Abstract

As soon as the role of Reactive Oxygen Species (ROS) in so-called civilization diseases, which include non-infectious chronic diseases such as cancer, diabetes or high blood pressure has been discovered, and the possibility of employing antioxidants as a remedy for these diseases have been proposed, scientists developed a broad spectrum of methods to determine antioxidant activity of pure chemicals and plant extracts, as well as dietary supplements. Most of these methods are based on simple redox reactions between antioxidant and ROS (for example ABTS, DPPH, or FRAP tests). However, chemical methods of assessing antioxidant activity are rarely biologically relevant. They do not mirror the real effect of antioxidants in living organisms, because they are used in non-physiological conditions of temperature and pH; neither they take metabolism nor intracellular transport under consideration. The perfect model for assessment of antioxidant activity in living organisms would be human or animal model, but such determinations are very complicated and often ambiguous. The current best alternative to chemical and human tests are assays employing cell culture models being less expensive than human tests, yet still reflecting biological systems more convincingly than chemical assays. Cellular antioxidant assays are performed under physiological pH and temperature, but most importantly, they take metabolism and intracellular transport under consideration. In this review, we present cellular tests used to determine antioxidant activity that are based on luminescence and fluorescence methods.

References

• 1. Aranda A., Sequedo L., Tolosa L., Quintas G., Burello E., Castell J.V., Gombau L.: Dichloro-dihydro-fluorescein diacetate (DCFH-DA) assay: a quantitative method for oxidative stress assessment of nanoparticle- -treated cells. Toxicol. In Vitro, 2013; 27: 954-963
  Google Scholar
• 2. Bartosz G.: Druga twarz tlenu. Wydawnictwo Naukowe PWN, Warszawa 2009
  Google Scholar
• 3. Bender S., Grabiano S.: Evaluation of the antioxidant activity of foods in human cells. Integrated study of biologically active antioxidants from Camellia sinensis. Nutrafoods, 2015; 14: 79-85
  Google Scholar
• 4. Bindokas V.P., Jordán J., Lee C.C., Miller R.J.: Superoxide production in rat hippocampal neurons: selective imaging with hydroethidine. J. Neurosci., 1996; 16: 1324-1336
  Google Scholar
• 5. Bucana C., Saiki I., Nayar R.: Uptake and accumulation of the vital dye hydroethidine in neoplastic cells. J. Histochem. Cytochem., 1986; 34: 1109-1115
  Google Scholar
• 6. Buettner G.R.: Moving free radical and redox biology ahead in the next decade(s). Free Rad. Biol. Med., 2015; 78: 236-238
  Google Scholar
• 7. Buettner G.R., Jurkiewicz B.A.: Ascorbate free radical as a marker of oxidative stress: an EPR study. Free Radic. Biol. Med., 1993; 14: 49-55
  Google Scholar
• 8. Chen X., Zou L.Q., Niu J., Liu W., Peng S.F., Liu C.M.: The stability, sustained release and cellular antioxidant activity of curcumin nanoliposomes. Molecules, 2015; 20: 14293-14311
  Google Scholar
• 9. Dmitriev R.I., Zhdanov A.V., Jasionek G., Papkovsky D.B.: Assessment of cellular oxygen gradients with a panel of phosphorescent oxygen- -sensitive probes. Anal. Chem., 2012; 84: 2930-2938
  Google Scholar
