Lipoperoxyl Radical Scavenging and Antioxidative Effects of Red Beet Pigments

Chapter

Abstract

Aerobic life is characterized by a steady formation of reactive oxygen species and free radicals, which is almost entirely counteracted by endogenous primary and secondary antioxidant systems. Maintenance of these systems is then imperative to ensure a continuous defense to cells and to avoid conditions known as oxidative stress. Apart from antioxidant vitamins, many compounds from the plant kingdom are now considered very helpful to maintain a proper cell redox balance. Among them, betalain pigments have received recent attention. Betanin (betanidin-5-O-β glucoside) is the main betacyanin from red beet. Redox potential, ability to interact with lipid structures and bioavailability in humans make this molecule a potential natural antioxidant with protective effects in vivo. This review summarizes the peroxyl radical-scavenging activity of the molecule and of its aglycone betanidin, as observed in a few chemical or biological models.

Keywords

Phenol Dopamine Glutathione Adduct Nitrite 

References

  1. Allegra, M., P.G. Furtmuller, W. Jantschko, M. Zederbauer, L. Tesoriere, M.A. Livrea, and C. Obinger. 2005. Mechanism of interaction of betanin and indicaxanthin with human myeloperoxidase and hypochlorous acid. Biochemical and Biophysical Research Communications 332: 837–844.CrossRefGoogle Scholar
  2. Allegra, M., L. Tesoriere, and M.A. Livrea. 2007. Betanin inhibits the myeloperoxidase/nitrite-induced oxidation of human low density lipoproteins. Free Radical Research 41: 335–341.CrossRefGoogle Scholar
  3. Avila, D.V., K.U. Ingold, J. Lusztyk, W.H. Green, and D.R. Procopio. 1995. Dramatic solvent effects on the absolute rate constants for abstraction of the hydroxylic hydrogen atom from tert-butyl hydroperoxide and phenol by the cumyloxyl radical. The role of hydrogen bonding. Journal of the American Chemical Society 117: 2929–2930.CrossRefGoogle Scholar
  4. Barclay, L.R.C. 1993. Model biomembranes: Quantitative studies of peroxidation, antioxidant action, partitioning, and oxidative stress. Canadian Journal of Chemistry 71: 1–16.CrossRefGoogle Scholar
  5. Barclay, L.R.C., K.A. Baskin, K.A. Dakin, S.J. Locke, and M.R. Vinqvist. 1990. The antioxidant activities of phenolic antioxidants in free radical peroxidation of phospholipid membranes. Canadian Journal of Chemistry 68: 2258–2269.CrossRefGoogle Scholar
  6. Barclay, L.R.C., C.E. Edwards, and M.R. Vinqvist. 1999. Media effects on antioxidant activities of phenols and cathecols. Journal of the American Chemical Society 121: 6226–6231.CrossRefGoogle Scholar
  7. Buettner, G. 1993. The pecking order of free radicals and antioxidants: Lipid peroxidation, α-tocopherol, and ascorbate. Archives of Biochemistry and Biophysics 300: 535–543.CrossRefGoogle Scholar
  8. Burner, U., P.G. Furtmuller, A.J. Kettle, W.H. Koppenol, and C. Obinger. 2000. Mechanism of reaction of myeloperoxidase with nitrite. Journal of Biological Chemistry 275: 20597–20601.CrossRefGoogle Scholar
  9. Burton, G.W., and K.U. Ingold. 1981. Autoxidation of biological molecules. 1. The antioxidant activity of vitamin E and related chain-breaking phenolic antioxidants in vitro. Journal of the American Chemical Society 103: 6472–6477.CrossRefGoogle Scholar
  10. Butera, D., L. Tesoriere, F. Di Gaudio, A. Bongiorno, M. Allegra, A.M. Pintaudi, R. Kohen, and M.A. Livrea. 2002. Antioxidant activities of sicilian prickly pear (Opuntia ficus indica) fruit extracts and reducing properties of its betalains: Betanin and indicaxantin. Journal of Agricultural and Food Chemistry 50: 6895–6901.CrossRefGoogle Scholar
