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Stabilization of erythrocytes against oxidative and hypotonic stress by tannins isolated from sumac leaves (Rhus typhina L.) and grape seeds (Vitis vinifera L.)

Abstract

Erythrocytes are constantly exposed to ROS due to their function in the organism. High tension of oxygen, presence of hemoglobin iron and high concentration of polyunsaturated fatty acids in membrane make erythrocytes especially susceptible to oxidative stress. A comparison of the antioxidant activities of polyphenol-rich plant extracts containing hydrolysable tannins from sumac leaves (Rhus typhina L.) and condensed tannins from grape seeds (Vitis vinifera L.) showed that at the 5–50 μg/ml concentration range they reduced to the same extent hemolysis and glutathione, lipid and hemoglobin oxidation induced by erythrocyte treatment with 400 μM ONOO or 1 mM HClO. However, extract (condensed tannins) from grape seeds in comparison with extract (hydrolysable tannins) from sumac leaves stabilized erythrocytes in hypotonic NaCl solutions weakly. Our data indicate that both hydrolysable and condensed tannins significantly decrease the fluidity of the surface of erythrocyte membranes but the effect of hydrolysable ones was more profound. In conclusion, our results indicate that extracts from sumac leaves (hydrolysable tannins) and grape seeds (condensed tannins) are very effective protectors against oxidative damage in erythrocytes.

Abbreviations

DPH:

1,6-diphenyl-1,3,5-hexatriene

GSH:

reduced glutathione

HClO:

hypochlorous acid

metHb:

methemoglobin

ONOO :

peroxynitrite

TMA-DPH:

1-(4-trimethylammoniumphenyl)-6-phenyl-1,3,5-hexatriene

References

  1. Martindale, J.L. and Holbrook, N.J. Cellular response to oxidative stress: signaling for suicide and survival. J. Cell Physiol. 192 (2002) 1–15.

    Article  PubMed  CAS  Google Scholar 

  2. Esteva, S., Pedret, R., Fort, N., Torrella, J.R., Pages, T. and Viscor, G. Oxidative stress status in rats after intermittent exposure to hypobaric hypoxia. Wilderness Environ. Med. 21 (2010) 325–331.

    Article  PubMed  Google Scholar 

  3. Roitman, E.V., Dement’eva, I.I., Azizova, O.A., Nikitina, E.V., Gagaeva, E.V. and Lopukhin, Iu.M. Changes in blood rheological properties and erythrocyte osmotic resistance in activation of free radical processes. Klin. Lab. Diagn. 3 (2001) 42–43.

    PubMed  Google Scholar 

  4. Brzeszczynska, J., Luciak, M. and Gwozdzinski, K. Alterations of erythrocyte structure and cellular susceptibility in patient with chronic renal failure: effect of haemodialysis and oxidative stress. Free Radic. Res. 42 (2008) 40–48.

    Article  PubMed  CAS  Google Scholar 

  5. Samukawa, K., Suzuki, Y., Ohkubo, N., Aoto, M., Sakanaka, M. and Mitsuda, N. Protective effect of ginsenosides Rg(2) and Rh(1) on oxidation-induced impairment of erythrocyte membrane properties. Biorheology 45 (2008) 689–700.

    PubMed  CAS  Google Scholar 

  6. Hatherill, J.R., Till, G.O. and Ward, P.A. Mechanisms of oxidant-induced changes in erythrocytes. Agents Actions 32 (1991) 351–358.

    Article  PubMed  CAS  Google Scholar 

  7. Nikolaidis, M.G. and Jamurtaz, A.Z. Blood as a reactive species generator and redox status regulator during exercise. Arch. Biochem. Biophys. 490 (2009) 77–84.

    Article  PubMed  CAS  Google Scholar 

  8. Nagababu, E., Mohanty, J.G., Ghamidipaty, S., Ostera, G.R. and Rifkind, J.M. Role of the membrane in the formation of heme degradation products in red blood cells. Life Sci. 86 (2010) 133–138.

    Article  PubMed  CAS  Google Scholar 

  9. Kiefmann, R., Rifkind, J.M., Nagababu, E. and Bhattacharya, J. Red blood cells induce hypoxic lung inflammation. Blood 111 (2008) 5205–5214.