• 10. Esipova T.V., Karagodov A., Miller J., Wilson D.F., Busch T.M., Vinogradov S.A.: Two new «protected» oxyphors for biological oximetry: properties and application in tumor imaging. Anal. Chem., 2011: 83: 8756-8765
  Google Scholar
• 11. Forman H.J., Augusto O., Brigelius-Flohe R., Dennery P.A., Kalyanaraman B., Ischiropoulos H., Mann G.E., Radi R., Roberts L.J.2nd, Vina J., Davies K.J.: Even free radicals should follow some rules: a guide to free radical research terminology and methodology. Free Radic. Biol. Med., 2015; 78: 233-235
  Google Scholar
• 12. Freeman B.A., Crapo J.D.: Biology of disease: free radicals and tissue injury. Lab. Invest., 1982; 47: 412-426
  Google Scholar
• 13. Gomes A., Fernandes E., Lima J.L.: Fluorescence probes used for detection of reactive oxygen species. J. Biochem. Biophys. Methods, 2005; 65; 45-80
  Google Scholar
• 14. Gouda M., Moustafa A., Hussein L., Hamza M.: Three week dietary intervention using apricots, pomegranate juice or/and fermented sour sobya and impact on biomarkers of antioxidative activity, oxidative stress and erythrocytic glutathione transferase activity among adults. Nutr. J., 2016; 15: 52
  Google Scholar
• 15. Halliwell B., Whiteman M.: Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? Br. J. Pharmacol., 2004; 142: 231-255
  Google Scholar
• 16. Hernandez L., Grasa L., Fagundes D.S., Gonzalo S., Arruebo M.P., Plaza M.A., Murillo M.D.: Role of potassium channels in rabbit intestinal motility disorders induced by 2,2’-azobis (2-amidinopropane) dihydrochloride (AAPH). J. Physiol. Pharmacol., 2010; 61: 279-286
  Google Scholar
• 17. Honzel D., Carter S.G., Redman K.A., Schauss A.G., Endres J.R., Jensen G.S.: Comparison of chemical and cell-based antioxidant methods for evaluation of foods and natural products: generating multifaceted data by parallel testing using erythrocytes and polymorphonuclear cells. J. Agric. Food Chem., 2008; 56: 8319-8325
  Google Scholar
• 18. Jakubowski W., Bartosz G.: Estimation of oxidative stress in Saccharomyces cerevisae with fluorescent probes. Int. J. Biochem. Cell Biol., 1997; 29: 1297-1301
  Google Scholar
• 19. Kalyanaraman B., Darley-Usmar V., Davies K.J., Dennery P.A., Forman H.J., Grisham M.B., Mann G.E., Moore K., Roberts L.J.2nd, Ischiropoulos H.: Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic. Biol. Med., 2012; 52: 1-6
  Google Scholar
• 20. Kanofsky J.R.: Singlet oxygen production by lactoperoxidase. J. Biol. Chem., 1983; 258: 5991-5993
  Google Scholar
• 21. Karadag A., Ozcelik B., Saner S.: Review of methods to determine antioxidant capacities. Food Anal. Methods, 2009; 2: 41
  Google Scholar
• 22. Klaude M., Eriksson S., Nygren J., Ahnström G.: The comet assay: mechanisms and technical considerations. Mutat. Res., 1996; 363: 89-96
  Google Scholar
• 23. Komatsu H., Yoshihara K., Yamada H., Kimura Y., Son A., Nishimoto S., Tanabe K.: Ruthenium complexes with hydrophobic ligands that are key factors for the optical imaging of physiological hypoxia. Chemistry, 2013; 19: 1971-1977
  Google Scholar
• 24. Koshiishi I., Tsuchida K., Takajo T., Komatsu M.: Radical scavenger can scavenge lipid allyl radicals complexed with lipoxygenase at lower oxygen content. Biochem. J., 2006; 395: 303-309
  Google Scholar
• 25. Koshiishi I., Tsuchida K., Takajo T., Komatsu M.: Quantification of lipid alkyl radicals trapped with nitroxyl radical via HPLC with postcolumn thermal decomposition. J. Lipid Res., 2005; 46: 2506-2513
