Inhibition of mitochondrial proton F0F1-ATPase/ATP synthase by polyphenolic phytochemicals

British Journal of Pharmacology

Volumn 130, Issue 5, 2000, Pages 1115-1123

  Zheng, Jianbiao ^a   Ramirez, Victor D ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Catechins; F0F1 ATPase ATP synthase; Flavonoids; Genistein; Mitochondria; Phytoestrogens; Resveratrol; Tea

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATE; BIOCHANIN A; BRAIN ENZYME; CURCUMIN; ENZYME INHIBITOR; EPICATECHIN GALLATE; EPIGALLOCATECHIN; GENISTEIN; KAEMPFEROL; LIVER ENZYME; MITOCHONDRIAL ENZYME; MORIN; PHLORIZIN; PHYTOESTROGEN; PICEATANNOL; POLYPHENOL DERIVATIVE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; QUERCETIN; RESVERATROL; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG POTENCY; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; GRAPE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; RAT; WINE;

EID: 0033922250     PISSN: 00071188     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjp.0703397     Document Type: Article

References (61)

1. ABRAHAMS, J.P., BUCHANAN, S.K., VAN RAAJJ, M.J., FEARNLEY, I.M., LESLIE, A.G.W. & WALKER, J.E. (1996). The structure of bovine F1-ATPase complexed with the peptide antibiotic efrapeptin. Proc. Natl. Acad. Sci. U.S.A., 93, 9420-9424.
2. ADLERCREUTZ, H. (1995). Phytoestrogens: epidemiology and a possible role in cancer protection. Environ. Health Perspect., 103, 103-112.
3. AKIYAMA, T., ISHIDA, J., NAKAGAWA, S., OGAWARA, H., WATANABE, S.-I., ITOH, N., SHIBUYA, M. & FUKAMI, Y. (1987). Genistein, a specific inhibitor of tyrosine-specific protein kinases. J. Biol. Chem., 262, 5592-5595.
4. 2+-ATPase. J. Pharmacol. Exp. Ther., 290, 227-234.
5. BARNES, S. & PETERSON, T.G. (1995). Biochemical targets of the isoflavone genistein in tumor cell lines. Proc. Soc. Exp. Biol. Med., 208, 103-108.
6. BOYER, P.D. (1997). The ATP synthase - a splendid molecular machine. Ann. Rev. Biochem., 66, 717-749.
7. BRADFORD, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254.
8. BRAVO, L. (1998). Polyphenols: chemistry, dietary sources, metabolism, and nutritional significance. Nutrition Rev., 56, 317-333.
9. CHUN, Y.J., KIM, M.Y. & GUENGERICH, F.P. (1999). Resveratrol is a selective human cytochrome P450 1A1 inhibitor. Biochem. Biophys. Res. Commun., 262, 20-24.
10. CIOLINO, H.P. & YEH, G.C. (1999). Inhibition of aryl hydrocarbon-induced cytochrome P-450 1A1 enzyme activity and CYP1A1 expression by resveratrol. Mol. Pharmacol., 56, 760-767.
11. CROSS, R.L. & KOHLBRENNER, W.E. (1978). The mode of inhibition of oxidative phosphorylation by efrapeptin (A23871). J. Biol. Chem., 253, 4865-4873.
12. + transporting ATP synthase on the surface of tumour cell lines. J. Exp. Med., 180, 273-281.
13. DASHWOOD, R.H. (1998). Indole-3-carbinol: anticarcinogen or tumor promoter in brassica vegetables? Chem. Biol. Interact., 110, 1-5.
14. DEMROW, H.S., SLANE, P.R. & FOLTS, J.D. (1995). Administration of wine and grape juice inhibits in vivo platelet activity and thrombosis in stenosed canine coronary arteries. Circulation, 91, 1182-1188.
