The Journal of Membrane Biology

, Volume 251, Issue 2, pp 247–261 | Cite as

In Vitro Anti/Pro-oxidant Activities of R. ferruginea Extract and Its Effect on Glioma Cell Viability: Correlation with Phenolic Compound Content and Effects on Membrane Dynamics

  • Desirée Magalhães dos Santos
  • Camila Valesca Jardim Rocha
  • Elita Ferreira da Silveira
  • Marcelo Augusto Germani Marinho
  • Marisa Raquel Rodrigues
  • Nichole Osti Silva
  • Ailton da Silva Ferreira
  • Neusa Fernandes de Moura
  • Gabriel Jorge Sagrera Darelli
  • Elizandra Braganhol
  • Ana Paula Horn
  • Vânia Rodrigues de Lima


Rapanea ferruginea antioxidant and antitumoral properties were not explored before in literature. This study aimed to investigate these biological activities for the R. ferruginea leaf extract and correlate them with its phenolic content and influence in biological membrane dynamics. Thus, in this study, anti/pro-oxidative properties of R. ferruginea leaf extract by in vitro DPPH and TBARS assays, with respect to the free radical reducing potential and to its activity regarding membrane free radical-induced peroxidation, respectively. Furthermore, preliminary tests related to the extract effect on in vitro glioma cell viability were also performed. In parallel, the phenolic content was detected by HPLC–DAD and included syringic and trans-cinnamic acids, quercetrin, catechin, quercetin, and gallic acid. In an attempt to correlate the biological activity of R. ferruginea extract and its effect on membrane dynamics, the molecular interaction between the extract and a liposomal model with natural-sourced phospholipids was investigated. Location and changes in vibrational, rotational, and translational lipid motions, as well as in the phase state of liposomes, induced by R. ferruginea extract, were monitored by Fourier-transform infrared spectroscopy, nuclear magnetic resonance, differential scanning calorimetry, and UV–visible spectroscopy. In its free form, the extract showed promising in vitro antioxidant properties. Free-form extract (at 1000µ g/mL) exposure reduced glioma cell in vitro viability in 40%, as evidenced by MTT tests. Pro-oxidant behavior was observed when the extract was loaded into liposomes. A 70.8% cell viability reduction was achieved with 500 µg/mL of liposome-loaded extract. The compounds of R. ferruginea extract ordered liposome interface and disorder edits a polar region. Phenolic content, as well as membrane interaction and modulation may have an important role in the oxidative and antitumoral activities of the R. ferruginea leaf extract.


R. ferruginea Extract Phenolic compounds Glioma Liposomes 



Soybean asolectin


Dynamic light scattering






Differential scanning calorimetry


Dulbecco’s modified Eagle’s medium


Enthalpy variation


Fetal bovine serum


Free induction decay


Fourier-transform infrared spectroscopy


Horizontal attenuated total reflection–Fourier-transform infrared spectroscopy


3-(4,5-Dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide


Nuclear magnetic resonance


Hydroxyl radical


Standard deviation


Thiobarbituric acid-reactive substances


Sodium 3-(trimethylsilyl)-[2,2,3,3-2H4]-1-propionate


Time delay


Stretching vibration



The authors would like to thank two Brazilian agencies, namely the Conselho de Desenvolvimento Científico e Tecnológico (CNPq) and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for their financial support. Also, we wish to thanks Professor João Cardoso de Lima, Ph.D. (Laboratory of Material Synthesis and Characterization- LSCM) from Federal University of Santa Catarina, for the careful assistance in DSC experiments. This paper is part of Desirée Magalhães dos Santos’ Master’s thesis which was carried out at the Post-graduate Program in Technological and Environmental Chemistry (FURG).

Compliance with Ethical Standards

Conflict of interest

The authors declare that there are no conflicts of interest.


