Flavonoids inhibit the amidolytic activity of human thrombin

Biochimie

Volumn 88, Issue 9, 2006, Pages 1297-1306

  Mozzicafreddo, M ^a   Cuccioloni, M ^a   Eleuteri, A M ^a   Fioretti, E ^a   Angeletti, M ^a  

^a UNIVERSITY OF CAMERINO   (Italy)

Author keywords

Bioinformatics; Biosensor; Equilibrium studies; Kinetics; Polyphenols

Indexed keywords

FLAVANOID; QUERCETIN; THROMBIN; AMIDASE; ARGATROBAN; FLAVONOID; PIPECOLIC ACID DERIVATIVE;

ALKALINITY; ARTICLE; BIOSENSOR; CHEMICAL BOND; DRUG ACTIVITY; DRUG EFFECT; DRUG SCREENING; DRUG STRUCTURE; HUMAN; PH; SPECTROPHOTOMETRY; BINDING COMPETITION; BINDING SITE; BLOOD CLOTTING; CHEMICAL STRUCTURE; CHEMISTRY; DRUG ANTAGONISM; ENZYME ACTIVATION; ENZYME STABILITY; GENETIC PROCEDURES; KINETICS; QUANTITATIVE STRUCTURE ACTIVITY RELATION;

AMIDOHYDROLASES; BINDING SITES; BINDING, COMPETITIVE; BIOSENSING TECHNIQUES; BLOOD COAGULATION; ENZYME ACTIVATION; ENZYME STABILITY; FLAVONOIDS; HUMANS; KINETICS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PIPECOLIC ACIDS; QUANTITATIVE STRUCTURE-ACTIVITY RELATIONSHIP; THROMBIN;

EID: 33748768976     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2006.04.007     Document Type: Article

References (91)