15. DEWICK, P.M. (1997). Medicinal Natural Products: a Biosynthetic Approach. John Wilev & Sons, Chichester.
16. DI PIETRO, A., GODINOT, C.. BOUILLANT, M.-L. & GAUTHERON, D.C. (1975). Pig heart mitochondrial ATPase: properties of purified and membrane-bound enzyme. Biochimie, 57, 959-967.
17. EVANS, B.A., GRIFFITHS, K. & MORTON, M.S. (1995). Inhibition of 5 alpha-reductase in genital skin fibroblasts and prostate tissue by dietary ligans and isoflavonoids. J. Endocrinol., 147, 295-302.
18. FANG, N. & CASIDA, J.E. (1998). Anticancer action of cube insecticide: correlation for rotenoid constituents between inhibition of NADH:ubiquinone oxidoreductase and induced ornithine decarboxylase activities. Proc. Natl. Acad. Sci. U.S.A., 95, 3380-3384.
19. FERRELL, J.E., SING, P.D.G.C., LOEW, G., KING, R., MANSOUR, J.M. & MANSOUR, T.E. (1979). Structure/activity studies of flavonoids as inhibitors of cyclic AMP phosphodiesterase and relationship to quantum chemical indices. Mol. Pharmacol., 16, 556-568.
20. FEWTRELL, C.M.S. & GOMPERTS, B.D. (1977). Effect of flavone inhibitors of transport ATPases on histamine secretion from rat mast cells. Nature, 265, 635-636.
21. FOTSIS, T., PEPPER, M., ADLERCREUTZ, H., FLEISCHMANN, G., HASE, T., MONTESANO, R. & SCHWEIGERER, L. (1993). Genistein, a dietary-derived inhibitor of in vitro angiogenesis. Proc. Natl. Acad. Sci. U.S.A., 90, 2690-2694.
22. FRANKEL, E.N., WATERHOUSE, A.L. & KINSELLA, J.E. (1993). Inhibition of human LDL oxidation by resveratrol. Lancet, 341, 1103-1104.
23. FURHMAN, B., LAVY, A. & AVIRAM, M. (1995). Consumption of red wine with meals reduces the susceptibility of human plasma and low-density lipoprotein to lipid peroxidation. Am. J. Clin. Nutr., 61, 549-554.
24. GEHM, B.D., MCANDREWS, J.M., CHIEN, P.-Y. & JAMESON, J.L. (1997). Resveratrol, a polyphenolic compound found in grapes and wine, is an agonist for the estrogen receptor. Proc. Natl. Acad. Sci. U.S.A., 94, 14138-14143.
25. GOLDBERG, D.M., YAN, J., NG, E., DIAMANDIS, E.P., KARUMANCHIRI, A., SOLEAS, G. & WATERHOUSE, A.L. (1995). A global survey of trans-resveratrol concentrations in commercial wines. Am. J. Enol. Vitic., 46, 159-165.
26. HARRIS, D.A. (1987). Spectrophotometric assays. In Spectrophotometry and Spectrofluorimetry: a Practical Approach. ed. Harris, D.A. & Bashford, C.L. pp. 49-90. Oxford: IRL Press.
27. +-ATPase: aspects of the structure-activity relationship and action mechanism. Life Sci., 45, 1111-1117.
28. HOLLMAN, P.C., FESKENS, E.J.M. & KATAN, M.B. (1999). Tea flavonols in cardiovascular disease and cancer epidemiology. Proc. Soc. Exp. Biol. Med., 220, 198-202.
29. HSIEH, C.-Y., SANTELL, R.C., HASLAM, S.Z. & HELFERICH, W.G. (1998). Estrogenic effects of genistein on the growth of estrogen receptor-positive human breast cancer (MCF-7) cells in vitro and in vivo. Cancer Res., 58, 3833-3838.
30. JANG. M., CAI, L., UDEANI, G.O., SLOWING, K.V., THOMAS, C.F., BEECHER, C.W., FONG, H.H., FARNSWORTH, N.R., KINGHORD, A.D., MEHTA, R.G., MOON, R.C. & PEZZUTO, J.M. (1997). Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science, 275, 218-220.