    Article  PubMed  CAS  Google Scholar 

  10. Lang, F., Lang, K.S., Lang, P.A., Huber, S.M. and Wieder, T. Osmotic shock-induced suicidal death of erythrocytes. Acta Physiol. (Oxf.) 187 (2006) 191–198.

    Article  CAS  Google Scholar 

  11. Minetti, M., Agati, L. and Malorni, W. The microenvironment can shift erythrocytes from a friendly to a harmful behavior: Pathogenetic implications for vascular diseases. Cardiovasc. Res. 75 (2007) 21–28.

    Article  PubMed  CAS  Google Scholar 

  12. Minetti, M., Pietraforte, D., Straface, E., Metere, A., Matarrese, P. and Malorni, W. Red blood cells as a model to differentiate between direct and indirect oxidation pathways of peroxynitrite. Methods Enzymol. 440 (2008) 253–272.

    Article  PubMed  CAS  Google Scholar 

  13. Haslam, E. Natural polyphenols (vegetable tannins) as drugs: possible modes of action. J. Nat. Prod. 59 (1996) 205–215.

    Article  PubMed  CAS  Google Scholar 

  14. Haslam, E. Vegetable tannins — Lessons of a phytochemical lifetime. Phytochemistry 68 (2007) 2713–2721.

    Article  PubMed  CAS  Google Scholar 

  15. Koleckar, V., Kubikova, K., Rehakova, Z., Kuca, K., Jun, D., Jahodar, L. and Opletal, L. Condensed and hydrosable tannins as antioxidants influencing the healt. Mini Rev. Med. Chem. 8 (2008) 436–447.

    Article  PubMed  CAS  Google Scholar 

  16. Zhu, Q.Y., Schramm, D.D., Gross, H.B., Holt, R.R., Kim, S.H., Yamaguchi, T., Kwik-Uribe, C.L. and Keen, C.L. Influence of cocoa flavanols and procyanidins on free radical-induced human erythrocyte hemolysis. Clin. Dev. Immunol. 12 (2005) 27–34.

    Article  PubMed  CAS  Google Scholar 

  17. Sangeetha, P., Balu, M., Haripriya, C. and Pannerselvam, C. Age associated changes in erythrocyte membrane surface change: Modulatory role of grape seed proanthocyanidins. Exp. Gerontol. 40 (2005) 820–828.

    Article  PubMed  CAS  Google Scholar 

  18. Carini, M., Aldini, G., Bombardelli, E., Morazzoni, P. and Facino, R.M. UVB-induced hemolysis of rat erythrocytes: Protective effect of procyanidins from grape seeds. Life Sci. 67 (2000) 1799–1814.

    Article  PubMed  CAS  Google Scholar 

  19. Fedeli, D., Berrettini, M., Gabryelak, T. and Falcioni G. The effect of some tannins on trout erythrocytes exposed to oxidative stress. Mutat. Res. 563 (2004) 89–96.

    PubMed  CAS  Google Scholar 

  20. Olchowik, E., Sciepuk, A., Mavlyanov, S., Abdulladjanova, N. and Zamaraeva, M. Antioxidant capacities of polyphenols from Sumac (Rhus typhina L.) leaves in protection of erythrocytes against oxidative damage. Biomed. Prev. Nutr. (2011), doi:10.1016/j.bionut.2011.06.008

  21. Islambekov, Sh.Yu., Mavlyanov, S.M., Kamaev, F.G. and Ismailov, A.I. Phenolic compounds of sumac. Chem. Nat. Comp. 30 (1994) 37–39.

    Article  Google Scholar 

  22. Pirniyazov, A.Zh., Abdulladzhanova, N.G., Mavlyanov, S.M., Kamaev, F.G. and Dalimov, D.N. 2003. Polyphenols from Vitis vinifera seeds. Chem. Nat. Comp. 39 (2003) 349–354.

    Article  CAS  Google Scholar 

  23. Soszyński, M. and Bartosz, G. Effect of peroxynitrite on erythrocytes. Biochim. Biophys. Acta 1291 (1996) 107–114.

    Article  PubMed  Google Scholar 

  24. Yagi, K. and Rastogi, R. Assay for lipid peroxides in animals tissues by thiobarbituric acid reaction. Annu. Rev. Biochem. 95 (1979) 351–358.

