Mitochondria accumulate large amounts of quercetin: Prevention of mitochondrial damage and release upon oxidation of the extramitochondrial fraction of the flavonoid

Journal of Nutritional Biochemistry

Volumn 21, Issue 5, 2010, Pages 397-404

  Fiorani, Mara ^a   Guidarelli, Andrea ^a   Blasa, Manuela ^a   Azzolini, Catia ^a   Candiracci, Manila ^a   Piatti, Elena ^a   Cantoni, Orazio ^a  

^a UNIVERSITY OF URBINO   (Italy)

Author keywords

Cellular uptake; Cytoprotection; Mitochondrial accumulation; Quercetin; Trans plasma membrane oxidoreductase

Indexed keywords

ALBUMIN; FLAVONOID; OXIDOREDUCTASE; PEROXYNITRITE; QUERCETIN; REACTIVE OXYGEN METABOLITE;

ANTIOXIDANT ACTIVITY; ARTICLE; BINDING AFFINITY; BIOACCUMULATION; BIOLOGICAL ACTIVITY; CELL DAMAGE; CELL MEMBRANE TRANSPORT; CELL PROTECTION; CELL SURVIVAL; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOSOLIC FRACTION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG MECHANISM; DRUG PROTEIN BINDING; ENZYME ACTIVATION; EXTRACELLULAR FLUID; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; LIPID PEROXIDATION; MITOCHONDRIAL MEMBRANE; OXIDATION REDUCTION REACTION;

CELL MEMBRANE; CYTOPROTECTION; CYTOSOL; FREE RADICAL SCAVENGERS; HUMANS; JURKAT CELLS; LIPID PEROXIDATION; MITOCHONDRIA; MITOCHONDRIAL DISEASES; OXIDATION-REDUCTION; OXIDOREDUCTASES; PEROXYNITROUS ACID; QUERCETIN; SPECTROMETRY, FLUORESCENCE; THIOBARBITURIC ACID REACTIVE SUBSTANCES;

EID: 77951498353     PISSN: 09552863     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2009.01.014     Document Type: Article

References (50)