31. KING, R.A. & BURSILL, D.B. (1998). Plasma and urinary kinetics of the isoflavones daidzein and genistein after a single soy mean in humans. Am. J. Clin. Nutr., 67, 867-872.
32. KUIPER, G.G.J.M., LEMMEN, J.G., CARLSSON, B., CORTON, J.C., SAFE, S.H,. VAN DER SAAG, P.T., VAN DER BURG, B. & GUSTAFSSON, J.-A. (1998). Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology, 139, 4252-4263.
33. LANG, D.R. & RACKER, E. (1974). Effects of quercetin and F1 inhibitor on mitochondrial ATPase and energy-linked reactions in submitochondrial particles. Biochim. Biophys. Acta, 333, 180-186.
34. LINNETT, P.E. & BEECHEY, R.B. (1979). Inhibitors of the ATP synthetase system. Methods Enzymol., 55, 472-518.
35. MATSUYAMA, S., XU, Q., VELOURS, J. & REED, J.C. (1998). The mitochondrial F0F1-ATPase proton pump is required for function of the proapoptotic protein Bax in yeast and mammalian cells. Mol. Cell., 1, 327-336.
36. MCENERY, M.W., BUHLER, Jr, E.L., AEBI, U. & PEDERSEN, P.L. (1984). Proton ATPase of rat liver mitochondria: preparation and visualization of a functional complex using the novel zwitterionic detergent 3-[(3-cholamidopropyl)dimethylammonio]-1-propansulfonate. J. Biol. Chem., 259, 4642-4651.
37. MCENERY, M.W., HULLIHEN, J. & PEDERSEN, P.L. (1989). F0 'proton channel' of rat liver mitochondria: rapid purification of a functional complex and a study of its interaction with the unique probe diethylstilbestrol. J. Biol. Chem., 264, 12029-12036.
38. MCENERY, M.W. & PEDERSEN, P.L. (1986). Diethylstilbestrol: a novel F0-directed probe of the mitochondrial proton ATPase. J. Biol. Chem., 261, 1745-1752.
39. 2+ ATPase by quercetin. J. Biol. Chem., 271, 24517-24525.
40. MOSER, T.L., STACK, M.S., ASPLIN, I., ENGHILD, J.J., HOJRUP, P., EVERITT, L., HUBCHAK, S., SCHNAPER, H.W. & PIZZO, S.V. (1999). Angiostatin binds ATP synthase on the surface of human endothelial cells. Proc. Natl. Acad. Sci. U.S.A., 96, 2811-2816.
41. MURKIES, A.L., WILCOX, G. & DAVIS, S.R. (1998). Clinical review 92: phytoestrogens. J. Clin. Endocrinol. Metab., 83, 297-303.
42. PEDERSEN, P.L. & AMZEL, L.M. (1993). ATP synthase: structure, reaction center, mechanism, and regulation of one of nature's most unique machines. J. Biol. Chem., 268, 9937-9940.
43. RAGAN, C.I., WILSON, M.T., DARLEY-USMAR, V.M. & LOWE, P.N. (1987). Subfractionation of mitochondria and isolation of the proteins of oxidative phosphorylation. In: Mitochondria: a Practical Approach. ed. Darley-Usmar, V.M., Rickwood, D. & Wilson, M.T. pp. 79-112. Oxford: IRL Press.
44. SERAFINI, M., MAIANI, G. & FERRO-LUZZI, A. (1998). Alcohol-free red wine enhances plasma antioxidant capacity in humans. J. Nutr., 128, 1003-1007.
45. SETCHELL, K.D.R. (1998). Phytoestrogens: the biochemistry, physiology, and implications for human health of soy isoflavones. Am. J. Clin. Nutr., 68, 1333S-1346S.
46. SHAO, Z.-M., ALPAUGH, M.L., FONTANA, J.A. & BARSKY, S.H. (1998). Genistein inhibits proliferation similarly in estrogen receptor-positive and negative human breast carcinoma cell lines characterized by P21WAF1 CIP1 induction, G2, M arrest, and apoptosis. J. Cell. Biochem., 69, 44-54.