    Article  Google Scholar 

  25. Pietraforte, D., Matarrese, P., Straface, E., Gambardella, L., Metere, A., Scorza, G., Leto, T.L., Malorni, W. and Minetti, M. Two different pathways are involved in peroxynitrite-induced senescence and apoptosis of human erythrocytes. Free Radic. Biol. Med. 42 (2007) 202–214.

    Article  PubMed  CAS  Google Scholar 

  26. Zavodnik, L.B., Zavodnik, I.B., Lapshyna E.A., Buko, V.U. and Bryszewska, M.J. Hypochlorous acid-induced membrane pore formation in red blood cells. Bioelectrochemistry 58 (2002) 157–161.

    Article  PubMed  CAS  Google Scholar 

  27. Ionov, M., Gordiyenko, N., Olchowik, E., Baram, N., Zijaev, K., Salakhutdinov, B., Bryszewska, M. and Zamaraeva, M. The immobilization of gossypol derivative on N-polyvinylpyrrolidone increases its water solubility and modifies membrane-active properties. J. Med. Chem. 52 (2009) 4119–4125.

    Article  PubMed  CAS  Google Scholar 

  28. Salikhov, Sh.I., Mavlyanov, S.M., Abdulladjanova, N.G., Pirniyazov, A.J., Dalimov, D.N., Salakhutdinov, B.A. and Kurmukov A.G. Polyphenols of some tannin containing plants and creation on their base drug remedies. New Research on Biotechnology and Medicine. New York: Nova Science (2006) 109–117.

  29. Amer, J., Ghoti, H., Rachmilewitz, E., Koren, A., Lenin, C. and Fibach, E. Red blood cells, platelets and polymorphonuclear neutrophils of patients with sickle cell disease exhibit oxidative stress that can be ameliorated by antioxidants. Br. J. Haematol. 132 (2006) 108–113.

    Article  PubMed  CAS  Google Scholar 

  30. Aslan, M. and Freeman, B.A. Redox-dependent impairment of vascular function in sickle cell disease. Free Radic. Biol. Med. 43 (2007) 1469–1483.

    Article  PubMed  CAS  Google Scholar 

  31. Pandey, K.B. and Rizvi, S.I. Markers of oxidative stress in erythrocytes and plasma during aging in humans. Oxid. Med. Cell Longev. 3 (2010) 2–12.

    Article  PubMed  Google Scholar 

  32. Sola, E., Vaya, A., Martinez, M., Moscardo, A., Corella, D., Santaolaria, M. L., Espana, F. and Mijares, A.H. Erythrocyte membrane phosphatidylserine exposure in obesity. Obesity (Silver Spring) 17 (2008) 318–322.

    Google Scholar 

  33. Hagerman, A.E., Riedl, K.M., Jones, G.A., Sovik, K.N., Ritchard, N.T, Hartzfeld, P.W. and Riechel, T.L. High molecular weight plant polyphenolics (tannins) as biological antioxidants. J. Agric. Food Chem. 46 (1998) 1887–1892.

    Article  CAS  Google Scholar 

  34. Tarahovsky, Y.S. Plant polyphenols in cell-cell interaction and communication. Plant Signal. Behav. 3 (2008) 609–611.

    Article  PubMed  Google Scholar 

  35. Scalbert, A. and Williamson, G. Dietary intake and bioavailability of polyphenols. J. Nutr. 130 (2000) 2073–2085.

    Google Scholar 

  36. Koren, E., Kohen, R. and Ginsburg, I. Polyphenols enhance total oxidant — scavenging capacities of human blood by binding to red blood cells. Exp. Biol. Med. (Maywood) 235 (2010) 689–699.

    Article  CAS  Google Scholar 

  37. Pennathur, S., Maitra, D., Byun, J., Slikovic, I., Abdulhamid, I., Saed, G.M., Diamond, M.P. and Abu-Soud, H.M. Potent antioxidative activity of lycopene: A potential role in scavenging hypochlorous acid. Free Radic. Biol. Med. 49 (2010) 205–213.

    Article  PubMed  CAS  Google Scholar 

  38. Zavodnik, I.B., Lapshina, E.A., Zavodnik, L.B., Bartosz, G., Soszynski, M. and Bryszewska, M. Hypochlorous acid damages erythrocyte membrane proteins and alters lipid bilayer structure and fluidity. Free Radic. Biol. Med. 30 (2001) 363–369.