  Google Scholar
• 26. Li N., Ragheb K., Lawler G., Sturgis J., Rajwa B., Melendez J.A., Robinson J.P.: Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J. Biol. Chem., 2003; 278: 8516-8525
  Google Scholar
• 27. Lobo V., Patil A., Phatak A., Chandra N.: Free radicals, antioxidants and functional foods: Impact on human health. Pharmacogn. Rev., 2010; 4: 118-126
  Google Scholar
• 28. Meng L., Wu Y., Yi T.: A ratiometric fluorescent probe for the detection of hydroxyl radicals in living cells. Chem. Commun., 2014; 50: 4843-4845
  Google Scholar
• 29. Mills E.M., Takeda K., Yu Z.X., Ferrans V., Katagiri Y., Jiang H., Lavigne M.C., Leto T.L., Guroff G.: Nerve growth factor treatment prevents the increase in superoxide produced by epidermal growth factor in PC12 cells. J. Biol. Chem., 1998; 273: 22165-22168
  Google Scholar
• 30. Niki E.: Assessment of antioxidant capacity in vitro and in vivo. Free Radic. Biol. Med., 2010; 49: 503-515
  Google Scholar
• 31. Okimoto Y., Watanabe A., Nikia E., Yamashita T., Noguchi N.: A novel fluorescent probe diphenyl-1-pyrenylphosphine to follow lipid peroxidation in cell membranes. FEBS Lett., 2000; 474: 137-140
  Google Scholar
• 32. Piasek A., Bartoszek A., Namieśnik J.: Substancje pochodzenia roślinnego przeciwdziałające kardiotoksyczności towarzyszącej chemioterapii nowotworów. Postępy Hig. Med. Dośw., 2009; 63: 142-158
  Google Scholar
• 33. Pryor W.A., Godber S.S.: Noninvasive measures of oxidative stress status in humans. Free Radic. Biol. Med., 1991; 10: 177-184
  Google Scholar
• 34. Rahman T., Hosen I., Islam M.M., Shekhar H.U.: Oxidative stress and human health. J. Adv. Biosci. Biotechnol., 2012; 3: 997-1019
  Google Scholar
• 35. Ray P.D, Huang B.W., Tsuji Y.: Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell. Signal., 2012; 24: 981-990
  Google Scholar
• 36. Reszka K.J., Wagner B.A., Burns C.P., Britigan B.E.: Effects of peroxidase substrates on the Amplex red/peroxidase assay: antioxidant properties of anthracyclines. Anal. Biochem., 2005; 342: 327-337
  Google Scholar
• 37. Rivera A., Maxwell S.A.: The p53-induced gene-6 (proline oxidase) mediates apoptosis through a calcineurin-dependent pathway. J. Biol. Chem., 2005; 280: 29346-29354
  Google Scholar
• 38. Robinson K.M., Janes M..S, Pehar M., Monette J.S., Ross M.F., Hagen T.M., Murphy M.P., Beckman J.S.: Selective fluorescent imaging of superoxide in vivo using ethidium-based probes. Proc. Natl. Acad. Sci. USA, 2006; 103: 15038-15043
  Google Scholar
• 39. Rothe G., Valet G.: Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 2’,7’-dichlorofluorescin. J. Leukoc. Biol., 1990; 47: 440-448
  Google Scholar
• 40. Schieber M., Chandel N.S.: ROS function in redox signaling and oxidative stress. Curr. Biol., 2014; 24: R453-R462
  Google Scholar
• 41. Setsukinai K., Urano Y., Kakinuma K., Majima H.J., Nagano T.: Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species. J. Biol. Chem., 2003; 278: 3170-3175
  Google Scholar
• 42. Sies H.: Oxidative stress: a concept in redox biology and medicine. Redox Biol., 2015; 4: 180-183
  Google Scholar
• 43. Sundaresan M., Yu Z.X., Ferrans V.J., Irani K., Finkel T.: Requirement for generation of H2 O2 for platelet-derived growth factor signal transduction. Science, 1995; 270: 296-299
  Google Scholar
