Interference of the polyphenol epicatechin with the biological chemistry of nitric oxide- and peroxynitrite-mediated reactions

Biochemical Pharmacology

Volumn 67, Issue 7, 2004, Pages 1285-1295

  Wippel, Rüdiger ^a   Rehn, Margit ^a   Gorren, Antonius C F ^a   Schmidt, Kurt ^a   Mayer, Bernd ^a  

^a UNIVERSITY OF GRAZ   (Austria)

Author keywords

CGMP; Cyclic GMP; Endothelial NO synthase (type III); ENOS; High performance liquid chromatography; HPLC; IFN; Inducible NO synthase (type II); INOS; Interferon; Lipopolysaccharide; LPS; MPO; Myeloperoxidase; Nitric oxide; NO; NO synthase; NOS; PBS

Indexed keywords

ALPHA INTERFERON; BICARBONATE; CYCLIC GMP; EPICATECHIN; FLAVONOID; LIPOPOLYSACCHARIDE; MYELOPEROXIDASE; NITRIC OXIDE; NITRITE; PEROXYNITRITE; PHORBOL 13 ACETATE 12 MYRISTATE; POLYPHENOL; REACTIVE NITROGEN SPECIES;

ANIMAL CELL; ARTICLE; CELL CULTURE; CONTROLLED STUDY; DRUG ACTIVITY; DRUG CYTOTOXICITY; DRUG EFFECT; ENDOTHELIUM CELL; ENZYME ACTIVITY; GENERAL ASPECTS OF DISEASE; HUMAN; HUMAN CELL; IC 50; INFLAMMATION; MACROPHAGE; MOUSE; NITRATION; NONHUMAN; OXIDATION; PRIORITY JOURNAL; SMOOTH MUSCLE RELAXATION;

CATECHIN; CYCLIC GMP; FLAVONOIDS; HL-60 CELLS; HUMANS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; OXIDATION-REDUCTION; PEROXYNITROUS ACID; PHENOLS; SIGNAL TRANSDUCTION; TYROSINE;

EID: 1542345741     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2003.11.017     Document Type: Article

References (72)