1. Hornyak T.J., Bishop P.D., and Shafer J.A. Alpha-thrombin-catalyzed activation of human platelet factor XIII: relationship between proteolysis and factor XIIIa activity. Biochemistry 28 (1989) 7326-7332
2. Ganguly P. Interaction of thrombin with human platelets. Br. J. Haematol. 29 (1975) 617-626
3. Rosenberg R.D., and Damus P.S. The purification and mechanism of action of human antithrombin-heparin cofactor. J. Biol. Chem. 248 (1973) 6490-6505
4. Olson S.T., and Chuang Y.J. Heparin activates antithrombin anticoagulant function by generating new interaction sites (exosites) for blood clotting proteinases. Trends Cardiovasc. Med. 12 (2002) 331-338
5. Esmon C.T., Esmon N.L., and Harris K.W. Complex formation between thrombin and thrombomodulin inhibits both thrombin-catalyzed fibrin formation and factor V activation. J. Biol. Chem. 257 (1982) 7944-7947
6. Kaplan K.L. Direct thrombin inhibitors. Expert Opin. Pharmacother. 4 (2003) 653-666
7. Hogg P.J., and Bock P.E. Modulation of thrombin and heparin activities by fibrin. Thromb. Haemost. 77 (1997) 424-433
8. Weitz J.I., Hudoba M., Massel D., Maraganore J., and Hirsh J. Clot-bound thrombin is protected from inhibition by heparin-antithrombin III but is susceptible to inactivation by antithrombin III-independent inhibitors. J. Clin. Invest. 86 (1990) 385-391
9. Weitz J.I. Low-molecular-weight heparins. N. Engl. J. Med. 337 (1997) 688-698
10. Manach C., Scalbert A., Morand C., Remesy C., and Jimenez L. Polyphenols: food sources and bioavailability. Am. J. Clin. Nutr. 79 (2004) 727-747
11. Robbins C.T.H.T.A., Hagerman A.E., Hjeljord O., Baker D.L., and Schwartz C.C.M.W.W. Role of tannins in defending plants against ruminants: Reduction in protein availability. Ecology 68 (1987) 98-107
12. Allison S.D., and Schultz J.C. Biochemical responses of chestnut oak to a galling cynipid. J. Chem. Ecol. 31 (2005) 151-166
13. Choi C., Bareiss C., Walenciak O., and Gross E.M. Impact of polyphenols on growth of the aquatic herbivore Acentria ephemerella. J. Chem. Ecol. 28 (2002) 2245-2256
14. David J.P., Ferran A., Gambier J., and Meyran J.C. Taste sensitivity of detritivorous mosquito larvae to decomposed leaf litter. J. Chem. Ecol. 28 (2002) 983-995
15. David J.P., Tilquin M., Rey D., Ravanel P., and Meyran J.C. Mosquito larval consumption of toxic arborescent leaf-litter, and its biocontrol potential. Med. Vet. Entomol. 17 (2003) 151-157
16. Hashim M.S., and Devi K.S. Insecticidal action of the polyphenolic rich fractions from the stem bark of Streblus asper on Dysdercus cingulatus. Fitoterapia 74 (2003) 670-676
17. Melo G.A., Shimizu M.M., and Mazzafera P. Polyphenoloxidase activity in coffee leaves and its role in resistance against the coffee leaf miner and coffee leaf rust. Phytochemistry 67 (2006) 277-285
18. Islam F.M., Rengifo J., Redden R.J., Basford K.E., and Beebe S.E. Association between seed coat polyphenolics (tannins) and disease resistance in common bean. Plant Foods Hum. Nutr. 58 (2003) 285-297
19. Salunkhe D.K., Jadhav S.J., Kadam S.S., and Chavan J.K. Chemical, biochemical, and biological significance of polyphenols in cereals and legumes. Crit. Rev. Food Sci. Nutr. 17 (1982) 277-305
20. Harris H.B. B.R., Influence of tannin content on preharvest seed germination in sorghum. Agron. J. 62 (1970) 835-836
21. Harris H.B., and Burns R.E. Relationship between tannin content of sorghum and preharvest seed molding. Agron. J. 65 (1973) 957-959
22. Rozema J., Bjorn L.O., Bornman J.F., Gaberscik A., Hader D.P., Trost T., Germ M., Klisch M., Groniger A., Sinha R.P., Lebert M., He Y.Y., Buffoni-Hall R., de Bakker N.V., van de Staaij J., and Meijkamp B.B. The role of UV-B radiation in aquatic and terrestrial ecosystems-an experimental and functional analysis of the evolution of UV-absorbing compounds. J. Photochem. Photobiol. B 66 (2002) 2-12
23. Harborne J.B., and Simmonds N.W. The natural distribution of the phenolic aglycones. Biochemistry of Phenolic Compounds (1964), Academic Press, New York 77-127