    Article  PubMed  CAS  Google Scholar 

  39. Robaszkiewicz, A., Greig, F.H., Pitt, A.R., Spickett, C.M., Bartosz, G. and Soszynski, M. Effect of phosphatidylcholine chlorohydrins on human erythrocytes. Chem. Phys. Lipids 163 (2010) 639–647.

    Article  PubMed  CAS  Google Scholar 

  40. Kleinbongard, P., Schulz, R., Rassaf, T., Lauer, T., Dejam, A., Jax, T., Kumara, I., Gharini, P., Kabanosa, S., Ozüyaman, B., Schnürch, H.G., Gödecke, A., Weber, A.A., Roberek, M., Roberek, H., Bloch, W., Rösen, P. and Kelm, M. Red blood cells express a functional endothelial nitric oxide synthase. Blood 107 (2006) 2943–2951.

    Article  PubMed  CAS  Google Scholar 

  41. Starodubtseva, M.N., Tattersall, A.L., Kuznetsova, T.G., Yegorenkov, N.I. and Ellory, J.C. Structural and functional changes in the membrane and membrane skeleton of red blood cells induced by peroxynitrite. Bioelectrochemistry 73 (2008) 155–162.

    Article  PubMed  CAS  Google Scholar 

  42. Rubbo, H., Trostchansky, A. and O’Donnell, V.B. Peroxynitrite-mediated lipid oxidation and nitration: mechanisms and consequences. Arch. Biochem. Biophys. 15 (2009) 167–172.

    Article  Google Scholar 

  43. Balavoine, G.A. and Geletti, Y.V. Peroxynitrite scavenging by different antioxidants. Part I: Convenient assay. Nitric Oxide 3 (1999) 40–54.

    Article  PubMed  CAS  Google Scholar 

  44. Tsuda, T., Kato, Y. and Osawa, T. Mechanism for peroxynitrite scavenging activity by anthocyanins. FEBS Lett. 484 (2000) 207–210.

    Article  PubMed  CAS  Google Scholar 

  45. Marzouk, M.S., Moharram, F.A., Mohamed, M.A., Gama-Eldeen, A.M. and Aboutabl. E.A. Anticancer and antioxidant tannins from Pimenta dioica leaves. Z. Naturforsch. C 62 (2007) 526–536.

    PubMed  CAS  Google Scholar 

  46. Romero, N., Denicola, A. and Radi, R. Red blood cells in the metabolism of nitric oxide-derived peroxynitrite. IUBMB Life 58 (2006) 572–580.

    Article  PubMed  CAS  Google Scholar 

  47. Hapner, C.D., Deuster, P. and Chen, Y. Inhibition of oxidative hemolysis by quercetin, but not other antioxidants. Chem. Biol. Interact. 186 (2010) 275–279.

    Article  PubMed  CAS  Google Scholar 

  48. Solarska, K., Lewińska, A., Karowicz-Bilińska, A. and Bartosz, G. The antioxidant properties of carnitine in vitro. Cell. Mol. Biol. Lett. 15 (2010) 90–97.

    Article  PubMed  CAS  Google Scholar 

  49. Verstraeten, S.V., Oteiza, P.I. and Fraga, C.G. Membrane effects of cocoa procyanidins in liposomes and Jurkat T cells. Biol. Res. 37 (2004) 293–300.

    Article  PubMed  Google Scholar 

  50. Labieniec, M. and Gabryelak, T. Effects of tannins on Chinese hamster cell line B14. Mutat. Res. 539 (2003) 127–135.

    PubMed  CAS  Google Scholar 

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Correspondence to Maria Zamaraeva.

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Paper authored by participant of the international conference: 18th Meeting, European Association for Red Cell Research, Wrocław — Piechowice, Poland, May 12–15th, 2011. Publication cost was covered by the organizers of this meeting.

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Olchowik, E., Lotkowski, K., Mavlyanov, S. et al. Stabilization of erythrocytes against oxidative and hypotonic stress by tannins isolated from sumac leaves (Rhus typhina L.) and grape seeds (Vitis vinifera L.). Cell Mol Biol Lett 17, 333–348 (2012). https://doi.org/10.2478/s11658-012-0014-7

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