1. Weiss S.J. Tissue destruction by neutrophils. N. Engl. J. Med. 320:1989;365-376.
2. Ischiropoulos H. Biological tyrosine nitration: a pathophysiological function of nitric oxide and reactive oxygen species. Arch. Biochem. Biophys. 356:1998;1-11.
3. 2 peptide. Proc. Natl. Acad. Sci. USA. 93:1996;3377-3382.
4. Go Y.M., Patel R.P., Maland M.C., Park H., Beckman J.S., Darley-Usmar V.M., Jo H. Evidence for peroxynitrite as a signaling molecule in flow-dependent activation of c-Jun NH(2)-terminal kinase. Am. J. Physiol. 277:1999;H1647-H1653.
5. Berlett B.S., Levine R.L., Stadtman E.R. Carbon dioxide stimulates peroxynitrite-mediated nitration of tyrosine residues and inhibits oxidation of methionine residues of glutamine synthetase: both modifications mimic effects of adenylylation. Proc. Natl. Acad. Sci. USA. 95:1998;2784-2789.
6. MacMillan-Crow L.A., Crow J.P., Thompson J.A. Peroxynitrite-mediated inactivation of manganese superoxide dismutase involves nitration and oxidation of critical tyrosine residues. Biochemistry. 37:1998;1613-1622.
7. Estevez A.G., Crow J.P., Sampson J.B., Reiter C., Zhuang Y., Richardson G.J., Tarpey M.M., Barbeito L., Beckman J.S. Induction of nitric oxide-dependent apoptosis in motor neurons by zinc-deficient superoxide dismutase. Science. 286:1999;2498-2500.
8. Eiserich J.P., Estevez A.G., Bamberg T.V., Ye Y.Z., Chumley P.H., Beckman J.S., Freeman B.A. Microtubule dysfunction by posttranslational nitrotyrosination of alpha-tubulin: a nitric oxide-dependent mechanism of cellular injury. Proc. Natl. Acad. Sci. USA. 96:1999;6365-6370.
9. van der Vliet A., Eiserich J.P., O'Neill C.A., Halliwell B., Cross C.E. Tyrosine modification by reactive nitrogen species: a closer look. Arch. Biochem. Biophys. 319:1995;341-349.
10. Lymar S.V., Hurst J.K. Carbon dioxide: physiological catalyst for peroxynitrite-mediated cellular damage or cellular protectant? Chem. Res. Toxicol. 9:1996;845-850.
11. Lymar S.V., Hurst J.K. Rapid reaction between peroxonitrite ion and carbon dioxide: implications for biological activity. J. Am. Chem. Soc. 117:1995;8867-8868.
12. Gow A., Duran D., Thom S.R., Ischiropoulos H. Carbon dioxide enhancement of peroxynitrite-mediated protein tyrosine nitration. Arch. Biochem. Biophys. 333:1996;42-48.
13. Denicola A., Freeman B.A., Trujillo M., Radi R. Peroxynitrite reaction with carbon dioxide/bicarbonate: kinetics and influence on peroxynitrite- mediated oxidations. Arch. Biochem. Biophys. 333:1996;49-58.
14. Burner U., Furtmuller P.G., Kettle A.J., Koppenol W.H., Obinger C. Mechanism of reaction of myeloperoxidase with nitrite. J. Biol. Chem. 275:2000;20597-20601.
15. Eiserich J.P., Cross C.E., Jones A.D., Halliwell B., van der Vliet A. Formation of nitrating and chlorinating species by reaction of nitrite with hypochlorous acid. A novel mechanism for nitric oxide-mediated protein modification. J. Biol. Chem. 271:1996;19199-19208.
16. Whiteman M., Hooper D.C., Scott G.S., Koprowski H., Halliwell B. Inhibition of hypochlorous acid-induced cellular toxicity by nitrite. Proc. Natl. Acad. Sci. USA. 99:2002;12061-12066.
17. Whiteman M., Rose P., Halliwell B. Inhibition of hypochlorous acid-induced oxidative reactions by nitrite: is nitrite an antioxidant? Biochem. Biophys. Res. Commun. 303:2003;1217-1224.
18. Whiteman M., Siau J.L., Halliwell B. Lack of tyrosine nitration by hypochlorous acid in the presence of physiological concentrations of nitrite. Implications for the role of nitryl chloride in tyrosine nitration in vivo. J. Biol. Chem. 278:2003;8380-8384.
19. Nathan C., Shiloh M.U. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc. Natl. Acad. Sci. USA. 97:2000;8841-8848.
20. Beckman J.S., Koppenol W.H. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and the ugly. Am. J. Physiol. 271:1996;C1424-C1437.
21. Klotz L.O., Sies H. Defenses against peroxynitrite: selenocompounds and flavonoids. Toxicol. Lett. 140/141:2003;125-132.
22. Schroeder P., Klotz L.O., Buchczyk D.P., Sadik C.D., Schewe T., Sies H. Epicatechin selectively prevents nitration but not oxidation reactions of peroxynitrite. Biochem. Biophys. Res. Commun. 285:2001;782-787.
23. Schroeder P., Klotz L.O., Sies H. Amphiphilic properties of (-)-epicatechin and their significance for protection of cells against peroxynitrite. Biochem. Biophys. Res. Commun. 307:2003;69-73.
24. Stoner G.D., Mukhtar H. Polyphenols as cancer chemopreventive agents. J. Cell. Biochem. Suppl. 22:1995;169-180.
25. Sanbongi C., Suzuki N., Sakane T. Polyphenols in chocolate, which have antioxidant activity, modulate immune functions in humans in vitro. Cell. Immunol. 177:1997;129-136.