  11. Byun, J., D.M. Mueller, J.S. Fabjan, and J.W. Heinecke. 1999. Nitrogen dioxide radical generated by the myeloperoxidase-hydrogen peroxide-nitrite system promotes lipid peroxidation of low density lipoprotein. FEBS Letters 455: 243–246.CrossRefGoogle Scholar
  12. Cao, G., E. Sofic, and R.L. Prior. 1997. Antioxidant and prooxidant behavior of flavonoids: Structure-activity relationships. Free Radical Biology & Medicine 22: 749–760.CrossRefGoogle Scholar
  13. Czapski, J., K. Mikolajczyk, and M. Kaczmarek. 2009. Relationship between antioxidant capacity of red beet juice and contents of its betalain pigments. Polish Journal of Food and Nutrition Sciences 59: 119–122.Google Scholar
  14. Daugherty, A., J.L. Dunn, D.L. Rateri, and J.W. Heinecke. 1994. Myeloperoxidase, a catalyst for lipoprotein oxidation, is expressed in human atherosclerotic lesions. The Journal of Clinical Investigation 94: 437–444.CrossRefGoogle Scholar
  15. Dröge, W. 2002. Free radicals in the physiological control of cell function. Physiological Reviews 82: 47–95.Google Scholar
  16. Echtay, K.S., T.C. Esteves, J.L. Pakai, M.B. Jekabson, A.J. Lambert, M. Portero-Otin, R. Pamplona, A.J. Vidal-Puig, S. Wang, S.J. Roebuck, and M.D. Brand. 2003. A signalling role for 4-hydroxy-2 nonenal in regulation of mitochondrial uncoupling. EMBO Journal 22: 4103–4110.CrossRefGoogle Scholar
  17. Eiserich, J.P., M. Hristova, C.E. Cross, A.D. Jones, B.A. Freeman, B. Halliwell, and A. van der Vliet. 1998. Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils. Nature 391: 393–397.CrossRefGoogle Scholar
  18. Escribano, J., M.A. Pedreno, F. Garcia-Carmona, and R. Munoz. 1998. Characterization of the antiradical activity of betalains from Beta vulgaris L. roots. Phytochemical Analysis 9: 124–127.CrossRefGoogle Scholar
  19. Esterbauer, H., J. Gebicki, H. Puhl, and G. Jürgens. 1992. The role of lipid peroxidation and antioxidants in oxidative modification of LDL. Free Radical Biology & Medicine 13: 341–390.CrossRefGoogle Scholar
  20. Foti, M., and G. Ruberto. 2001. Kinetic solvent effects on phenolic antioxidants determined by spectrophotometric measurements. Journal of Agricultural and Food Chemistry 49: 342–348.CrossRefGoogle Scholar
  21. Frank, T., F.C. Stintzing, R. Carle, I. Bitsch, D. Quaas, G. Strass, R. Bitsch, and M. Netzel. 2005. Urinary pharmacokinetics of betalains following consumption of red beet juice in healthy humans. Pharmacological Research 52: 290–297.CrossRefGoogle Scholar
  22. Fukuzawa, K. 2008. Dynamics of lipid peroxidation and antioxidation of α-tocopherol in membranes. Journal of Nutritional Science and Vitaminology 54: 273–285.CrossRefGoogle Scholar
  23. Gandia-Herrero, F., J.A. Escribano, and F. Garcia-Carmona. 2007. Characterization of the activity of tyrosinase on betanidin. Journal of Agricultural and Food Chemistry 55: 1546–1551.CrossRefGoogle Scholar
  24. Gandia-Herrero, F., J.A. Escribano, and F. Garcia-Carmona. 2010. Structural implications on color, fluorescence, and antiradical activity in betalains. Planta 232: 449–460.CrossRefGoogle Scholar
  25. Giles, G.I. 2006. The redox regulation of thiol dependent signaling pathways in cancer. Current Pharmaceutical Design 12: 4427–4443.CrossRefGoogle Scholar
  26. Giorgio, M., M. Trinei, E. Migliaccio, and P.G. Pelicci. 2007. Hydrogen peroxide: A metabolic by-product or a common mediator of ageing signals? Nature Reviews. Molecular Cell Biology 8: 722–728.CrossRefGoogle Scholar
  27. Gliszczynska-Swiglo, A., H. Szymusiak, and P. Malinowska. 2006. Betanin, the main pigment of red beet: Molecular origin of its exceptionally high free radical-scavenging activity. Food Additives and Contaminants 23: 1079–1087.CrossRefGoogle Scholar