• 44. Towne V., Will M., Oswald B., Zhao Q.: Complexities in horseradish peroxidase-catalyzed oxidation of dihydroxyphenoxazine derivatives: appropriate ranges for pH values and hydrogen peroxide concentrations in quantitative analysis. Anal. Biochem., 2004; 334: 290-296
  Google Scholar
• 45. Votyakova T.V., Reynolds I.J.: Detection of hydrogen peroxide with Amplex Red: interference by NADH and reduced glutathione auto-oxidation. Arch. Biochem. Biophys., 2004; 431: 138-144
  Google Scholar
• 46. Wang L.F., Chen J.Y., Xie H.H., Ju X.R., Liu R.H.: Phytochemical profiles and antioxidant activity of Adlay varieties. J. Agric. Food Chem., 2013; 61: 5103-5113
  Google Scholar
• 47. Wardman P.: Fluorescent and luminescent probes for measurement of oxidative and nitrosative species in cells and tissues: progress, pitfalls, and prospects. Free Radic. Biol. Med., 2007; 43: 995-1022
  Google Scholar
• 48. Wen L., Guo X., Liu R.H., You L., Abbasi A.M., Fu X.: Phenolic contents and cellular antioxidant activity of Chinese hawthorn ‘‘Crataegus pinnatifida’’. Food Chem., 2015; 186: 54-62
  Google Scholar
• 49. Wen Y., Liu K., Yang H., Li Y., Lan H., Liu Y., Zhang X., Yi T.: A highly sensitive ratiometric fluorescent probe for the detection of cytoplasmic and nuclear hydrogen peroxide. Anal. Chem., 2014; 86: 9970-9976
  Google Scholar
• 50. Wen Y., Liu K., Yang H., Liu Y., Chen L., Liu Z., Huang C., Yi T.: Mitochondria-directed fluorescent probe for the detection of hydrogen peroxide near mitochondrial DNA. Anal. Chem. 2015; 87: 10579-10584
  Google Scholar
• 51. Werber J., Wang Y.J., Milligan M., Li X., Ji J.A.: Analysis of 2,2′-azobis (2-amidinopropane) dihydrochloride degradation and hydrolysis in aqueous solutions. J. Pharm. Sci., 2011; 100: 3307-3315
  Google Scholar
• 52. Wolfe K.L., Liu R.H.: Cellular antioxidant activity (CAA) assay for assessing antioxidants, foods, and dietary supplements. J. Agric. Food Chem., 2007; 55: 8896-8907
  Google Scholar
• 53. Yazdani M.: Concerns in the application of fluorescent probes DCDHF-DA, DHR 123 and DHE to measure reactive oxygen species in vitro. Toxicol. In Vitro, 2015; 30: 578-582
  Google Scholar
• 54. Ye Z.W., Zhang J., Townsend D.M., Tew K.D.: Oxidative stress, redox regulation and diseases of cellular differentiation. Biochim. Biophys. Acta, 2015; 1850: 1607-1621
  Google Scholar
• 55. Yoshida Y., Itoh N., Saito Y., Hayakawa M., Niki E.: Application of water-soluble radical initiator, 2,2’-azobis-[2-(2-imidazolin-2-yl)propane] dihydrochloride, to a study of oxidative stress. Free Radic. Res., 2004; 38: 375-384
  Google Scholar
• 56. Zhao H., Joseph J., Fales H.M., Sokoloski E.A., Levine R.L., Vasquez- -Vivar J., Kalyanaraman B.: Detection and characterization of the product of hydroethidine and intracellular superoxide by HPLC and limitations of fluorescence. Proc. Natl. Acad. Sci. USA, 2005; 102: 5727-5732
  Google Scholar
• 57. Zhou M., Diwu Z., Panchuk-Voloshina N., Haugland R.P.: A stable nonfluorescent derivative of resorufin for the fluorometric determination of trace hydrogen peroxide: applications in detecting the activity of phagocyte NADPH oxidase and other oxidases. Anal. Biochem., 1997; 253: 162-168
  Google Scholar
• 58. Zuo L., Zhou T., Pannell B.K., Ziegler A.C., Best T.M.: Biological and physiological role of reactive oxygen species – the good, the bad and the ugly. Acta Physiol., 2015; 214: 329-348
  Google Scholar

Full text