  1. Akbarzadeh A, Rezaei-Sadabady R, Davaran S, Joo SW, Zarghami N, Hanifehpour H, Samiei M, Kouhi K, Nejati-Koshki K (2013) Liposome: classification, preparation, and applications. Nanoscale Res Lett 8:102–111PubMedPubMedCentralCrossRefGoogle Scholar
  2. Andersen ML, Lauridsen RK, Skibsted LH (2003) Optimising the use of phenolic compounds in foods. In: Johnson I, Williamson G (eds) Phytochemical functional foods. Woodhead Publishing Ltd, Cambridge, pp 315–346CrossRefGoogle Scholar
  3. AOAC (Association of Official Analytical Chemist) (1980) Official methods of analysis, 14th edn. AOAC, Washington, DCGoogle Scholar
  4. Azambuja CRL, dos Santos LG, Rodrigues MR, Rodrigues RFM, da Silveira EF, Azambuja JH, Flores AFC, Horn AP, Dora CL, Muccillo-Baisch AL, Braganhol E, da Silva Pinto L, Parize AL, de Lima VR (2015) Physico-chemical characterization of asolectin-genisteinliposomal system: an approach to analyze its in vitro antioxidant potential and effect in glioma cells viability. Chem Phys Lipids 193:24–35PubMedCrossRefGoogle Scholar
  5. Baccarin T, Muceneeki RS, Bresolin TMB, Yunes RA, Malheiros A, Lucinda-Silva RM (2011) Development and validation of an HPLC-PDA method for the determination of myrsinoic acid B in the extracts of Rapanea ferruginea Mez. Talanta 85:1221–1224PubMedCrossRefGoogle Scholar
  6. Bangham AD, Hill MW, Miller NG (1974) Preparation and use of liposomes as models of biological membranes. Methods Membr Biol 1:1–68Google Scholar
  7. Baruah K, Phong HPPD, Norouzitallab P, Defoirdt T, Bossier P (2015) The gnotobiotic brine shrimp (Artemia franciscana) model system reveals that the phenolic compound pyrogallol protects against infection through its prooxidant activity. Free Rad Biol Med 89:593–601PubMedCrossRefGoogle Scholar
  8. Beentje HJ (1994) Kenya trees, shrubs and lianas. National Museums of Kenya, NairobiGoogle Scholar
  9. Bernardi A, Braganhol E, Jäger E, Figueiró F, Edelweiss MI, Pohlmann AR, Guterres SS, Battastini MO (2009) Indomethacin-loaded nanocapsules treatment reduces in vivo glioblastoma growth in a rat glioma model. Cancer Lett 281:53–63PubMedCrossRefGoogle Scholar
  10. Bilge D, Sahin I, Kazanci N, Severcan F (2014) Interactions of tamoxifen with distearoyl phosphatidylcholine multilamellar vesicles: FTIR and DSC studies. Spectrochim Acta A Mol Biomol Spectrosc 130:250–256Google Scholar
  11. Bird RP, Draper AH (1984) Comparative studies on different methods of malondyaldehyde determination. Methods Enzymol 105:295–305Google Scholar
  12. Bohmont C, Aaronson LM, Mann K, Pardini RS (1987) Inhibition of mitochondrial NADH oxidase, succinoxidase, and ATPase by naturally occurring flavonoids. J Nat Prod 50:427–433PubMedCrossRefGoogle Scholar
  13. Brito AF, Ribeiro M, Abrantes AM, Mamede AC, Laranjo M, Casalta-Lopes JE, Gonçalves AC, Sarmento-Ribeiro AB, Tralhão JG, Botelho MF (2016) New approach for treatment of primary liver tumors: the role of quercetin. Nutr Cancer 4:1–17Google Scholar
  14. Casal HL, Mantsch HH (1984) Polymorphic phase behaviour of phospholipid membranes studied by infrared spectroscopy. Biochim Biophys Acta 779:381–401Google Scholar
  15. Casal HL, Cameron DG, Smith ICP, Mantsch HH (1980) Acholeplasma laidlawii membranes: a Fourier transform infrared study of the influence of protein on lipid organization and dynamics. Biochemistry 19:444–451PubMedCrossRefGoogle Scholar
  16. Castelli F, Trombetta D, Tomaiano A, Bonina F, Romeo G, Uccella N, Saija A (1997) Dipalmitoylphosphatidylcholine/linoleic acid mixed unilamellar vesicles as model membranes for studies on novel free-radical scavengers. JPM 37:135–141Google Scholar
