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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

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Abstract

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.

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Abbreviations

ASO:

Soybean asolectin

DLS:

Dynamic light scattering

DMPC:

Dimyristoylphosphatidylcholine

DPPC:

Dipalmitoylphosphatidylcholine

DSC:

Differential scanning calorimetry

DMEM:

Dulbecco’s modified Eagle’s medium

∆H:

Enthalpy variation

FBS:

Fetal bovine serum

FID:

Free induction decay

FTIR:

Fourier-transform infrared spectroscopy

HATR–FTIR:

Horizontal attenuated total reflection–Fourier-transform infrared spectroscopy

MTT:

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

NMR:

Nuclear magnetic resonance

∙OH:

Hydroxyl radical

S.D.:

Standard deviation

TBARS:

Thiobarbituric acid-reactive substances

TSP:

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

τ:

Time delay

ν:

Stretching vibration

References

  • 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 8:102–111

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 315–346

    Chapter  Google Scholar 

  • AOAC (Association of Official Analytical Chemist) (1980) Official methods of analysis, 14th edn. AOAC, Washington, DC

    Google Scholar 

  • 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 193:24–35

    Article  PubMed  CAS  Google Scholar 

  • 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 85:1221–1224

    Article  CAS  PubMed  Google Scholar 

  • Bangham AD, Hill MW, Miller NG (1974) Preparation and use of liposomes as models of biological membranes. Methods Membr Biol 1:1–68

    CAS  Google Scholar 

  • 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 89:593–601

    Article  CAS  PubMed  Google Scholar 

  • Beentje HJ (1994) Kenya trees, shrubs and lianas. National Museums of Kenya, Nairobi

    Google Scholar 

  • 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 281:53–63

    Article  CAS  PubMed  Google Scholar 

  • 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 130:250–256

  • Bird RP, Draper AH (1984) Comparative studies on different methods of malondyaldehyde determination. Methods Enzymol 105:295–305

    Google Scholar 

  • Bohmont C, Aaronson LM, Mann K, Pardini RS (1987) Inhibition of mitochondrial NADH oxidase, succinoxidase, and ATPase by naturally occurring flavonoids. J Nat Prod 50:427–433

    Article  CAS  PubMed  Google Scholar 

  • 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 4:1–17

    Google Scholar 

  • Casal HL, Mantsch HH (1984) Polymorphic phase behaviour of phospholipid membranes studied by infrared spectroscopy. Biochim Biophys Acta 779:381–401

  • 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 19:444–451

    Article  CAS  PubMed  Google Scholar 

  • 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 37:135–141

    CAS  Google Scholar 

  • 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 34:648–662

    Article  CAS  PubMed  Google Scholar 

  • 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:e54255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 48:407–417

    CAS  Google Scholar 

  • Chen C, Tripp CP (2008) An infrared spectroscopic based method to measure membrane permeance in liposomes. Biochim Biophys Acta 1778:2266–2272

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Zhou J, Ji C (2010) Quercetin: a potential drug to reverse multidrug resistance. Life Sci 87:333–338

    Article  CAS  PubMed  Google Scholar 

  • 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 478:129–137

    Article  CAS  Google Scholar 

  • Cholbi MR, Pays M, Alcaraz MJ (1991) Inhibitory effects of phenolic compounds on carbon tetrachloride-induced microsomal lipid peroxidation. Experientia 47:195–199

    Article  CAS  PubMed  Google Scholar 

  • 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 100:891–896

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 45:445–454

    Article  CAS  Google Scholar 

  • Conklin KA (2000) Dietary antioxidants during cancer chemotherapy: impact on chemotherapeutic effectiveness and development of side effects. Nutr Cancer 37:1–18

    Article  CAS  PubMed  Google Scholar 

  • 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 7:1323–1329

    CAS  Google Scholar 

  • 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 32:467–477

    Article  CAS  PubMed  Google Scholar 

  • 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 49:169–175

    PubMed  Google Scholar 

  • 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 132:197–208

    Article  PubMed  CAS  Google Scholar 

  • 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 16:83–91

    Article  CAS  Google Scholar 

  • 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 34:109–114

    Article  CAS  PubMed  Google Scholar 

  • Dufourc EJ (2006) Solid state NMR in biomembranes. In: Larijani B, Rosser CA, Woscholski R (eds) Chemical biology: applications and techniques. Wiley, London

    Google Scholar 

  • Ekmekcioglu C, Feyertag J, Marktl W (1998) Cinnamic acid inhibits proliferation and modulates brush border membrane enzyme activities in Caco-2 cells. Cancer Lett 128:137–144