24. Silva M.M., Santos M.R., Caroco G., Rocha R., Justino G., and Mira L. Structure-antioxidant activity relationships of flavonoids: a reexamination. Free Radic. Res. 36 (2002) 1219-1227
25. Paganga G., Miller N., and Rice-Evans C.A. The polyphenolic content of fruit and vegetables and their antioxidant activities. What does a serving constitute?. Free Radic. Res. 30 (1999) 153-162
26. Skrzydlewska E., Ostrowska J., Stankiewicz A., and Farbiszewski R. Green tea as a potent antioxidant in alcohol intoxication. Addict. Biol. 7 (2002) 307-314
27. Nie G., Wei T., Shen S., and Zhao B. Polyphenol protection of DNA against damage. Methods Enzymol. 335 (2001) 232-244
28. Kanakis C.D., Tarantilis P.A., Polissiou M.G., and Tajmir-Riahi H.A. Interaction of ntioxidant flavonoids with tRNA: intercalation or external binding and comparison with flavonoid-DNA adducts. DNA Cell Biol. 25 (2006) 116-123
29. Nakagawa T., Yokozawa T., Terasawa K., Shu S., and Juneja L.R. Protective activity of green tea against free radical- and glucose-mediated protein damage. J. Agric. Food Chem. 50 (2002) 2418-2422
30. Beretz A., and Cazenave J.P. Old and new natural products as the source of modern antithrombotic drugs. Planta Med. 57 (1991) S68-S72
31. Zhao X., Gu Z., Attele A.S., and Yuan C.S. Effects of quercetin on the release of endothelin, prostacyclin and tissue plasminogen activator from human endothelial cells in culture. J. Ethnopharmacol. 67 (1999) 279-285
32. Feldman K.S., Sambandam A., Lemon S.T., Nicewonger R.B., Long G.S., Battaglia D.F., Ensel S.M., and Laci M.A. Binding affinities of gallotannin analogs with bovine serum albumin: ramifications for polyphenol-protein molecular recognition. Phytochemistry 51 (1999) 867-872
33. Haslam E. Polyphenol-protein interactions. Biochem. J. 139 (1974) 285-288
34. Hatano T., Hori M., Hemingway R.W., and Yoshida T. Size exclusion chromatographic analysis of polyphenol-serum albumin complexes. Phytochemistry 63 (2003) 817-823
35. Jobstl E., O'Connell J., Fairclough J.P., and Williamson M.P. Molecular model for astringency produced by polyphenol/protein interactions. Biomacromolecules 5 (2004) 942-949
36. Richard T., Vitrac X., Merillon J.M., and Monti J.P. Role of peptide primary sequence in polyphenol-protein recognition: an example with neurotensin. Biochim. Biophys. Acta 1726 (2005) 238-243
37. Shanmuganayagam D., and Folts J. Effect of polyphenolic flavonoid compounds on platelets. Methods Enzymol. 335 (2001) 369-380
38. Gutzeit H.O., Henker Y., Kind B., and Franz A. Specific interactions of quercetin and other flavonoids with target proteins are revealed by elicited fluorescence. Biochem. Biophys. Res. Commun. 318 (2004) 490-495
39. Ermakova S., Choi B.Y., Choi H.S., Kang B.S., Bode A.M., and Dong Z. The intermediate filament protein vimentin is a new target for epigallocatechin gallate. J. Biol. Chem. 280 (2005) 16882-16890
40. Gaedeke J., Noble N.A., and Border W.A. Curcumin blocks fibrosis in anti-Thy 1 glomerulonephritis through up-regulation of heme oxygenase 1. Kidney Int. 68 (2005) 2042-2049
41. Gupta Y.K., Sharma M., and Briyal S. Antinociceptive effect of trans-resveratrol in rats: Involvement of an opioidergic mechanism. Methods Find. Exp. Clin. Pharmacol. 26 (2004) 667-672
42. Hung C.F., Huang T.F., Chiang H.S., and Wu W.B. (-)-Epigallocatechin-3-gallate, a polyphenolic compound from green tea, inhibits fibroblast adhesion and migration through multiple mechanisms. J. Cell. Biochem. 96 (2005) 183-197
43. Lee W.J., Shim J.Y., and Zhu B.T. Mechanisms for the inhibition of DNA methyltransferases by tea catechins and bioflavonoids. Mol. Pharmacol. 68 (2005) 1018-1030
44. Nifli A.P., Bosson-Kouame A., Papadopoulou N., Kogia C., Kampa M., Castagnino C., Stournaras C., Vercauteren J., and Castanas E. Monomeric and oligomeric flavanols are agonists of membrane androgen receptors. Exp. Cell Res. 309 (2005) 329-339
45. Palermo C.M., Westlake C.A., and Gasiewicz T.A. Epigallocatechin gallate inhibits aryl hydrocarbon receptor gene transcription through an indirect mechanism involving binding to a 90 kDa heat shock protein. Biochemistry 44 (2005) 5041-5052