  28. Halliwell, B., J. Rafter, and A. Jenner. 2005. Health promotion by flavonoids, tocopherols, tocotrienols, and other phenols: Direct or indirect effects? Antioxidant or not? American Journal of Clinical Nutrition 81: 268S–276S.Google Scholar
  29. Hancock, J.T. 2009. The role of redox mechanisms in cell signaling. Molecular Biotechnology 43: 162–166.CrossRefGoogle Scholar
  30. Heinecke, J.W. 1998. Oxidants and antioxidants in the pathogenesis of atherosclerosis: Implications for the oxidized low density lipoprotein hypothesis. Atherosclerosis 141: 1–15.CrossRefGoogle Scholar
  31. Heller, J.I., J.R. Crowley, S.L. Hazen, D.M. Salvay, P. Wagner, S. Pennathur, and J.W. Heinecke. 2000. p-Hydroxyphenylacetaldehyde, an aldehyde generated by myeloperoxidase, modifies phospholipid amino groups of low density lipoprotein in human atherosclerotic intima. Journal of Biological Chemistry 275: 9957–9962.CrossRefGoogle Scholar
  32. Herbach, K.M., F.C. Stintzing, and R. Carle. 2006. Betalain stability and degradation. Structural and chromatic aspects. Journal of Food Science 71: R41–R50.CrossRefGoogle Scholar
  33. Ingold, K. 1969. Peroxy radicals. Accounts of Chemical Research 2: 1–9.CrossRefGoogle Scholar
  34. Jia, Z.-S., B. Zhou, L. Yang, L.-M. Wu, and Z.-L. Liu. 1998. Antioxidant synergism of tea polyphenols and α-tocopherol against free radical induced peroxidation of linoleic acid in solution. Journal of the Chemical Society, Perkin Transactions 2: 911–915.Google Scholar
  35. Kamlet, M.J., and R.W. Taft. 1976. The solvatochromic comparison method. I. The beta-scale of solvent hydrogen-bond acceptor (HBA) basicities. Journal of the American Chemical Society 98: 377–383.CrossRefGoogle Scholar
  36. Kanner, J., S. Harel, and R. Granit. 2001. Betalains—A new class of dietary cationized antioxidants. Journal of Agricultural and Food Chemistry 49: 5178–5185.CrossRefGoogle Scholar
  37. Klebanoff, S.J. 1980. Oxygen metabolism and the toxic properties of phagocytes. Annals of Internal Medicine 93: 480–489.Google Scholar
  38. Kostyuk, V.A., T. Kraemer, H. Sies, and T. Schewe. 2003. Myeloperoxidase/nitrite-mediated lipid peroxidation of low-density lipoprotein as modulated by flavonoids. FEBS Letters 537: 146–150.CrossRefGoogle Scholar
  39. Kushi, L.H., E.B. Lenart, and W.C. Willett. 1995. Health implication of Mediterranean diets in light of contemporary knowledge. 1. Plant foods and dairy products. American Journal of Clinical Nutrition 61(suppl 6): 1407S–1415S.Google Scholar
  40. Lee, M.Y., and K.K. Griendling. 2008. Redox signaling, vascular function, and hypertension. Antioxidants & Redox Signaling 10: 1045–1059.CrossRefGoogle Scholar
  41. Leitinger, N. 2005. Oxidised phospholipids as triggers of inflammation in atherosclerosis. Molecular Nutrition & Food Research 49: 1063–1071.CrossRefGoogle Scholar
  42. Leonarduzzi, G., A. Scavazza, F. Biasi, E. Chiarpotto, S. Camandola, S. Vogel, L. Dargel, and G. Poli. 1997. The lipid peroxidation end product 4-hydroxy-2,3 nonenal upregulates transforming growth factor beta1 expression in the macrophage lineage: A link between oxidative injury and fibrosclerosis. The FASEB Journal 11: 851–857.Google Scholar
  43. Leonarduzzi, G., B. Sottero, and G. Poli. 2010. Targeting tissue oxidative damage by means of cell signaling modulators: The antioxidant concept revisited. Pharmacology and Therapeutics 128: 336–374.CrossRefGoogle Scholar
  44. Lin, R.I.-S. 1995. Phytochemical and antioxidants. In Functional foods, ed. I.E. Goldberg, 393–441. New York: Chapman and Hall.Google Scholar
  45. Livrea, M.A., and L. Tesoriere. 2004. Antioxidant activities of prickly pear (Opuntia ficus indica) fruit and its betalains. In Herbal and traditional medicines, ed. L. Packer, C.N. Ong, and B. Halliwell, 537–556. New York: Marcel Dekker.Google Scholar