    Article  CAS  PubMed  Google Scholar 

  • 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 2:16–31

    Article  PubMed  PubMed Central  Google Scholar 

  • Elsayed MMA, Cevc G (2011) Turbidity spectroscopy for characterization of submicroscopic drug carriers, such as nanoparticles and lipid vesicles: size determination. Pharm Res 28:2204–2222

    Article  CAS  PubMed  Google Scholar 

  • Erlejman AG, Verstraeten SV, Fraga CJ, Oteiza PI (2004) The interaction of flavonoids with membranes: potential determinant of flavonoid antioxidant effects. Free Radic Res 38:1311–1320

    Article  CAS  PubMed  Google Scholar 

  • 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 159:88–94

    Article  CAS  PubMed  Google Scholar 

  • 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 8:37–53

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Feigenson GW, Chan SI (1974) Nuclear magnetic relaxation behavior of lecithin multilayers. J Am Chem Soc 96:1312–1319

    Article  CAS  PubMed  Google Scholar 

  • 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 115:11–18

  • Fukumoto LR, Mazza G (2000) Assessing antioxidant and prooxidant activities of phenolic componds. J Agric Food Chem 48:3597–3604

    Article  CAS  PubMed  Google Scholar 

  • Galati G, O’Brien P (2004) Potential toxicity of flavonoids and other dietaryphenolics: significance for their chemopreventive and anticancer properties. Free Radic Biol Med 37:287–303

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez RP, Baez EG (2014) Evaluation of antidiabetic, antioxidant and antiglycating activities of the Eysenhardtia polystachya. Pharmacogn Mag 10:404–418

    Article  Google Scholar 

  • 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 17:370–376

    Article  CAS  PubMed  Google Scholar 

  • Halliwell B, Gutteridge JMC (2000) Free radicals in biology and medicine. Oxford University Press, New York

    Google Scholar 

  • Halliwell B, Hoult JR, Blake DR (1988) Oxidants, inflammation and anti-inflammatory drugs. FASEB J 2:2867–2873

    Article  CAS  PubMed  Google Scholar 

  • 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 9:38–43

    Article  CAS  PubMed  Google Scholar 

  • 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 147:78–86

    Article  CAS  PubMed  Google Scholar 

  • 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 33:209–215

    Article  CAS  PubMed  Google Scholar 

  • Hope MJ, Bally MB, Mayer LD, Janoff AS, Cullis PR (1986) Generation of multilamellar and unilamellar phospholipid vesicles. Chem Phys Lipids 40:89–107

    Article  Google Scholar 

  • 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 48:3170–3176

    Article  CAS  PubMed  Google Scholar 

  • 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 141:3967–3976

    Article  CAS  PubMed  Google Scholar 

  • 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 18:1526–1530

    Article  CAS  Google Scholar 

  • 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 24:235–245

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 150:32–38

    Article  CAS  PubMed  Google Scholar 

  • 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 302:266–274

    Article  CAS  PubMed  Google Scholar 

  • 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 101:181–189

    Article  CAS  PubMed  Google Scholar 

  • Kokwaro JO (1993) Medicinal plants of East Africa. Kenya Literature Bureau, Nairobi

    Google Scholar 

  • Koppenol WH (1990) Oxyradical reactions: from bond-dissociation energies to reduction potentials. FEBS Lett 264:165–167

    Article  CAS  PubMed  Google Scholar 

  • Koynova R, Caffrey M (1998) Phases and phase transitions of the phosphatidylcholines. Biochim Biophys Acta 1376:91–145

  • Kresheck GD, Kale K, Vallone MD (1980) Calorimetric studies of the interaction between asolectin vesicles and surfactants. J Colloid Interface Sci 73:460–466

    Article  CAS  Google Scholar 

  • 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 129:588–593

    Article  CAS  Google Scholar 

  • Lambert JD, Elias RJ (2010) The antioxidant and pro-oxidant activities of green tea polyphenols: a role in cancer prevention. Arch Biochem Biophys 501:65–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamson DW, Brignall MS (2000) Antioxidant and cancer III: quercetin. Altern Med Rev 5:196–208

    CAS  PubMed  Google Scholar 

  • 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 62:345–350

    Article  CAS  PubMed  Google Scholar 

  • 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 12:4163–4176

    Article  Google Scholar 

  • 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 1169:264–274

    Article  PubMed  Google Scholar 

  • Lorenzi H (1992) Árvores brasileiras. Nova Odessa, São Paulo

    Google Scholar 

  • 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 984:267–272

  • Madsen HL, Bertelsen G (1995) Spices as antioxidants. Trends Food Sci Technol 6:271–277