  17. Caturla N, Vera-Samper E, Villalaín J, Mateo CR, Micol V (2003) The relationship between the antioxidant and the antibacterial properties of galloylated catechins and the structure of phospholipid model membranes. Free Rad Biol Med 34:648–662PubMedCrossRefGoogle Scholar
  18. Chan ST, Yang NC, Huang CS, Liao JW, Yeh SL (2013) Quercetin enhances the antitumor activity of trichostatin A through upregulation of p53 protein expression in vitro and in vivo. PLoS ONE 8:e54255PubMedPubMedCentralCrossRefGoogle Scholar
  19. Chang HY, Ho YL, Sheu MJ, Lin YH, Tseng MC, Wu SH, Huang GJ, Chang YS (2007) Antioxidant and free radical scavenging activities of Phellinus merrillii extracts. Bot Stud 48:407–417Google Scholar
  20. Chen C, Tripp CP (2008) An infrared spectroscopic based method to measure membrane permeance in liposomes. Biochim Biophys Acta 1778:2266–2272PubMedCrossRefGoogle Scholar
  21. Chen C, Zhou J, Ji C (2010) Quercetin: a potential drug to reverse multidrug resistance. Life Sci 87:333–338PubMedCrossRefGoogle Scholar
  22. Cheng Z, Li Y, Chang W (2003) Kinetic deoxyribose degradation assay and its application in assessing the antioxidant activities of phenolic compounds in a Fenton- type reaction system. Anal Chim Acta 478:129–137CrossRefGoogle Scholar
  23. Cholbi MR, Pays M, Alcaraz MJ (1991) Inhibitory effects of phenolic compounds on carbon tetrachloride-induced microsomal lipid peroxidation. Experientia 47:195–199PubMedCrossRefGoogle Scholar
  24. Cikman O, Soylemez O, Ozkan OF, Kiraz HA, Sayar I, Ademoglu S, Taysi S, Karaayvaz M (2015) Antioxidant activity of syringic acid prevents oxidative stress in L-arginine-induced acute pancreatitis: an experimental study on rats. Int Surg 100:891–896PubMedPubMedCentralCrossRefGoogle Scholar
  25. Cincin ZB, Unlu M, Kiran B, Bireller ES, Baran Y, Cakmakoglu B (2014) Molecular mechanisms of quercetrin-induced apoptosis in non-small cell lung cancer. Arch Medic Res 45:445–454CrossRefGoogle Scholar
  26. Conklin KA (2000) Dietary antioxidants during cancer chemotherapy: impact on chemotherapeutic effectiveness and development of side effects. Nutr Cancer 37:1–18PubMedCrossRefGoogle Scholar
  27. Cruz AB, Kazmierczak K, Gazoni VF, Monteiro ER, Fronza LM, Martins P, Yunes RA, Bürger C, Tomio TA, Freitas RA, Malheiros A (2013) Bio- guided isolation of antimicrobial compounds from Rapanea ferruginea and its cytotoxic and genotoxic potential. J Med Plant Res 7:1323–1329Google Scholar
  28. Cury TAC, Yoneda JS, Zuliani JP, Soares AM, Stabeli RG, Calderon LA, Ciancaglini P (2015) Cinnamic acid derived compounds loaded into liposomes: antileishmanial activity, production standardisation and characterisation. J Microencapsul 32:467–477PubMedCrossRefGoogle Scholar
  29. De Lima VR, Caro MSB, Munford ML, Desbat B, Dufourc E, Pasa AA, Creczynski-Pasa TB (2010) Influence of melatonin on the order of phosphatidylcholine-based membranes. J Pineal Res 49:169–175PubMedGoogle Scholar
  30. De Lima VR, Morfim MP, Teixeira A, Creczynski-Pasa TB (2004) Relationship between the action of reactive oxygen and nitrogen species on bilayer membranes and antioxidants. Chem Phys Lipids 132:197–208PubMedCrossRefGoogle Scholar
  31. De Vargas FS, Almeida PDO, de Boleti APA, Pereira MM, de Souza TP, de Vasconcellos MC, Nunez CV, Pohlit AM, Lima ES (2016) Antioxidant activity and peroxidase inhibition of Amazonian plants extracts traditionally used as anti-inflammatory. BMC Comp Altern Med 16:83–91CrossRefGoogle Scholar
  32. Dhar P, Ghosh S, Bhattacharyya DK (1999) Dietary effects of conjugated octadecatrienoic fatty acid (9 cis, 11 trans, 13 trans) levels on blood lipids and nonenzymatic in vitro lipid peroxidation in rats. Lipids 34:109–114PubMedCrossRefGoogle Scholar
  33. Dufourc EJ (2006) Solid state NMR in biomembranes. In: Larijani B, Rosser CA, Woscholski R (eds) Chemical biology: applications and techniques. Wiley, LondonGoogle Scholar