  46. Ma, Q. 2010. Transcriptional responses to oxidative stress: Pathological and toxicological implications. Pharmacology and Therapeutics 125: 376–393.CrossRefGoogle Scholar
  47. Martin, K.R., and J.C. Barrett. 2002. Reactive oxygen species as double-edged swords in cellular processes: Low-dose cell signaling versus high-dose toxicity. Human and Experimental Toxicology 21: 71–75.CrossRefGoogle Scholar
  48. Matsuzawa, A., and H. Ichijo. 2008. Redox control of cell fate by MAP kinase: Physiological roles of ASK1-MAP kinase pathway in stress signaling. Biochimica et Biophysica Acta 1780: 1325–1336.CrossRefGoogle Scholar
  49. Niki, E. 1990. Free radical initiators as source of water- or lipid-soluble peroxyl radicals. In Methods in enzymology, ed. L. Packer and A.N. Glazer, vol. 186, 100–108Google Scholar
  50. Niki, E. 1996. α-tocopherol. In Handbook of antioxidants, ed. E. Cadenas and L. Packer, 3–26. New York: Marcel Dekker.Google Scholar
  51. Pan, J.S., M.Z. Hong, and J.L. Ren. 2009. Reactive oxygen species: A double-edged sword in oncogenesis. World Journal of Gastroenterology 15: 1702–1707.CrossRefGoogle Scholar
  52. Pedrielli, P., and L.H. Skibsted. 2002. Antioxidant synergy and regeneration effect of quercetin, (−)-epicatechin, and (+)-catechin on α-tocopherol in homogeneous solutions of peroxidating methyl linoleate. Journal of Agricultural and Food Chemistry 50: 7138–7144.CrossRefGoogle Scholar
  53. Pryor, W.A., and L. Castle. 1984. Chemical methods for detection of lipid hydroperoxides. In Methods in enzymology, vol. 105, ed. L. Packer, 203–208. New york: Academic Press.Google Scholar
  54. Rice-Evans, C.A., N.J. Miller, and G. Paganga. 1996. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radical Biology & Medicine 20: 933–956.CrossRefGoogle Scholar
  55. Sampson, J.B., Y. Ye, H. Rosen, and J.S. Beckman. 1998. Myeloperoxidase and horseradish peroxidase catalyze tyrosine nitration in proteins from nitrite and hydrogen peroxide. Archives of Biochemistry and Biophysics 356: 207–213.CrossRefGoogle Scholar
  56. Shirai, M., J.H. Moon, T. Tsushida, and J. Terao. 2001. Inhibitory effect of a quercetin metabolite, quercetin 3-O-beta-D-glucuronide, on lipid peroxidation in liposomal membranes. Journal of Agricultural and Food Chemistry 49: 5602–5608.CrossRefGoogle Scholar
  57. Steinberg, D., S. Parthasarathy, T.E. Carew, J.C. Khoo, and J.L. Witztum. 1989. Beyond cholesterol. Modifications of low-density lipoprotein that increase its atherogenicity. The New England Journal of Medicine 320: 915–924.CrossRefGoogle Scholar
  58. Steinbrecher, U.P., J.L. Wiztum, S. Parthasarathy, and D. Steinberg. 1987. Decrease in reactive amino groups during oxidation or endothelial cell modification of LDL. Correlation with changes in receptor-mediated catabolism. Arteriosclerosis 7: 135–143.CrossRefGoogle Scholar
  59. Stintzing, F.C., and R. Carle. 2004. Functional properties of anthocyanins and betalains in plants, food, and in human nutrition. Trends in Food Science and Technology 15: 19–38.CrossRefGoogle Scholar
  60. Tesoriere, L., D. Butera, D. D’Arpa, F. Di Gaudio, M. Allegra, C. Gentile, and M.A. Livrea. 2003. Increased resistance to oxidation of betalain-enriched human low density lipoproteins. Free Radical Research 37: 689–696.CrossRefGoogle Scholar
  61. Tesoriere, L., M. Allegra, D. Butera, and M.A. Livrea. 2004a. Absorption, excretion, and distribution in low density lipoproteins of dietary antioxidant betalains. Potential health effects of betalains in humans. American Journal of Clinical Nutrition 80: 941–945.Google Scholar
