The Journal of Membrane Biology

, Volume 247, Issue 8, pp 703–712 | Cite as

Antioxidant Capacity of Ugni molinae Fruit Extract on Human Erythrocytes: An In Vitro Study

  • Mario Suwalsky
  • Marcia Avello


Ugni molinae is an important source of molecules with strong antioxidant activity widely used as a medicinal plant in Southern Chile–Argentina. Total phenol concentration from its fruit extract was 10.64 ± 0.04 mM gallic acid equivalents. Analysis by means of HPLC/MS indicated the presence of the anthocyanins cyanidin and peonidin, and the flavonol quercitin, all in glycosylated forms. Its antioxidant properties were assessed in human erythrocytes in vitro exposed to HClO oxidative stress. Scanning electron microscopy showed that HClO induced an alteration in erythrocytes from a normal shape to echinocytes; however, this change was highly attenuated in samples containing U. molinae extracts. It also had a tendency in order to reduce the hemolytic effect of HClO. In addition, X-ray diffraction experiments were performed in dimyristoylphosphatidylcholine (DMPC) and dimyristoylphosphatidylethanolamine bilayers, classes of lipids preferentially located in the outer and inner monolayers, respectively, of the human erythrocyte membrane. It was observed that U. molinae only interacted with DMPC. Results by fluorescence spectroscopy on DMPC large unilamellar vesicles and isolated unsealed human erythrocyte membranes also showed that it interacted with the erythrocyte membrane and DMPC. It is possible that the location of U. molinae components into the membrane outer monolayer might hinder the diffusion of HClO and of free radicals into cell membranes and the consequent decrease of the kinetics of free radical reactions.


Ugni molinae Fruit extract Antioxidant Human erythrocyte membrane 



Scanning electron microscopy


Red blood cell suspension






Reactive oxygen species


Gallic acid equivalents


Large unilamellar vesicles


Isolated unsealed human erythrocyte membranes



To FONDECYT (Project 1130043) and to P. Osorio and Dr. C. P. Sotomayor for valuable technical assistance.