46. Rimbach G., Saliou C., Canali R., and Virgili F. Interaction between cultured endothelial cells and macrophages: in vitro model for studying flavonoids in redox-dependent gene expression. Methods Enzymol. 335 (2001) 387-397
47. Saliou C., Valacchi G., and Rimbach G. Assessing bioflavonoids as regulators of NF-kappa B activity and inflammatory gene expression in mammalian cells. Methods Enzymol. 335 (2001) 380-387
48. Vitseva O., Varghese S., Chakrabarti S., Folts J.D., and Freedman J.E. Grape seed and skin extracts inhibit platelet function and release of reactive oxygen intermediates. J. Cardiovasc. Pharmacol. 46 (2005) 445-451
49. Wung B.S., Hsu M.C., Wu C.C., and Hsieh C.W. Resveratrol suppresses IL-6-induced ICAM-1 gene expression in endothelial cells: effects on the inhibition of STAT3 phosphorylation. Life Sci. 78 (2005) 389-397
50. Melzig M.F., Loser B., and Ciesielski S. Inhibition of neutrophil elastase activity by phenolic compounds from plants. Pharmazie 56 (2001) 967-970
51. Lupidi G., Angeletti M., Eleuteri A.M., Tacconi L., Coletta M., and Fioretti E. Peroxynitrite-mediated oxidation of fibrinogen inhibits clot formation. FEBS Lett. 462 (1999) 236-240
52. Bieth J.G. Some Kinetic Consequences of the Tight Binding of Protein-Proteinase-Inhibitors to Proteolytic Enzymes and Their Application to the Determination of Dissociation Constants. In: Fritz H., Tschesche H., Greene L.J., and Truscheit E. (Eds). Bayer-Symposium V "Proteinase Inhibitors" (1974), Springer-Verlag, Berlin 463-469
53. Davies R.J., Edwards P.R., Watts H.J., Lowe C.R., Buckle P.E., Yeung D., Kinning T.M., and Pollard-Knight D.V. Crabb (1994), J.W. Ed. ed., Academic Press, San Diego 285-292
54. Ayala Y., and Di Cera E. Molecular recognition by thrombin. Role of the slow->fast transition, site-specific ion binding energetics and thermodynamic mapping of structural components. J. Mol. Biol. 235 (1994) 733-746
55. + binding site of thrombin. J. Biol. Chem. 270 (1995) 22089-22092
56. Wells C.M., and Di Cera E. Thrombin is a Na (+)-activated enzyme. Biochemistry 31 (1992) 11721-11730
57. Hall D.R., and Winzor D.J. Use of a resonant mirror biosensor to characterize the interaction of carboxypeptidase A with an elicited monoclonal antibody. Anal. Biochem. 244 (1997) 152-160
58. Shi F., Winzor D.J., and Jackson C.M. Temperature dependence of the thrombin-catalyzed proteolysis of prothrombin. Biophys. Chem. 110 (2004) 1-13
59. Bevington, P.R., Data reduction and error analysis for the physical sciences, McGraw-Hill book company. 195-203.
60. De Crescenzo G., Grothe S., Zwaagstra J., Tsang M., and O'Connor-McCourt M.D. Real-time monitoring of the interactions of transforming growth factor-beta (TGF-beta) isoforms with latency-associated protein and the ectodomains of the TGF-beta type II and III receptors reveals different kinetic models and stoichiometries of binding. J. Biol. Chem. 276 (2001) 29632-29643
61. Roden L.D., and Myszka D.G. Global analysis of a macromolecular interaction measured on BIAcore. Biochem. Biophys. Res. Commun. 225 (1996) 1073-1077
62. Adema, E., Gebert, U., Roche Diagnostics, Tutzing, Germany.
63. Jim R.T. A study of the plasma thrombin time. J. Lab. Clin. Med. 50 (1957) 45-60
64. Triplett D.A. Coagulation and bleeding disorders: review and update. Clin. Chem. 46 (2000) 1260-1269
65. Krumrine J., Raubacher F., Brooijmans N., and Kuntz I. Principles and methods of docking and ligand design. In: Bourne E.P., and Wessig H. (Eds). Structural bioinformatics (2003), Wiley-Liss 443-476
66. MOE. Chemical computing (2001), Group Inc, Canada
67. Metropolis N., Rosenbluth A.W., Rosenbluth M.N., and Teller A.H. Equation of state calculations by fast computing machines. J. Chem. Phys. 21 (1953) 1087-1092
68. Halgren T.A. The Merck force Field. J. Comp. Chem. 17 (1996) 490
69. Bohm M., St Rzebecher J., and Klebe G. Three-dimensional quantitative structure-activity relationship analyses using comparative molecular field analysis and comparative molecular similarity indices analysis to elucidate selectivity differences of inhibitors binding to trypsin, thrombin, and factor Xa. J. Med. Chem. 42 (1999) 458-477