  62. Tesoriere, L., D. Butera, A.M. Pintaudi, M. Allegra, and M.A. Livrea. 2004b. Supplementation with cactus pear (Opuntia ficus indica) fruit decreases oxidative stress in healthy humans: A comparative study with vitamin C. American Journal of Clinical Nutrition 80: 391–395.Google Scholar
  63. Tesoriere, L., D. Butera, M. Allegra, M. Fazzari, and M.A. Livrea. 2005. Distribution of betalain pigments in red blood cells after consumption of cactus pear fruits and increased resistance of the cells to ex vivo-induced oxidative hemolysis in humans. Journal of Agricultural and Food Chemistry 53: 1266–1270.CrossRefGoogle Scholar
  64. Tesoriere, L., M. Fazzari, F. Angileri, C. Gentile, and M.A. Livrea. 2008. In vitro digestion of betalainic foods. Stability and bioaccessibility of betaxanthins and betacyanins and antioxidative potential of food digesta. Journal of Agricultural and Food Chemistry 56: 10487–10492.CrossRefGoogle Scholar
  65. Tesoriere, L., M. Allegra, C. Gentile, and M.A. Livrea. 2009. Betacyanins as phenol antioxidants. Chemistry and mechanistic aspects of the lipoperoxyl radical scavenging activity in solution and liposomes. Free Radical Research 43: 706–717.CrossRefGoogle Scholar
  66. Turco-Liveri, M.L., L. Sciascia, R. Lombardo, L. Tesoriere, E. Passante, and M.A. Livrea. 2007. Spectrophotometric evidence for the solubilization site of betalain pigments in membrane biomimetic systems. Journal of Agricultural and Food Chemistry 55: 2836–2840.CrossRefGoogle Scholar
  67. Uchida, K. 2007. Lipid peroxidation and redox-sensitive signaling pathways. Current Atherosclerosis Reports 9: 216–221.CrossRefGoogle Scholar
  68. Valgimigli, L., J.T. Banks, K.U. Ingold, and J. Lusztyk. 1995. Kinetic solvent effects on hydroxylic hydrogen atom abstractions are independent of the nature of the abstracting radical. Two extreme tests using vitamin e and phenol. Journal of the American Chemical Society 117: 9966–9971.CrossRefGoogle Scholar
  69. Valko, M., D. Leibfritz, J. Moncol, M.T. Cronin, M. Mazur, and J. Telser. 2007. Free radicals and antioxidants in normal physiological functions and human disease. The International Journal of Biochemistry & Cell Biology 39: 44–84.CrossRefGoogle Scholar
  70. van der Vliet, A., J.P. Eiserich, B. Halliwell, and C.E. Cross. 1997. Formation of reactive nitrogen species during peroxidase-catalyzed oxidation of nitrite. A potential additional mechanism of nitric oxide-dependent toxicity. Journal of Biological Chemistry 272: 7617–7625.CrossRefGoogle Scholar
  71. Willett, W.C., F. Sacks, A. Trichopoulou, G. Drescher, A. Ferro-Luzzi, E. Helsing, and D. Trichopoulous. 1995. Mediterranean diet pyramid: A cultural model for healthy eating. American Journal of Clinical Nutrition 61(suppl 6): 1402S–1406S.Google Scholar
  72. Wu, W.S., R.K. Tsai, C.H. Chang, S. Wang, J.R. Wu, and Y.X. Chang. 2006. Reactive oxygen species mediated sustained activation of protein kinase C alpha and extracellular signal-regulated kinase for migration of human hepatoma cell Hepg2. Molecular Cancer Research 4: 747–758.CrossRefGoogle Scholar
  73. Yamamoto, Y., E. Niki, and Y. Kamiya. 1982. Oxidation of lipids: III. Oxidation of methyl linoleate in solution. Lipids 17: 870–877.CrossRefGoogle Scholar
  74. Zou, B., Q. Miao, L. Yang, and Z.-L. Liu. 2005. Antioxidative effects of flavonols and their glycosides against the free-radical induced peroxidation of linoleic acid in solution and in micelles. Chemistry – A European Journal 11: 680–691.CrossRefGoogle Scholar

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© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Dipartimento STEMBIOUniversità di PalermoPalermoItaly

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