  34. Ekmekcioglu C, Feyertag J, Marktl W (1998) Cinnamic acid inhibits proliferation and modulates brush border membrane enzyme activities in Caco-2 cells. Cancer Lett 128:137–144PubMedCrossRefGoogle Scholar
  35. Elkholi R, Renault TT, Serasinghe MN, Chipuk JE (2014) Putting the pieces together: how is the mitochondrial pathway of apoptosis regulated in cancer and chemotherapy? Cancer Metab 2:16–31PubMedPubMedCentralCrossRefGoogle Scholar
  36. Elsayed MMA, Cevc G (2011) Turbidity spectroscopy for characterization of submicroscopic drug carriers, such as nanoparticles and lipid vesicles: size determination. Pharm Res 28:2204–2222PubMedCrossRefGoogle Scholar
  37. Erlejman AG, Verstraeten SV, Fraga CJ, Oteiza PI (2004) The interaction of flavonoids with membranes: potential determinant of flavonoid antioxidant effects. Free Radic Res 38:1311–1320PubMedCrossRefGoogle Scholar
  38. Fagali N, Catalá A (2009) Fe2+ and Fe3+ initiated peroxidation of sonicated and non-sonicated liposomes made of retinal lipids in different aqueous media. Chem Phys Lipids 159:88–94PubMedCrossRefGoogle Scholar
  39. Farhan M, Yar Khan H, Oves M, Al-Harrasi A, Rehmani N, Arif H, Hadi SM, Ahmad A (2016) Cancer therapy by catechins involves redox cycling of copper ions and generation of reactive oxygen species. Toxins 8:37–53PubMedPubMedCentralCrossRefGoogle Scholar
  40. Feigenson GW, Chan SI (1974) Nuclear magnetic relaxation behavior of lecithin multilayers. J Am Chem Soc 96:1312–1319PubMedCrossRefGoogle Scholar
  41. Fraceto LF, Spisnic A, Schreiere S, de Paula E (2005) Differential effects of uncharged aminoamide local anesthetics on phospholipid bilayers, as monitored by 1H NMR measurements. Biophys Chem 115:11–18Google Scholar
  42. Fukumoto LR, Mazza G (2000) Assessing antioxidant and prooxidant activities of phenolic componds. J Agric Food Chem 48:3597–3604PubMedCrossRefGoogle Scholar
  43. Galati G, O’Brien P (2004) Potential toxicity of flavonoids and other dietaryphenolics: significance for their chemopreventive and anticancer properties. Free Radic Biol Med 37:287–303PubMedCrossRefGoogle Scholar
  44. Gutierrez RP, Baez EG (2014) Evaluation of antidiabetic, antioxidant and antiglycating activities of the Eysenhardtia polystachya. Pharmacogn Mag 10:404–418CrossRefGoogle Scholar
  45. Hadi SM, Bhat SH, Azmi AS, Hanif S, Shamim U, Ullah MF (2007) Oxidative breakage of cellular DNA by plant polyphenols: a putative mechanism for anticancer properties. Semin Cancer Biol 17:370–376PubMedCrossRefGoogle Scholar
  46. Halliwell B, Gutteridge JMC (2000) Free radicals in biology and medicine. Oxford University Press, New YorkGoogle Scholar
  47. Halliwell B, Hoult JR, Blake DR (1988) Oxidants, inflammation and anti-inflammatory drugs. FASEB J 2:2867–2873PubMedCrossRefGoogle Scholar
  48. Hattori T, Andoh T, Sakai N, Yamada H, Kameyama Y, Ohki K, Nozawa Y (1987) Membrane phospholipid composition and membrane fluidity of human brain tumour: a spin label study. Neurol Res 9:38–43PubMedCrossRefGoogle Scholar
  49. Herec M, Islamov A, Kuklin A, Gagós M, Gruszecki WI (2007) Effect of antibiotic amphotericin B on structural and dynamic properties of lipid membranes formed with egg yolk phosphatidylcholine. Chem Phys Lipids 147:78–86PubMedCrossRefGoogle Scholar
  50. Hess S, Padoani C, Scorteganha LC, Holzmann I, Malheiros A, Yunes RA, Monache FD, Souza MMD (2010) Assessment of mechanisms involved in antinociception caused by myrsinoic acid B. Biol Pharm Bull 33:209–215PubMedCrossRefGoogle Scholar
  51. Hope MJ, Bally MB, Mayer LD, Janoff AS, Cullis PR (1986) Generation of multilamellar and unilamellar phospholipid vesicles. Chem Phys Lipids 40:89–107CrossRefGoogle Scholar