    Article  CAS  Google Scholar 

  • Mahboob M, Rahman MF, Crover P (2005) Serum lipid peroxidation and antioxidant enzyme levels in male and female diabetic patients. Singapore Med J 46:322–324

    CAS  PubMed  Google Scholar 

  • 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 15:1311–1333

    Article  CAS  PubMed  Google Scholar 

  • Makabe H, Miyazaki S, Kamo T, Hirota M (2003) Myrsinoic acid E, an anti-inflammatory compound from Myrsine seguinii. Biosci Biotechnol Biochem 67:2038–2041

    Article  CAS  PubMed  Google Scholar 

  • Mamat N, Jamal JA, Jantan I, Husain K (2014) Xanthine oxidase inhibitory and DPPH radical scavenging activities of some Primulaceae species. Sains Malaysiana 43:1827–1833

    Article  CAS  Google Scholar 

  • 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 1788:1296–1303

    Article  PubMed  CAS  Google Scholar 

  • 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 7:50–56

    Article  CAS  Google Scholar 

  • Mason WP (2008) Emerging drugs for malignant glioma. Expert Opin Emerg Drugs 13:81–94

    Article  CAS  PubMed  Google Scholar 

  • McDonald S, Prenzler PD, Antolovich M, Robards K (2001) Phenolic content and antioxidant activity of olive extracts. Food Chem 73:73–84

    Article  CAS  Google Scholar 

  • 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 40:1–12

    Article  CAS  PubMed  Google Scholar 

  • Mochizuki M, Yamazaki S, Kano K, Ikeda T (2002) Kinetic analysis and mechanistic aspects of autoxidation of catechins. BiochimBiophys Acta 1569:35–44

    CAS  Google Scholar 

  • 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 4:136–146

  • Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63

    Article  CAS  PubMed  Google Scholar 

  • 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 22:746–751

    Article  PubMed  Google Scholar 

  • 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 2:304–309

    Article  Google Scholar 

  • Njogu MK, Matasyoh JC, Kibor AC (2015) Rapanea melanophloeos leaves extracts against Schistosoma mansonimiracidia. Research 2:1303–1308

    Google Scholar 

  • Ohkawa H, Oshishi N, Yagi K (1979) Assay for lipid peroxides in animal-tissues by thiobarbituricacid reaction. Anal Biochem 95:351–358

    Article  CAS  PubMed  Google Scholar 

  • Ohtani K, Maw S, Hostettmann K (1993) Molluscicidal and antifungal triterpenoid saponins from Rapanea melanophloeos leaves. Phytochemistry 33:83–86

    Article  CAS  Google Scholar 

  • 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 73:1667–1681

    Article  CAS  PubMed  Google Scholar 

  • 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 71:2108–2115

    Article  CAS  Google Scholar 

  • Ramos S (2008) Cancer chemoprevention and chemotherapy: dietary polyphenols and signalling pathways. Mol Nutr Food Res 52:507–526

    Article  CAS  PubMed  Google Scholar 

  • Ramanan PN, Rao MN (1987) Antimicrobial activity of cinnamic acid derivates. Ind J Exp Biol 25:42–43

    CAS  Google Scholar 

  • Rigas B, Sun Y (2008) Induction of oxidative stress as a mechanism of action of chemopreventive agents against cancer. Br J Canc 98:1157–1160

  • 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 7:1564–1573

    Article  PubMed  CAS  Google Scholar 

  • 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 36:329–340

    Article  CAS  PubMed  Google Scholar 

  • Sakagami H, Satoh K (1997) Pro-oxidant action of two antioxidants: ascorbic acid and gallic acid. Anticancer Res 17:221–224

    CAS  PubMed  Google Scholar 

  • 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 21:909–914

    Article  CAS  PubMed  Google Scholar 

  • 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 186:298–305

    Article  PubMed  CAS  Google Scholar 

  • 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, Fortaleza

  • 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 51:8–15

  • 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 1668:215–222

    Article  CAS  PubMed  Google Scholar 

  • Sholfield CR (1981) Composition of soybean lecithin. JAOCS 58:889–892

    Article  Google Scholar 

  • Shalaby S, Horwitz BA (2015) Plant phenolic compounds and oxidative stress: integrated signals in fungal–plant interactions. Curr Genet. 61:347–357