70. Hall L.H., and Kier L.B. The molecular connectivity Chi Indices and Kappa Shape Indices in structure-property modeling. Rev. Computational Chemistry 2 (1991)
71. Shrake A., and Rupley J.A. Environment and exposure to solvent of protein atoms. Lysozyme and insulin. J. Mol. Biol. 79 (1973) 351-371
72. Richards F.M. Areas, volumes, packing and protein structure. Annu. Rev. Biophys. Bioeng. 6 (1977) 151-176
73. Filizola M., Tasso S.M., Loew G.H., and Villar H.O. Global physicochemical properties as activity discriminants for the mGluR1 subtype of metabotropic glutamate receptors. J. Comput. Chem. 22 (2001) 2018-2027
74. Koehler K.A., and Magnusson S. The binding of proflavin to thrombin. Arch. Biochem. Biophys. 160 (1974) 175-184
75. Segel I.H. Enzyme kinetics: behavior and analysis of rapid equilibrium and steady-state enzyme systems (1993), John Wiley & sons (Inc.109-111)
76. Sonder S.A., and Fenton II J.W. Thrombin specificity with tripeptide chromogenic substrates: comparison of human and bovine thrombins with and without fibrinogen clotting activities. Clin. Chem. 32 (1986) 934-937
77. Antonini E., Ascenzi P., Menegatti E., and Guarneri M. Multiple intermediates in the reaction of bovine beta-trypsin with bovine pancreatic trypsin inhibitor (Kunitz). Biopolymers 22 (1983) 363-375
78. Okamoto S., Hijikata A., Kikumoto R., Tonomura S., Hara H., Ninomiya K., Maruyama A., Sugano M., and Tamao Y. Potent inhibition of thrombin by the newly synthesized arginine derivative No. 805. The importance of stereo-structure of its hydrophobic carboxamide portion. Biochem. Biophys. Res. Commun. 101 (1981) 440-446
79. Lakowics J.R. Quenching of fluorescence (1983), Principles of fluorescence spectroscopy 262-263
80. Antonini E., Ascenzi P., Bolognesi M., Menegatti E., and Guarneri M. Transient removal of proflavine inhibition of bovine beta-trypsin by the bovine basic pancreatic trypsin inhibitor (Kunitz). A case for "chronosteric effects". J. Biol. Chem. 258 (1983) 4676-4678
81. Dangles O., Dufour C., Manach C., Morand C., and Remesy C. Binding of flavonoids to plasma proteins. Methods Enzymol. 335 (2001) 319-333
82. Dufour C., and Dangles O. Flavonoid-serum albumin complexation: determination of binding constants and binding sites by fluorescence spectroscopy. Biochim. Biophys. Acta 1721 (2005) 164-173
83. Ray S., Bagchi D., Lim P.M., Bagchi M., Gross S.M., Kothari S.C., Preuss H.G., and Stohs S.J. Acute and long-term safety evaluation of a novel IH636 grape seed proanthocyanidin extract. Res. Commun. Mol. Pathol. Pharmacol. 109 (2001) 165-197
84. Yamakoshi J., Saito M., Kataoka S., and Kikuchi M. Safety evaluation of proanthocyanidin-rich extract from grape seeds. Food Chem. Toxicol. 40 (2002) 599-607
85. Ferguson L.R. Role of plant polyphenols in genomic stability. Mutat. Res. 475 (2001) 89-111
86. Scalbert A., and Williamson G. Dietary intake and bioavailability of polyphenols. J. Nutr. 130 (2000) 2073S-2085S
87. Conti E., Rivetti C., Wonacott A., and Brick P. X-ray and spectrophotometric studies of the binding of proflavin to the S1 specificity pocket of human alpha-thrombin. FEBS Lett. 425 (1998) 229-233
88. Banner D.W., and Hadvary P. Crystallographic analysis at 3.0-A resolution of the binding to human thrombin of four active site-directed inhibitors. J. Biol. Chem. 266 (1991) 20085-20093
89. Maffei Facino R., Carini M., Aldini G., Bombardelli E., Morazzoni P., and Morelli R. Free radicals scavenging action and anti-enzyme activities of procyanidines from Vitis vinifera. A mechanism for their capillary protective action. Arzneimittelforschung 44 (1994) 592-601
90. Bode W. X-ray crystal structures of thrombin in complex with D-Phe-Pro-Arg and with small benzamidine- and arginine-based "non-peptidic" inhibitors. Adv. Exp. Med. Biol. 340 (1993) 15-26
91. Bode W., Wei A.Z., Huber R., Meyer E., Travis J., and Neumann S. X-ray crystal structure of the complex of human leukocyte elastase (PMN elastase) and the third domain of the turkey ovomucoid inhibitor. EMBO J. 5 (1986) 2453-2458