1. Middleton E., Kandaswami C., Theoharides T.C. The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease and cancer. Pharmacol Rev 2000, 52:673-751.
2. Hertog M.G.L., Feskens E.J.M., Hollman P.C.H., Katan M.B., Kromhout D. Dietary antioxidant flavonoids and risk of coronary heart disease: the Zutphen Elderly Study. Lancet 1993, 342:1007-1011.
3. Arts I.C.W., Hollmann P.C.H. Polyphenols and disease risk in epidemiologic studies. Am J Clin Nutr 2005, 81:317S-325S.
4. Afanas'ev I.B., Dorozhko A.I., Brodskii A.V., Kostyuk V.A., Potapovitch A.I. Chelating and free radical scavenging mechanisms of inhibitory action of rutin and quercetin in lipid peroxidation. Biochem Pharmacol 1989, 38:1763-1769.
5. Bors W., Heller W., Michel C., Saran M. Radical chemistry of flavonoid antioxidants. Adv Exp Med Biol 1990, 264:165-170.
6. Rice-Evans C., Miller N., Pagana G. Antioxidant properties of phenolic compounds. Trends Plant Sci 1997, 2:152-159.
7. Williams R.J., Spencer J.P., Rice-Evans C. Flavonoids: antioxidants or signalling molecules?. Free Radic Biol Med 2004, 36:838-849.
8. Storz P. Mitochondrial ROS-radical detoxification, mediated by protein kinase D. Trends Cell Biol 2007, 17:13-18.
9. Le Bras M., Clément M.V., Pervaiz S., Brenner C. Reactive oxygen species and the mitochondrial signaling pathway of cell death. Histol Histopathol 2005, 20:205-219.
10. Arnoult D. Apoptosis-associated mitochondrial outer membrane permeabilization assays. Methods 2008, 44:229-234.
11. Andreyev A.Y., Kushnareva Y.E., Starkov A.A. Mitochondrial metabolism of reactive oxygen species. Biochemistry 2005, 70:200-214.
12. Fiorani M., Accorsi A., Cantoni O. Human red blood cells as a natural flavonoid reservoir. Free Rad Res 2003, 37:1931-1938.
13. Strobel P., Allard C., Perez-Acle T., Calderon R., Aldunate R., Leighton F. Myricetin, quercetin and catechin-gallate inhibit glucose uptake in isolated rat adipocytes. Biochem J 2005, 386:471-478.
14. Johnston K., Sharp P., Clifford M., Morgan L. Dietary polyphenols decrease glucose uptake by human intestinal Caco-2 cells. FEBS Lett 2005, 579:1653-1657.
15. Fiorani M., Accorsi A., Blasa M., Diamantini G., Piatti E. Flavonoids from Italian multifloral honeys reduce the extracellular ferricyanide in human red blood cells. JAgric Food Chem 2006, 54:8328-8334.
16. Fiorani M., Accorsi A. Dietary flavonoids as intracellular substrates for an erythrocyte trans-plasma membrane oxidoreductase activity. Br J Nutr 2005, 94:338-345.
17. Brookes P.S., Digerness S.B., Parks D.A., Darley-Usmar V. Mitochondrial function in response to cardiac ischemia-reperfusion after oral treatment with quercetin. Free Radic Biol Med 2002, 32:1220-1228.
18. Montero M., Lobatón C.D., Hernández-Sanmiguel E., Santodomingo J., Vay L., Moreno A., et al. Direct activation of the mitochondrial calcium uniporter by natural plant flavonoids. Biochem J 2004, 384:19-24.
19. Dorta D.J., Pigoso A.A., Mingatto F.E., Rodrigues T., Prado I.M.R., Helena A.F.C., et al. The interaction of flavonoids with mitochondria: effects on energetic processes. Chem Biol Interact 2005, 152:67-78.
20. Trumbeckaite S., Bernatoniene J., Majiene D., Jakštas V., Savickas A., Toleikis A. The effect of flavonoids on rat heart mitochondrial function. Biomed Pharmacother 2006, 60:245-248.
21. Park C., So H.S., Shin C.H., Baek S.H., Moon B.S., Shin S.H., et al. Quercetin protects the hydrogen peroxide-induced apoptosis via inhibition of mitochondrial dysfunction in H9c2 cardiomyoblast cells. Biochem Pharmacol 2003, 66:1287-1295.
22. Radi R., Beckman J.S., Bush K.M., Freeman B.A. Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. J Biol Chem 1991, 266:4244-4250.
23. Tommasini I., Sestili P., Cantoni O. Delayed formation of hydrogen peroxide mediates the lethal response evoked by peroxynitrite in U937 cells. Mol Pharmacol 2002, 61:870-878.
24. Day A.J., Bao Y., Morgan M.R.A., Williamson G. Conjugation position of quercetin glucuronides and effect on biological activity. Free Radic Biol Med 2000, 29:1234-1243.
25. Lutsenko E.A., Cárcamo J.M., Golde D.W. Vitamin C prevents DNA mutation induced by oxidative stress. J Biol Chem 2002, 277:16895-16899.
26. Li X., Cobb C.E., Hill K.E., Burk R.F., May J.M. Mitochondrial uptake and recycling of ascorbic acid. Arch Biochem Biophys 2001, 387:143-153.