    Article  CAS  PubMed  Google Scholar 

  • 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 232:275–280

    Article  CAS  Google Scholar 

  • 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 31:1424–1435

    Article  PubMed  CAS  Google Scholar 

  • 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 80:285–294

    Article  CAS  PubMed  Google Scholar 

  • 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 17:269–272

    CAS  PubMed  Google Scholar 

  • Symons AM, Dowling EJ (1987) Free radicals, oxidant stress and drug action. London, Richelieu Press, pp 99–120

    Google Scholar 

  • Tawata S, Taira S, Kobamoto N, Zhu J, Ishihara M, Toyama S (1996) Synthesis and antifungal activity of cinnamic acid esters. Biosci Biotechnol Biochem 60:909–910

    Article  CAS  PubMed  Google Scholar 

  • 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 161:105–121

    Article  Google Scholar 

  • 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 87:17–22

    Article  CAS  PubMed  Google Scholar 

  • Toyran N, Severcan F (2003) Competitive effect of vitamin D2 and Ca2+ on phospholipid model membranes: an FTIR study. J Mol Struct 123:165–176

    CAS  Google Scholar 

  • Ulrich AS, Sami M, Watts A (1994) Hydration of DOPC bilayers by differential scanning calorimetry. Biochim Biophys Acta 1191:225–230

  • Wagner A, Vorauer-Uhl K (2011) Liposome technology for industrial purposes. J Drug Deliv. https://doi.org/10.1155/2011/591325

    Article  PubMed  Google Scholar 

  • 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:e51764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 2012:1–13

    Google Scholar 

  • 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 22:301–307

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Cheng Y, Xie L, Zhang R (1999) Effects of genistein and daidzein on membrane characteristics of HTC cells. Nutr Cancer 33:100–104

    Article  CAS  PubMed  Google Scholar 

  • 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 338:258–266

Download references

Acknowledgements

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).

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Authors and Affiliations

  1. Programa de Pós-Graduação em Química Tecnológica e Ambiental, Escola de Química e Alimentos, Universidade Federal do Rio Grande, Av. Itália, km 8, Campus Carreiros, Rio Grande, RS, 96203-900, Brazil

    Desirée Magalhães dos Santos, Camila Valesca Jardim Rocha, Marisa Raquel Rodrigues, Nichole Osti Silva, Neusa Fernandes de Moura & Vânia Rodrigues de Lima

  2. Programa de Pós Graduação em Ciências Fisiológicas, Instituto de Ciências Biológicas, Universidade Federal do Rio Grande, Av. Itália, km 8, Campus Carreiros, Rio Grande, RS, 96203-900, Brazil

    Elita Ferreira da Silveira, Marcelo Augusto Germani Marinho & Ana Paula Horn

  3. Programa de Pós-Graduação em Ciência e Engenharia de Materiais, Universidade Federal de Santa Catarina, Trindade, Florianópolis, SC, 88040-900, Brazil

    Ailton da Silva Ferreira

  4. Instituto Federal de Educação, Ciência e Tecnologia Catarinense, Campi Abelardo Luz, Blumenau, SC, 89051-000, Brazil

    Ailton da Silva Ferreira

  5. Facultad de Química, Universidad de la Republica, Av. Gral. Flores 2124, C.P. 11800, Montevideo, Uruguay

    Gabriel Jorge Sagrera Darelli

  6. Programa de Pós-Graduação em Ciências da Saúde, Universidade Federal de Ciências da Saúde de Porto Alegre, Porto Alegre, RS, 90050-170, Brazil

    Elizandra Braganhol

Authors
  1. Desirée Magalhães dos Santos
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  2. Camila Valesca Jardim Rocha
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  3. Elita Ferreira da Silveira
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  4. Marcelo Augusto Germani Marinho
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  5. Marisa Raquel Rodrigues
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  6. Nichole Osti Silva
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  7. Ailton da Silva Ferreira
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  8. Neusa Fernandes de Moura
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  9. Gabriel Jorge Sagrera Darelli
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  10. Elizandra Braganhol
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  11. Ana Paula Horn
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  12. Vânia Rodrigues de Lima
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Corresponding author

Correspondence to Vânia Rodrigues de Lima.

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dos Santos, D.M., Rocha, C.V.J., da Silveira, E.F. et al. 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. J Membrane Biol 251, 247–261 (2018). https://doi.org/10.1007/s00232-018-0017-z

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  • DOI: https://doi.org/10.1007/s00232-018-0017-z

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