  52. Hu C, Zhang Y, Kitts DD (2000) Evaluation of antioxidant and prooxidant activities of bamboo Phyllostachysnigra var. Henonis leaves extract in vitro. J Agric Food Chem 48:3170–3176PubMedCrossRefGoogle Scholar
  53. Ignea C, Dorobant C, Mintoff CP, Branza-Nichita N, Ladomery MR, Kefalas P, Chedea VS (2013) Modulation of the antioxidant/pro-oxidant balance, cytotoxicity and antiviral actions of grape seed extracts. Food Chem 141:3967–3976PubMedCrossRefGoogle Scholar
  54. Inoue M, Suzuki R, Sakaguchi N, Li Z, Takeda T, Ogihara Y, Jiang BY, Chen Y (1995) Selective induction of cell death in cancer cells by gallic acid. Biol Pharmacol Bull 18:1526–1530CrossRefGoogle Scholar
  55. Jo HY, Kim Y, Park HW, Moon HE, Bae S, Kim J, Paek SH (2015) The unreability of MTT assay in the cytotoxic test of primary cultured glioblastoma cells. Exp Neurobiol 24:235–245PubMedPubMedCentralCrossRefGoogle Scholar
  56. Kello M, Drutovic D, Pilatova MB, Tischlerova V, Perjesi P, Mojzis J (2016) Chalcone derivatives cause accumulation of colon cancer cells in the G2/M phase and induce apoptosis. Life Sci 150:32–38PubMedCrossRefGoogle Scholar
  57. Khan AQ, Khan R, Rehman MU, Lateef A, Tahir M, Ali F, Sultana S (2012) Soy isoflavones (daidzein & genistein) inhibit 12-O-tetradecanoylphorbol-13-acetate (TPA)-induced cutaneous inflammation via modulation of COX-2 and NF-kB in Swiss albino mice. Toxicology 302:266–274PubMedCrossRefGoogle Scholar
  58. Kim JH, Campbell BC, Mahoney N, Chan KL, May GS (2006) Targeting antioxidative signal transduction and stress response system: control of pathogenic Aspergillus with phenolics that inhibit mitochondrial function. J Appl Microbiol 101:181–189PubMedCrossRefGoogle Scholar
  59. Kokwaro JO (1993) Medicinal plants of East Africa. Kenya Literature Bureau, NairobiGoogle Scholar
  60. Koppenol WH (1990) Oxyradical reactions: from bond-dissociation energies to reduction potentials. FEBS Lett 264:165–167PubMedCrossRefGoogle Scholar
  61. Koynova R, Caffrey M (1998) Phases and phase transitions of the phosphatidylcholines. Biochim Biophys Acta 1376:91–145Google Scholar
  62. Kresheck GD, Kale K, Vallone MD (1980) Calorimetric studies of the interaction between asolectin vesicles and surfactants. J Colloid Interface Sci 73:460–466CrossRefGoogle Scholar
  63. Krilov D, Kosovic M, Serec K (2014) Spectroscopic studies of alpha tocopherol interaction with a model liposome and its influence on oxidation dynamics. Spectrochim Acta A 129:588–593CrossRefGoogle Scholar
  64. Lambert JD, Elias RJ (2010) The antioxidant and pro-oxidant activities of green tea polyphenols: a role in cancer prevention. Arch Biochem Biophys 501:65–72PubMedPubMedCentralCrossRefGoogle Scholar
  65. Lamson DW, Brignall MS (2000) Antioxidant and cancer III: quercetin. Altern Med Rev 5:196–208PubMedGoogle Scholar
  66. Liu L, Hudgins WR, Shack S, Yin MQ, Samid D (1995) Cinnamic acid: a natural product with potential use in cancer intervention. Int J Cancer 62:345–350PubMedCrossRefGoogle Scholar
  67. Liu L, Mu L-M, Yan Y, Wu J-S, Hu Y-J, Bu Y-Z, Zhang J-Y, Liu R, Li X-Q, Lu W-L (2017) The use of functional pirubicin liposomes to induce programmed death in refractory breast cancer. Int J Nanomed 12:4163–4176CrossRefGoogle Scholar
  68. López-García F, Micol V, Villalaín J, Gómez-Fernández JC (1993) Infrared spectroscopic study of the interaction of diacylglycerol with phosphatidylserine in the presence of calcium. Biochim Biophys Acta 1169:264–274PubMedCrossRefGoogle Scholar
  69. Lorenzi H (1992) Árvores brasileiras. Nova Odessa, São PauloGoogle Scholar
  70. Lynch DV, Steponkus PL (1989) Lyotropic phase behavior of unsaturated phosphatidylcholine species: relevance to the mechanism of plasma membrane destabilization and freezing injury. Biochim Biophys Acta 984:267–272Google Scholar