  1. Arora A, Byren T, Nair M, Strasburg G (2000) Modulation of liposomal membrane fluidity by flavonoids and isoflavonoids. Arch Biochem Biophys 373:102–109CrossRefPubMedGoogle Scholar
  2. Battistelli M, De Sanctis R, De Bellis R, Cucchiarini L et al (2005) Rhodiola rosea as antioxidant in red blood cells: ultrastructural and hemolytical behavior. Eur J Histochem 49:243–254PubMedGoogle Scholar
  3. Boon JM, Smith BD (2002) Chemical control of phospholipid distribution across bilayer membranes. Med Res Rev 22:251–281CrossRefPubMedGoogle Scholar
  4. Bornschein M, Voigt R (1982) Tratado de tecnología farmacéutica. Acribia, ZaragozaGoogle Scholar
  5. Carr A, Vissers M, Domigan N, Winterbourn C (1997) Modification of red cell membrane lipids by hypochlorous acid and hemolysis by preformed lipid clorohydrins. Redox Rep 3:263–271PubMedGoogle Scholar
  6. Cho MJ, Howard LR, Prior RL, Clark JR (2004) Flavonoid glycosides and antioxidant capacity of various blackberry, blueberry and red grape genotypes determined by high-performance liquid chromatography/mass spectrometry. J Sci Food Agric 84:1771–1782CrossRefGoogle Scholar
  7. Devaux PF, Zachowsky A (1994) Maintenance and consequences of membrane phospholipids asymmetry. Chem Phys Lipids 73:107–120CrossRefGoogle Scholar
  8. Dodge JT, Mitchell C, Hanahan DJ (1963) The preparation and chemical characterization of haemoglobin-free ghosts of human erythrocytes. Arch Biochem Biopys 100:119–130CrossRefGoogle Scholar
  9. Foncea R, Carvajal C, Leighton F (2000) Endothelial cell oxidative stress and signal transduction. Biol Res 33:86–96CrossRefGoogle Scholar
  10. Fuenzalida C (2008) Caracterización física-química y botánica de berries de mirtáceas nativas de la cordillera costera de la provincia de Valdivia, Chile. Thesis, Austral University, ChileGoogle Scholar
  11. Gomes S, Somavilla N, Gomes-Bezerra K, do Cuoto S et al (2009) Leaf anatomy of Myrtaceae species: contributions to the taxonomy and phylogeny. Acta Bot Bras 23:223–238Google Scholar
  12. Hawkins C, Davies M (1998) Hypochlorite induces damage to proteins: formation of nitrogen centered radicals from lysine residues and their role in protein fragmentation. Biochem J 332:617–625PubMedCentralCrossRefPubMedGoogle Scholar
  13. Hoffmann A (1991) Flora silvestre de Chile zona araucana, 2nd edn. Claudio Gay, SantiagoGoogle Scholar
  14. Jiménez M, Zambrano M, Aguilar M (2004) Estabilidad de pigmentos en frutas sometidas a tratamiento con energía de microondas. Inf Technol 15:61–66Google Scholar
  15. Lakowicz JR (1999) Principles of fluorescence spectroscopy, 2nd edn. Kluwer/Plenum, New YorkCrossRefGoogle Scholar
  16. Lambert JD, Sang S, Yang CS (2007) Possible controversy over dietary polyphenols: benefits vs risks. Chem Res Toxicol 20:583–585CrossRefPubMedGoogle Scholar
  17. Lim G, Wortis M, Mukhopadhyay R (2002) Stomatocyte–discocyte–echinocyte sequence of the human red blood cell: evidence for the bilayer-couple hypothesis from membrane mechanics. Proc Natl Acad Sci USA 99:16766–16769CrossRefGoogle Scholar
  18. Martínez-Navarrete N, Camacho M, Martínez J (2008) Los compuestos bioactivos de las frutas y sus efectos en la salud. Activ Diet 2:64–68CrossRefGoogle Scholar
  19. Medel F (1979) Prospección de arbustos frutales en el sur de Chile. Agro Sur 7:94–97Google Scholar
  20. Morris JC (1966) The acid ionisation of HOCl from 5 degree to 35 degree. J Phys Chem 70:3798–3805CrossRefGoogle Scholar
  21. Nakagawa K, Kawagoe M, Yoshimura M, Arata A et al (2000) Differential effects of flavonoid quercitin on oxidative damages induced by hydrophilic and lipophilic radical generators in hepatic lysosomal fractions of mice. J Health Sci 46:509–512CrossRefGoogle Scholar
  22. Orellana P (2005) Estudio del efecto estructural del fitocomplejo presente en el infuso de las hojas de Ugni molinae Turcz. (“Murtilla”) sobre la fluidez de membranas celulares. Thesis, Faculty of Pharmacy, University of Concepción, ChileGoogle Scholar
  23. Parasassi T, Gratton E (1995) Membrane lipid domain and dynamics as detected by laurdan fluorescence. J Fluoresc 5:59–69CrossRefPubMedGoogle Scholar
  24. Parasassi T, De Stasio G, d’Ubaldo A, Gratton E (1990) Phase fluctuation in phospolipid membranes revealed by laurdan fluorescence. Biophys J 57:1179–1186PubMedCentralCrossRefPubMedGoogle Scholar
  25. Rozzi S (1984) Las plantas, fuente de salud. Pía Soc. San Pablo, SantiagoGoogle Scholar
  26. Ruiz M (2008) Compuestos fenólicos en frutos de calafate (Berberis microphylla) y comparación de su capacidad antioxidante con otros berries del sur de Chile. Thesis, University of Concepción, ChileGoogle Scholar
  27. Ruiz M, Hermosín-Gutiérrez I, Mardones C, Vergara C et al (2010) Polyphenols and antioxidant activity of Calafate (Berberis microphylla) fruits and other native berries from Southern Chile. J Agric Food Chem 58:6081–6089CrossRefPubMedGoogle Scholar
  28. Scheuermann E, Seguel I, Montenegro A, Bustos R et al (2008) Evolution of aroma compounds of murtilla fruits (Ugni molinae Turcz.) during storage. J Sci Food Agric 88:485–492CrossRefGoogle Scholar
  29. Sheetz MP, Singer SJ (1974) Biological membranes as bilayer couples. A molecular mechanism of drug–erythrocyte induced interactions. Proc Natl Acad Sci USA 71:4457–4461PubMedCentralCrossRefPubMedGoogle Scholar
  30. Suwalsky M (1996) Phospholipid bilayers. In: Salamone JC (ed) Polymeric material encyclopedia. CRC, Boca Raton, pp 5073–5078Google Scholar
  31. Suwalsky M, Orellana P, Avello M, Villena F, Sotomayor CB (2006) Human erythrocytes are affected in vitro by extracts of Ugni molinae leaves. Food Chem Toxicol 44:1393–1398CrossRefPubMedGoogle Scholar
  32. Suwalsky M, Vargas P, Avello M, Villena F, Sotomayor CP (2008) Human erythrocytes are affected in vitro by extracts of Aristotelia chilensis (Maqui) leaves. Int J Pharm 63:85–90CrossRefGoogle Scholar
  33. Suwalsky M, Oyarce K, Avello M, Villena F, Sotomayor CP (2009) Human erythrocytes and molecular models of cell membranes are affected in vitro by Balbisia peduncularis (Amancay) extracts. Chem Biol Interact 179:413–418CrossRefPubMedGoogle Scholar
  34. Torres A, Seguel I, Contreras G, Castro M (1999) Caracterización físico-química de frutos de murta (murtilla) Ugni molinae Turcz. Agric Technol 59:260–270Google Scholar
  35. Vargas-Simón G, Soto-Hernández R, Rodríguez M (2002) Análisis preliminar de antocianinas en fruto de Icaco. Rev Fitoq Mex 25:261–264Google Scholar
  36. Velioglu Y, Mazza G, Gao L, Oomah B (1998) Antioxidant activity and total phenolics in selected fruits, vegetables and grain products. J Agric Food Chem 46:4113–4117CrossRefGoogle Scholar
  37. Vissers M, Winterbourn C (1995) Oxidation of intracellular glutathione after exposure of human red blood cells to hypochlorous acid. Biochem J 307:57–62PubMedCentralCrossRefPubMedGoogle Scholar
  38. Vissers M, Carr A, Chapman A (1998) Comparison of human red cells lysis by hypochlorous and hypobromous acids: insights into the mechanism of lysis. Biochem J 330:131–138PubMedCentralCrossRefPubMedGoogle Scholar
  39. Vives MA, Infante MR, Garcia E, Selve C, Maugras M, Vinardell MP (1999) Erythrocyte hemolysis and shape changes induced by new lysine-derivate surfactants. Chem Biol Interact 118:1–18CrossRefPubMedGoogle Scholar
  40. Zavodnik I, Lapshina E, Zavodnik L, Bartosz G (2001) Hypochlorous acid damages erythrocyte membrane proteins and alters lipid bilayer structure and fluidity. Free Radic Biol Med 30:363–369CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Faculty of Chemical SciencesUniversity of ConcepciónConcepciónChile
  2. 2.Faculty of PharmacyUniversity of ConcepciónConcepciónChile

Personalised recommendations