26. Rice-Evans C.A., Miller N.J., Paganga G. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic Biol. Med. 20:1996;933-956.
27. Geleijnse J.M., Launer L.J., Van der Kuip D.A., Hofman A., Witteman J.C. Inverse association of tea and flavonoid intakes with incident myocardial infarction: the Rotterdam Study. Am. J. Clin. Nutr. 75:2002;880-886.
28. van Acker S.A., Tromp M.N., Haenen G.R., van der Vijgh W.J., Bast A. Flavonoids as scavengers of nitric oxide radical. Biochem. Biophys. Res. Commun. 214:1995;755-759.
29. Robak J., Gryglewski R.J. Flavonoids are scavengers of superoxide anions. Biochem. Pharmacol. 37:1988;837-841.
30. Kostyuk V.A., Kraemer T., Sies H., Schewe T. Myeloperoxidase/nitrite- mediated lipid peroxidation of low-density lipoprotein as modulated by flavonoids. FEBS Lett. 537:2003;146-150.
31. Brennan M.L., Wu W., Fu X., Shen Z., Song W., Frost H., Vadseth C., Narine L., Lenkiewicz E., Borchers M.T., Lusis A.J., Lee J.J., Lee N.A., Abu-Soud H.M., Ischiropoulos H., Hazen S.L. A tale of two controversies: defining both the role of peroxidases in nitrotyrosine formation in vivo using eosinophil peroxidase and myeloperoxidase-deficient mice, and the nature of peroxidase-generated reactive nitrogen species. J. Biol. Chem. 277:2002;17415-17427.
32. Leber A., Hemmens B., Klosch B., Goessler W., Raber G., Mayer B., Schmidt K. Characterization of recombinant human endothelial nitric-oxide synthase purified from the yeast Pichia pastoris. J. Biol. Chem. 274:1999;37658-37664.
33. Kukovetz W.R., Holzmann S. Tolerance and cross tolerance between SIN-1 and nitric oxide in bovine coronary arteries. J. Cardiovasc Pharmacol. 14:1989;S40-S46.
34. Pfeiffer S., Gorren A.C., Schmidt K., Werner E.R., Hansert B., Bohle D.S., Mayer B. Metabolic fate of peroxynitrite in aqueous solution. Reaction with nitric oxide and pH-dependent decomposition to nitrite and oxygen in a 2:1 stoichiometry. J. Biol. Chem. 272:1997;3465-3470.
35. Schmidt K., Klatt P., Mayer B. Reaction of peroxynitrite with oxyhaemoglobin: interference with photometrical determination of nitric oxide. Biochem. J. 301:1994;645-647.
36. Mayer B., Brunner F., Schmidt K. Inhibition of nitric oxide synthesis by methylene blue. Biochem. Pharmacol. 45:1993;367-374.
37. 15N ]nitrate in biological fluids Anal. Biochem. 126:1982;131-138.
38. Golser R., Gorren A.C., Leber A., Andrew P., Habisch H.J., Werner E.R., Schmidt K., Venema R.C., Mayer B. Interaction of endothelial and neuronal nitric-oxide synthases with the bradykinin B2 receptor. Binding of an inhibitory peptide to the oxygenase domain blocks uncoupled NADPH oxidation. J. Biol. Chem. 275:2000;5291-5296.
39. Mayer B., Klatt P., Werner E.R., Schmidt K. Molecular mechanisms of inhibition of porcine brain nitric oxide synthase by the antinociceptive drug 7-nitro-indazole. Neuropharmacology. 33:1994;1253-1259.
40. Kettle A.J., Winterbourn C.C. Assays for the chlorination activity of myeloperoxidase. Methods Enzymol. 233:1994;502-512.
41. Shigenaga M.K. Quantitation of protein-bound 3-nitrotyrosine by high-performance liquid chromatography with electrochemical detection. Methods Enzymol. 301:1999;27-40.
42. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:1976;248-254.
43. Kooy N.W., Royall J.A., Ischiropoulos H., Beckman J.S. Peroxynitrite-mediated oxidation of dihydrorhodamine 123. Free Radic Biol. Med. 16:1994;149-156.
44. Crow J.P. Dichlorodihydrofluorescein and dihydrorhodamine 123 are sensitive indicators of peroxynitrite in vitro: implications for intracellular measurement of reactive nitrogen and oxygen species. Nitric Oxide. 1:1997;145-157.
45. Schrammel A., Pfeiffer S., Schmidt K., Koesling D., Mayer B. Activation of soluble guanylyl cyclase by the nitrovasodilator 3-morpholinosydnonimine involves formation of S-nitrosoglutathione. Mol. Pharmacol. 54:1998;207-212.
46. Miranda K.M., Espey M.G., Wink D.A. A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide. 5:2001;62-71.
47. Rosen G.M., Pou S., Ramos C.L., Cohen M.S., Britigan B.E. Free radicals and phagocytic cells. FASEB J. 9:1995;200-209.
48. Augusto O., Bonini M.G., Amanso A.M., Linares E., Santos C.C., De Menezes S.L. Nitrogen dioxide and carbonate radical anion: two emerging radicals in biology. Free Radic Biol. Med. 32:2002;841-859.
49. Cadenas S., Cadenas A.M. Fighting the stranger-antioxidant protection against endotoxin toxicity. Toxicology. 180:2002;45-63.
50. Pfeiffer S., Leopold E., Hemmens B., Schmidt K., Werner E.R., Mayer B. Interference of carboxy-PTIO with nitric oxide- and peroxynitrite-mediated reactions. Free Radic Biol. Med. 22:1997;787-794.