  71. Madsen HL, Bertelsen G (1995) Spices as antioxidants. Trends Food Sci Technol 6:271–277CrossRefGoogle Scholar
  72. Mahboob M, Rahman MF, Crover P (2005) Serum lipid peroxidation and antioxidant enzyme levels in male and female diabetic patients. Singapore Med J 46:322–324PubMedGoogle Scholar
  73. Maher EA, Furnari FB, Bachoo RM, Rowitch DH, Louis DN, Cavenee WK, DePinho RA (2001) Malignant glioma: genetics and biology of a grave matter. Genes Dev 15:1311–1333PubMedCrossRefGoogle Scholar
  74. Makabe H, Miyazaki S, Kamo T, Hirota M (2003) Myrsinoic acid E, an anti-inflammatory compound from Myrsine seguinii. Biosci Biotechnol Biochem 67:2038–2041PubMedCrossRefGoogle Scholar
  75. Mamat N, Jamal JA, Jantan I, Husain K (2014) Xanthine oxidase inhibitory and DPPH radical scavenging activities of some Primulaceae species. Sains Malaysiana 43:1827–1833CrossRefGoogle Scholar
  76. Manrique-Moreno M, Garidel P, Suwalsky M, Howe J, Bradenburg K (2009) The membrane-activity of ibuprofen, diclofenac, and naproxen: a physico-chemical study with lecithin phospholipids. Biochim Biophys Acta 1788:1296–1303PubMedCrossRefGoogle Scholar
  77. Manrique-Moreno M, Howe J, Suwalsky M, Garidel P, Brandenburg K (2010) Physicochemical interaction study of non-steroidal anti-inflammatory drugs with dimyristoylphosphatidylethanolamine liposomes. Lett Drug Des Discov 7:50–56CrossRefGoogle Scholar
  78. Mason WP (2008) Emerging drugs for malignant glioma. Expert Opin Emerg Drugs 13:81–94PubMedCrossRefGoogle Scholar
  79. McDonald S, Prenzler PD, Antolovich M, Robards K (2001) Phenolic content and antioxidant activity of olive extracts. Food Chem 73:73–84CrossRefGoogle Scholar
  80. Milardi D, Sciacca MFM, Pappalardo M, Grasso DM, La Rosa C (2011) The role of aromatic side-chains in amyloid growth and membrane interaction of the islet amyloid polypeptide fragment LANFLVH. Eur Biophys J 40:1–12PubMedCrossRefGoogle Scholar
  81. Mochizuki M, Yamazaki S, Kano K, Ikeda T (2002) Kinetic analysis and mechanistic aspects of autoxidation of catechins. BiochimBiophys Acta 1569:35–44Google Scholar
  82. Mosa RA, Lazarus GG, Gwala PE, Oyedeji AO, Opoku AR (2011) In vitro anti-platelet aggregation, antioxidant and cytotoxic activity of extracts of some Zulu medicinal plants. J Nat Prod 4:136–146Google Scholar
  83. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63PubMedCrossRefGoogle Scholar
  84. Murzakhmetova M, Moldakarimov S, Tancheva L, Abarova S, Serkedjieva J (2008) Antioxidant and prooxidant properties of a polyphenol-rich extract from Geranium sanguineum L. in vitro and in vivo. Phytother Res 22:746–751PubMedCrossRefGoogle Scholar
  85. Muthukumaran J, Srinivasan S, Venkatesan RS, Ramachandran V, Muruganathan U (2013) Syringic acid, a novel natural phenolic acid, normalizes hyperglycemia with special reference to glycoprotein components in experimental diabetic rats. J Acute Dis 2:304–309CrossRefGoogle Scholar
  86. Njogu MK, Matasyoh JC, Kibor AC (2015) Rapanea melanophloeos leaves extracts against Schistosoma mansonimiracidia. Research 2:1303–1308Google Scholar
  87. Ohkawa H, Oshishi N, Yagi K (1979) Assay for lipid peroxides in animal-tissues by thiobarbituricacid reaction. Anal Biochem 95:351–358PubMedCrossRefGoogle Scholar
  88. Ohtani K, Maw S, Hostettmann K (1993) Molluscicidal and antifungal triterpenoid saponins from Rapanea melanophloeos leaves. Phytochemistry 33:83–86CrossRefGoogle Scholar
  89. Parejo I, Viladomat F, Bastida J, Rosas-Romero A, Saavedra G, Murcia MA, Jiménez MA, Codina C (2003) Investigation of Bolivian plant extracts for their radical scavenging activity and antioxidant activity. Life Sci 73:1667–1681PubMedCrossRefGoogle Scholar
