Lapsley, K., Rosen, R.T., Ho, C.T.: New prenylated benzoic acid and other constituents from almond hulls (Prunus amygdalus Batsch). J. Agric. Food Chem. 50, 607–609 (2002)

    Article  Google Scholar 

  4. Meshkini, A. Acetone extract of almond hulls provides protection against oxidative damage and membrane protein degradation. J. Acupunct. Meridian. Stud. 9, 134–142 (2016)

    Article  Google Scholar 

  5. Freedman, J.E.: Oxidative Stress and Platelets. Arterioscler. Thromb. Vasc. Biol. 28, 11–16 (2008)

    Article  Google Scholar 

  6. Handin, R.I., Karabin, R., Boxer, G.J.: Enhancement of platelet function by superoxide anion. J. Clin. Invest. 59, 959–965 (1977)

    Article  Google Scholar 

  7. Lopez, J.J., Salido, G.M., Gomez-Arteta, E., Rosado, J.A., Pariente, J.A.: Thrombin induces apoptotic events through the generation of reactive oxygen species in human platelets. J. Thromb. Haemost. 5, 1283–1291 (2007)

    Article  Google Scholar 

  8. Piccirillo, C., Rodrigues, C.L., Pintado, M.E., Castro, P.M.L. Extraction of Valuable Compounds from Ginja Cherry By-Products: Effect of the Solvent and Antioxidant Properties. Waste Biomass Valori. 2, 365–371 (2011)

    Article  Google Scholar 

  9. Proestos, C., Boziaris, I.S., Nychas, G.J.E., Komaitis, M.: Analysis of flavonoids and phenolic acids in Greek aromatic plants: Investigation of their antioxidant capacity and antimicrobial activity. Food Chem. 95, 664–671 (2006)

    Article  Google Scholar 

  10. Rojas, R., Contreras-Esquivel, J., Orozco-Esquivel, M.T., Munoz, C., Aguirr-Joya, J.A., Aguilar, C.N.: Mango Peel as source of antioxidants and pectin: microwave assisted extraction. Waste Biomass Valori. 6, 1095–1102 (2015)

    Article  Google Scholar 

  11. Pownall, T.L., Udenigwe, C.C., Aluko, R.E.: Amino acid composition and antioxidant properties of pea seed (Pisum sativum L.) enzymatic protein hydrolysate fractions. J. Agric. Food Chem. 58, 4712–4718 (2010)

    Article  Google Scholar 

  12. Olas, B., Hamed, A.I., Oleszek, W., Stochmal, A.: Extracts from Tribulus species may modulate platelet adhesion by interfering with arachidonic acid metabolism. Platelets. 26, 87–92 (2015)

    Article  Google Scholar 

  13. Bertino, A.M., Qi, X.Q., Li, J., Xia, Y., Kuter, D.J.: Apoptotic markers are increased in platelets stored at 37 °C. Transfusion. 43, 857–866 (2003)

    Article  Google Scholar 

  14. Meshkini, A., Yazdanparast, R.: Involvement of oxidative stress in taxol-induced apoptosis in chronic myelogenous leukemia K562 cells. Exp. Toxicol. Pathol. 64, 357–365 (2012)

    Article  Google Scholar 

  15. Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J.: Protein measurement with the folin phenol reagent. J. Biol. Chem. 193, 265–275 (1951)

    Google Scholar 

  16. Drapper, H.H., Hadley, M.: Malondialdehyde determination as index of lipid peroxidation. Methods Enzymol. 186, 421–431 (1990)

    Article  Google Scholar 

  17. Caccese, D., Pratico, D., Ghiselli, A., Natoli, S., Pignatelli, P., Sanguigni, V., Iuliano, L., Violi, F.: Superoxide anion and hydroxyl radical release by collagen-induced platelet aggregation–role of arachidonic acid metabolism. Thromb. Haemost. 83, 485–490 (2008)

    Article  Google Scholar 

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

    Article  Google Scholar 

  19. Siriwardhana, S.K.W., Shahidi, F.: Antiradical activity of extracts of almond and its by-products. J. Am. Oil Chem. Soc. 79, 903–908 (2002)

    Article  Google Scholar 

  20. Wijerante, S.S.K., Amarowicz, R., Shahidi, F.: Antioxidant activity of almonds and their by-products in food model systems. J. Am. Oil Chem. Soc. 83, 223–230 (2006)

    Article  Google Scholar 

  21. Ostertag, L.M., OKennedy, N., Horgan, G.W., Kroon, P.A., Duthie, G.G., 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. 55, 1624–1636 (2011)