51. Pfeiffer S., Schrammel A., Koesling D., Schmidt K., Mayer B. Molecular actions of a Mn(III)Porphyrin superoxide dismutase mimetic and peroxynitrite scavenger: reaction with nitric oxide and direct inhibition of NO synthase and soluble guanylyl cyclase. Mol. Pharmacol. 53:1998;795-800.
52. Huang Y., Chan N.W., Lau C.W., Yao X.Q., Chan F.L., Chen Z.Y. Involvement of endothelium/nitric oxide in vasorelaxation induced by purified green tea (-)epicatechin. Biochim. Biophys. Acta. 1427:1999;322-328.
53. Stoclet J.C., Kleschyov A., Andriambeloson E., Diebolt M., Andriantsitohaina R. Endothelial no release caused by red wine polyphenols. J. Physiol. Pharmacol. 50:1999;535-540.
54. Leikert J.F., Rathel T.R., Wohlfart P., Cheynier V., Vollmar A.M., Dirsch V.M. Red wine polyphenols enhance endothelial nitric oxide synthase expression and subsequent nitric oxide release from endothelial cells. Circulation. 106:2002;1614-1617.
55. Wallerath T., Deckert G., Ternes T., Anderson H., Li H., Witte K., Forstermann U. Resveratrol, a polyphenolic phytoalexin present in red wine, enhances expression and activity of endothelial nitric oxide synthase. Circulation. 106:2002;1652-1658.
56. Chan M.M., Fong D., Ho C.T., Huang H.I. Inhibition of inducible nitric oxide synthase gene expression and enzyme activity by epigallocatechin gallate, a natural product from green tea. Biochem. Pharmacol. 54:1997;1281-1286.
57. Chan M.M., Ho C.T., Huang H.I. Effects of three dietary phytochemicals from tea, rosemary and turmeric on inflammation-induced nitrite production. Cancer Lett. 96:1995;23-29.
58. Ketsawatsakul U., Whiteman M., Halliwell B. A reevaluation of the peroxynitrite scavenging activity of some dietary phenolics. Biochem. Biophys. Res. Commun. 279:2000;692-699.
59. 2 adduct and of reactions with L-tyrosine and related compounds as studied by N-15 chemically induced dynamic nuclear polarization. Arch. Biochem. Biophys. 368:1999;303-318.
60. Santos C.X.C., Bonini M.G., Augusto O. Role of the carbonate radical anion in tyrosine nitration and hydroxylation by peroxynitrite. Arch. Biochem. Biophys. 377:2000;146-152.
61. Miau J.L., Wang W.F., Pan J.X., Lu C.Y., Li R.Q., Yao S.D. The scavenging reactions of nitrogen dioxide radical and carbonate radical by tea polyphenol derivatives: a pulse radiolysis study. Radiat Phys. Chem. 60:2001;163-168.
62. Schroeder P., Zhang H., Klotz L.O., Kalyanaraman B., Sies H. (-)-Epicatechin inhibits nitration and dimerization of tyrosine in hydrophilic as well as hydrophobic environments. Biochem. Biophys. Res. Commun. 289:2001;1334-1338.
63. Pfeiffer S., Schmidt K., Mayer B. Dityrosine formation outcompetes tyrosine nitration at low steady-state concentrations of peroxynitrite. Implications for tyrosine modification by nitric oxide/superoxide in vivo. J. Biol. Chem. 275:2000;6346-6352.
64. Pfeiffer S., Lass A., Schmidt K., Mayer B. Protein tyrosine nitration in cytokine-activated murine macrophages. Involvement of a peroxidase/nitrite pathway rather than peroxynitrite. J. Biol. Chem. 276:2001;34051-34058.
65. Espey M.G., Xavier S., Thomas D.D., Miranda K.M., Wink D.A. Direct real-time evaluation of nitration with green fluorescent protein in solution and within human cells reveals the impact of nitrogen dioxide vs. peroxynitrite mechanisms. Proc. Natl. Acad. Sci. USA. 99:2002;3481-3486.
66. van der Vliet A., Eiserich J.P., Halliwell B., Cross C.E. Formation of reactive nitrogen species during peroxidase-catalyzed oxidation of nitrite. A potential additional mechanism of nitric oxide-dependent toxicity. J. Biol. Chem. 272:1997;7617-7625.
67. Eiserich J.P., Hristova M., Cross C.E., Jones A.D., Freeman B.A., Halliwell B., van der Vliet A. Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils. Nature. 391:1998;393-397.
68. Hazen S.L., Zhang R., Shen Z., Wu W., Podrez E.A., MacPherson J.C., Schmitt D., Mitra S.N., Mukhopadhyay C., Chen Y., Cohen P.A., Hoff H.F., Abu-Soud H.M. Formation of nitric oxide-derived oxidants by myeloperoxidase in monocytes: pathways for monocyte-mediated protein nitration and lipid peroxidation in vivo. Circ Res. 85:1999;950-958.
69. Baldus S., Eiserich J.P., Brennan M.L., Jackson R.M., Alexander C.B., Freeman B.A. Spatial mapping of pulmonary and vascular nitrotyrosine reveals the pivotal role of myeloperoxidase as a catalyst for tyrosine nitration in inflammatory diseases. Free Radic Biol. Med. 33:2002;1010.
70. Arteel G.E., Sies H. Protection against peroxynitrite by cocoa polyphenol oligomers. FEBS Lett. 462:1999;167-170.
71. Arteel G.E., Schroeder P., Sies H. Reactions of peroxynitrite with cocoa procyanidin oligomers. J. Nutr. 130:2000;2100S-2104S.
72. Furuno K., Akasako T., Sugihara N. The contribution of the pyrogallol moiety to the superoxide radical scavenging activity of flavonoids. Biol. Pharm. Bull. 25:2002;19-23.