  90. Ponou BK, Teponno RB, Ricciutelli M, Quassinti L, Bramucci M, Lupidi G, Barboni L, Tapondjou LA (2010) Dimeric antioxidant and cytotoxic triterpenoid saponins from Terminali aivorensis A. Chev Phytochem 71:2108–2115CrossRefGoogle Scholar
  91. Ramos S (2008) Cancer chemoprevention and chemotherapy: dietary polyphenols and signalling pathways. Mol Nutr Food Res 52:507–526PubMedCrossRefGoogle Scholar
  92. Ramanan PN, Rao MN (1987) Antimicrobial activity of cinnamic acid derivates. Ind J Exp Biol 25:42–43Google Scholar
  93. Rigas B, Sun Y (2008) Induction of oxidative stress as a mechanism of action of chemopreventive agents against cancer. Br J Canc 98:1157–1160Google Scholar
  94. Rodríguez-Pérez C, Quirantes-Piné R, Uberos J, Jiménez-Sánchez C, Peña A, Segura-Carretero A (2016) Antibacterial activity of isolated phenolic compounds from cranberry (Vaccinium macrocarpon) against Escherichia coli. Food Funct 7:1564–1573PubMedCrossRefGoogle Scholar
  95. Sagrista ML, Garcia AF, Africa de Madariaga M, Mora M (2002) Antioxidant and pro-oxidant effect of the thiolic compounds N-acetyl-l-cysteine and glutathione against free radical-induced lipid peroxidation. Free Radic Res 36:329–340PubMedCrossRefGoogle Scholar
  96. Sakagami H, Satoh K (1997) Pro-oxidant action of two antioxidants: ascorbic acid and gallic acid. Anticancer Res 17:221–224PubMedGoogle Scholar
  97. Salganik RI, Albright CD, Rodgers J, Kim J, Zeisel SH, Sivashinskiy MS, Dyke TAV (2000) Dietary antioxidant depletion: enhancement of tumor apoptosis and inhibition of brain tumor growth in transgenic mice. Carcinogenesis 21:909–914PubMedCrossRefGoogle Scholar
  98. Šamec D, Durgo K, Grúz J, Kremer D, Kosalec I, Piliac-Žegarac J, Salopek-Sondi B (2014) Genetic and phytochemical variability of six Teucri marduini L. populations and their antioxidant/prooxidant behavior examined by biochemical, macromolecule- and cell-based approaches. Food Chem 186:298–305PubMedCrossRefGoogle Scholar
  99. Saura-Calixto FD, Pérez-Jiménez J, Sampaio CG, Morais SM, Brito ES, Alves RE, Rufino MSM (2007) Determinação da atividade antioxidante total em frutas pela captura do radical livre DPPH e ABTS – Metodologia Científica. EMBRAPA, FortalezaGoogle Scholar
  100. Sousa RS, Nogueira AOM, Gobel Marques V, Clementin RM, de Lima VR (2013) Effects of α-eleostearic acid on asolectin liposomes dynamics: relevance to its antioxidant activity. Bioorg Chem 51:8–15Google Scholar
  101. Severcan F, Sahin I, Kazanci N (2005) Melatonin strongly interacts with zwitterionic model membranes: evidence from Fourier transform infrared spectroscopy and differential scanning calorimetry. Biochim Biophys Acta 1668:215–222PubMedCrossRefGoogle Scholar
  102. Sholfield CR (1981) Composition of soybean lecithin. JAOCS 58:889–892CrossRefGoogle Scholar
  103. Shalaby S, Horwitz BA (2015) Plant phenolic compounds and oxidative stress: integrated signals in fungal–plant interactions. Curr Genet. 61:347–357PubMedCrossRefGoogle Scholar
  104. Scordino M, Sabatino L, Traulo P, Gargano M, Panto V, Gagliano G (2011) HPLC–PDA/ESI–MS/MS detection of polymethoxylated flavones in highly degraded citrus juice: a quality control case study. Eur Food Res Technol 232:275–280CrossRefGoogle Scholar
  105. Silveira EF, Chassot JM, Teixeira FC, Azambuja JH, Debom G, Beira FT, Del Pino FAB, Lourenço A, Horn AP, Cruz L, Spanevello RM, Braganhol E (2013) Ketoprofen-loaded polymeric nanocapsules selectively inhibit cancer cell growth in vitro and in preclinical model of glioblastoma multiforme. Invest New Drugs 31:1424–1435PubMedCrossRefGoogle Scholar
  106. Sinha R, Joshi A, Joshi UJ, Srivastava S, Govil G (2014) Localization and interaction of hydroxyflavones with lipid bilayer model membranes: a study using DSC and multinuclear NMR. Eur J Med Chem 80:285–294PubMedCrossRefGoogle Scholar