27. Li X., Cobb C.E., May J.M. Mitochondrial recycling of ascorbic acid from dehydroascorbic acid: dependence on the electron transport chain. Arch Biochem Biophys 2002, 403:103-110.
28. 2. Biochem J 2002, 366:307-314.
29. Beutler E. Red cell metabolism: a manual of biochemical methods 1984, Grune and Stratton, Inc., London, NW. 3th ed.
30. Robinson J., Cooper J.M. Method of determining oxygen concentrations in biological media, suitable for calibration of the oxygen electrode. Anal Biochem 1970, 33:390-399.
31. Avron M., Shavit N. A sensitive simple method for determination of ferrocyanide. Anal Biochem 1963, 6:549-555.
32. Santos A.C., Uyemura S.A., Lopes J.L.C., Bazon J.N., Mingatto F.E., Curti C. Effect of naturally occurring flavonoids on lipid peroxidation and membrane permeability transition in mitochondria. Free Radic Biol Med 1998, 24:1455-1461.
33. Fiorani M., De Sanctis R., De Bellis R., Dachà M. Intracellular flavonoids as electron donors for extracellular ferricyanide reduction in human erythrocytes. Free Radic Biol Med 2002, 32:64-72.
34. Himmelreich U., Kuchel P.W. 13C-NMR studies of transmembrane electron transfer to extracellular ferricyanide in human erythrocytes. Eur J Biochem 1997, 246:638-645.
35. May J.M., Qu Z.C. Ascorbate-dependent electron transfer across the human erythrocyte membrane. Biochim Biophys Acta 1999, 1421:19-31.
36. May J.M., Qu Z.C., Morrow J.D., Cobb C.E. Ascorbate-dependent protection of human erythrocytes against oxidant stress generated by extracellular diazobenzene sulfonate. Biochem Pharmacol 2000, 60:47-53.
37. VanDuijn M.M., Tijssen K., VanSteveninck J., Van den Broek P.J.A., Van der Zee J. Erythrocytes reduce extracellular ascorbate free radicals using intracellular ascorbate as an electron donor. J Biol Chem 2000, 275:27720-27725.
38. May J.M., Qu Z.C., Cobb C.E. Extracellular reduction of the ascorbate free radical by human erythrocytes. Biochem Biophys Res Commun 2000, 267:118-123.
39. Nifli A.P., Theodoropoulos P.A., Munier S., Castagnino C., Roussakis E., Katerinopoulos H.E., et al. Quercetin exhibits a specific fluorescence in cellular milieu: a valuable tool for the study of its intracellular distribution. J Agric Food Chem 2007, 55:2873-2878.
40. Dufour C., Loonis M., Dangles O. Inhibition of the peroxidation of linoleic acid by the flavonoid quercetin within their complex with human serum albumin. Free Radic Biol Med 2007, 43:241-252.
41. Diniz A., Escuder-Gilabert L., Lopes N.P., Villanueva-Camañas R.M., Sagrado S., Medina-Hernández M.J. Characterization of interactions between polyphenolic compounds and human serum proteins by capillary electrophoresis. Anal Bioanal Chem 2008, 391:625-632.
42. Xiao J., Suzuki M., Jiang X., Chen X., Yamamoto K., Ren F., Xu M. Influence of B-ring hydroxylation on interactions of flavonols with bovine serum albumin. J Agric Food Chem 2008, 56:2350-2356.
43. Juqun X., Rong G. Interactions between flavonoids and hemoglobin in lecithin liposomes. Int J Biol Macromol 2007, 40:305-311.
44. Moon Y.J., Wang X., Morris M.E. Dietary flavonoids: effects on xenobiotic and carcinogen metabolism. Toxicol in Vitro 2006, 20:187-210.
45. Sestili P., Guidarelli A., Dachà M., Cantoni O. Quercetin prevents DNA single strand breakage and cytotoxicity caused by tert-butylhydroperoxide: free radical scavenging versus iron chelating mechanism. Free Radic Biol Med 1998, 25:196-200.
46. Spencer J.P., Abd-el-Mohsen M.M., Rice-Evans C. Cellular uptake and metabolism of flavonoids and their metabolites: implications for their bioactivity. Arch Biochem Biophys 2004, 423:148-161.
47. Spencer J.P., Schroeter H., Kuhnle G., Srai S.K., Tyrrell R.M., Hahn U., et al. Epicatechin and its in vivo metabolite, 3'-O-methyl epicatechin, protect human fibroblasts from oxidative-stress-induced cell death involving caspase-3 activation. Biochem J 2001, 354:493-500.
48. Manach C., Williamson G., Morand C., Scalbert A., Rémésy C. Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am J Clin Nutr 2005, 81:230S-242S.
49. Williamson G., Manach C. Bioavailability and bioefficacy of polyphenols in humans. II. Review of 93 intervention studies. Am J Clin Nutr 2005, 81:243S-255S.
50. Tukey R.H., Strassburg C.P. Human UDP-glucuronosyltransferases: metabolism, expression, and disease. Annu Rev Pharmacol Toxicol 2000, 40:581-616.