    Article  Google Scholar 

  22. Luceri, C., Giannini, L., Lodovici, M., Antonucci, E., Abbate, R., Masini, E., Dolara, P.: p-Coumaric acid, a common dietary phenol, inhibits platelet activity in vitro and in vivo. Br. J. Nutr. 97, 458–463 (2007)

    Article  Google Scholar 

  23. Oh, W.J., Endale, M., Park, S.C., Cho, J.Y., Rhee, M.H.: Dual Roles of quercetin in platelets: phosphoinositide-3-Kinase and MAP kinases inhibition, and cAMP-dependent vasodilator-stimulated phosphoprotein stimulation. Evi. Based Complement Altern. Med. 2012, 485262 (2012)

    Google Scholar 

  24. Rasul, A.L., Khan, M., Ali, M., Li, J., Li, X.: Targeting apoptosis pathways in cancer with alantolactone and isoalantolactone. Sci. World J. 2013, 248532 (2013)

    Article  Google Scholar 

  25. Chen, H.H., Wang, T.C., Lee, Y.C., Shen, P.T., Chang, J.Y., Yeh, T.K., Huang, C.H., Chang, H.H., Cheng, S.Y., Lin, C.Y., Shih, C., Chen, C.T., Liu, W.M., Chen, C.H., Kuo, C.C.: Novel Nrf2/ARE activator, trans-Coniferylaldehyde, induces a HO-1-mediated defense mechanism through a dual p38α/MAPKAPK-2 and PK-N3 signaling pathway. Chem. Res. Toxicol. 28, 1681–1692 (2015)

    Article  Google Scholar 

  26. Esfahlan, A.J., Jamei, R., Esfahlan, R.J.: The importance of almond (Prunus amygdalus L.) and its by-products. Food Chem. 120, 349–360 (2010)

    Article  Google Scholar 

  27. Geleijnse, J.M., Launer, L.J., Hofman, A., Pols, H.A., Witteman, J.C.: Tea flavonoids may protect against atherosclerosis: the Rotterdam Study. Arch. Intern. Med. 159, 2170–2174 (1999)

    Article  Google Scholar 

  28. Kris-Etherton, P.M., Keen, C.L.: Evidence that the antioxidant flavonoids in tea and cocoa are beneficial for cardiovascular health. Curr. Opin. Lipidol. 13, 41–49 (2002)

    Article  Google Scholar 

  29. Kim, M.S., Shin, W.C., Kang, D.K., Sohn, H.Y.: Anti-thrombosis activity of sinapic acid isolated from the lees of Bokbunja wine. J. Microbiol. Biotechnol. 26, 61–65 (2016)

    Article  Google Scholar 

  30. Krotz, F., Sohn, H.Y., Gloe, T., Zahler, S., Riexinger, T., Schiele, T.M., Becker, B.F., Theisen, K., Klauss, V., Pohl, U.: NAD(P)H-oxidase-dependent platelet superoxide anion release increases platelet recruitment. Blood. 100, 917–924 (2002)

    Article  Google Scholar 

  31. Corti, R., Flammer, A.J., Hollenberg, N.K., Lüscher, T.F.: Cocoa and cardiovascular health. Circulation. 119, 1433–1441 (2009)

    Article  Google Scholar 

  32. Loffredo, L., Carnevale, R., Perri, L., Catasca, E., Augelletti, T., Albanese, F., Piccheri, C., Nocella, C., Pignatelli, P., Violi, F.: NOX2-mediated arterial dysfunction in smokers: acute effect of dark chocolate. Heart. 97, 1776–1781 (2011)

    Article  Google Scholar 

Download references

Acknowledgements

The author appreciates the financial support of this investigation by the Research Council of Ferdowsi University of Mashhad (Grant No. 2/29843).

Author information

Authors and Affiliations

  1. Department of Chemistry, Faculty of Science, Ferdowsi University of Mashhad, P. O. Box 9177948974, Mashhad, Iran

    Azadeh Meshkini

Authors
  1. Azadeh Meshkini
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Azadeh Meshkini.

Ethics declarations

Conflict of interest

There is no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Meshkini, A. Modulation of Oxidative Stress in Thrombin-Stimulated Platelets by Almond by-Product. Waste Biomass Valor 9, 1015–1025 (2018). https://doi.org/10.1007/s12649-016-9801-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12649-016-9801-0

Keywords

Search

Navigation