  107. Surh YJ (2008) NF-kappa B and Nrf2 as potential chemopreventive targets of some anti-inflammatory and antioxidative phytonutrients with antiinflamatory and antioxidative activities. Asia Pac J Clin Nutr 17:269–272PubMedGoogle Scholar
  108. Symons AM, Dowling EJ (1987) Free radicals, oxidant stress and drug action. London, Richelieu Press, pp 99–120Google Scholar
  109. Tawata S, Taira S, Kobamoto N, Zhu J, Ishihara M, Toyama S (1996) Synthesis and antifungal activity of cinnamic acid esters. Biosci Biotechnol Biochem 60:909–910PubMedCrossRefGoogle Scholar
  110. The Angiosperm Phylogeny Group (2009) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants. Bot J Linn Soc 161:105–121CrossRefGoogle Scholar
  111. Tirosh O, Kohen R, Katzhendler J, Alon A, Barenholz Y (1997) Oxidative stress effect on the integrity of lipid bilayers is modulated by cholesterol level of bilayers. Chem Phys Lipids 87:17–22PubMedCrossRefGoogle Scholar
  112. Toyran N, Severcan F (2003) Competitive effect of vitamin D2 and Ca2+ on phospholipid model membranes: an FTIR study. J Mol Struct 123:165–176Google Scholar
  113. Ulrich AS, Sami M, Watts A (1994) Hydration of DOPC bilayers by differential scanning calorimetry. Biochim Biophys Acta 1191:225–230Google Scholar
  114. Wagner A, Vorauer-Uhl K (2011) Liposome technology for industrial purposes. J Drug Deliv. PubMedCrossRefGoogle Scholar
  115. Wang G, Zhang J, Liu L, Sharma S, Dong Q (2012) Quercetin potentiates doxorubicin mediated antitumor effects against liver cancer throughp53/Bcl-xl. PLoS ONE 7:e51764PubMedPubMedCentralCrossRefGoogle Scholar
  116. Wei X, Chen D, Yi Y, Qi H, Gao X, Fang H, Gu Q, Wang L, Gu L (2012)Syringic acid extracted from Herba dendrobii prevents diabetic cataract pathogenesis by inhibiting aldose reductase activity.Evid-Based Comp Altern Med 2012:1–13Google Scholar
  117. Wilms LC, Kleinjans JC, Moonen EJ, Briedé JJ (2008) Discriminative protection against hydroxyl and superoxide anion radicals by quercetin in human leucocytes in vitro. Toxicol In Vitro 22:301–307PubMedCrossRefGoogle Scholar
  118. Yu J, Cheng Y, Xie L, Zhang R (1999) Effects of genistein and daidzein on membrane characteristics of HTC cells. Nutr Cancer 33:100–104PubMedCrossRefGoogle Scholar
  119. Zhao L, Feng S, Kocherginsky N, Kostetski I (2007) DSC and EPR investigations on effects of cholesterol component on molecular interactions between paclitaxel and phospholipid within lipid bilayer membrane. Int J Pham 338:258–266Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Desirée Magalhães dos Santos
    • 1
  • Camila Valesca Jardim Rocha
    • 1
  • Elita Ferreira da Silveira
    • 2
  • Marcelo Augusto Germani Marinho
    • 2
  • Marisa Raquel Rodrigues
    • 1
  • Nichole Osti Silva
    • 1
  • Ailton da Silva Ferreira
    • 3
    • 4
  • Neusa Fernandes de Moura
    • 1
  • Gabriel Jorge Sagrera Darelli
    • 5
  • Elizandra Braganhol
    • 6
  • Ana Paula Horn
    • 2
  • Vânia Rodrigues de Lima
    • 1
  1. 1.Programa de Pós-Graduação em Química Tecnológica e Ambiental, Escola de Química e AlimentosUniversidade Federal do Rio GrandeRio GrandeBrazil
  2. 2.Programa de Pós Graduação em Ciências Fisiológicas, Instituto de Ciências BiológicasUniversidade Federal do Rio GrandeRio GrandeBrazil
  3. 3.Programa de Pós-Graduação em Ciência e Engenharia de MateriaisUniversidade Federal de Santa CatarinaFlorianópolisBrazil
  4. 4.Instituto Federal de Educação, Ciência e Tecnologia CatarinenseBlumenauBrazil
  5. 5.Facultad de QuímicaUniversidad de la RepublicaMontevideoUruguay
  6. 6.Programa de Pós-Graduação em Ciências da SaúdeUniversidade Federal de Ciências da Saúde de Porto AlegrePorto AlegreBrazil

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