47. STEVENS, M.F., MCCALL, C.J., LELIEVELD, P., ALEXANDER, P., RICHTER, A. & DAVIES, D.E. (1994). Structural studies on bioactive compounds. 23. Synthesis of polyhydroxylated 2-phenylbenzothiazoles and a comparison of their cytotoxicities and pharmacological properties with genistein and quercetin. J. Med. Chem., 37, 1689-1695.
48. THAM, D.M., GARDNER, C.D. & HASKELL, W.L. (1998). Clinical review 97: Potential health benefits of dietary phytoestrogens: a review of the clinical, epidemiological, and mechanistic evidence. J. Clin. Endocrinol. Metab., 83, 2223-2235.
49. VAN RAAJJ, M.J., ABRAHAMS, J.P., LESLIE, A.G.W. & WALKER, J.E. (1996). The structure of bovine F1-ATPase complexed with the antibiotic inhibitor aurovertin B. Proc. Natl. Acad. Sci. U.S.A., 93, 6913-6917.
50. VUORINEN, K., YLITALO, K., PEUHKURINEN, K., RAATIKAINEN, P., ALA-RAMI, A. & HASSINEN, I.E. (1995). Mechanisms of ischemic preconditioning in rat myocardium: roles of adenosine, cellular energy state, and mitochondrial F1F0-ATPase. Circulation. 91, 2810-2818.
51. WALLACE, D.C. (1999). Mitochondrial diseases in man and mouse. Science. 283, 1482-1488.
52. WATANABE, S., YAMAGUCHI, M., SOBUE, T., TAKAHASHI, T., MIURA, T., ARAI, Y., MAZUR, W., WAHALA, K. & ADLERCREUTZ, H. (1998). Pharmacokinetics of soybean isoflavones in plasma, urine and feces of men after ingestion of 60 g baked soybean powder (kinako). J. Nutr., 128, 1710-1715.
53. WATKINS, T.R. (1997). Wine: Nutritional and Therapeutic Benefits. American Chemical Society, Washington, DC.
54. WOLVETANG, E.J., JOHNSON, K.L., KRAUER. K., RALPH, S.J. & LINNANE, A.W. (1994). Mitochondrial respiratory chain inhibitors induce apoptosis. FEBS Lett., 339, 40-44.
55. XU, X., HARRIS, K.S., WANG, H.J., MURPHY, P.A. & HENDRICH, S. (1995). Bioavailability of soybean isoflavones depends upon gut microflora in women. Nutr., 125, 2307-2315.
56. YANG, C.S., KIM, S., YANG, G.-Y., LEE, M.-J., LIAO, J., CHUNG, J.Y. & HO, C.-T. (1999). Inhibition of carcinogenesis by tea: bioavailability of tea polyphenols and mechanisms of actions. Proc. Soc. Exp. Biol. Med., 220, 213-217.
57. YE, X., KROHN, R.L., LIU, W., JOSHI, S.S., KUSZYNSKI, C.A., MCGINN, T.R., BAGCHI, M., PREUSS, H.G., STOHS, S.J. & BAGCHI, D. (1999). The cytotoxic effects of a novel 1H 636 grape seed proanthocyanidin extract on culture human cancer cells. Mol. Cell. Biochem., 196, 99-108.
58. ZHENG, J. & RAMIREZ, V.D. (1999a). Purification and identification of an estrogen binding protein from rat brain: oligomycin sensitivity-conferring protein (OSCP), a subunit of mitochondrial F0F1-ATP synthase ATPase. J. Steroid Biochem. Mol. Biol., 68, 65-75.
59. +-ATPase of porcine cortex. Eur. J. Pharmacol., 368, 95-102.
60. ZHENG, J. & RAMIREZ, V.D. (1999c). Piceatannol, a stilbene phytochemical, inhibits mitochondrial F0F1-ATPase activity by targeting the F1 complex. Biochem. Biophys. Res. Commun., 261, 499-503.
61. ZINI, R., MORIN, C., BERTELLI, A., BERTELLI, A.A. & TILLEMENT, J.P. (1999). Effects of resveratrol on the rat brain respiratory chain. Drugs Exp. Clin. Res., 25, 87-97.