Kinetics of the inhibition of bovine liver dihydrofolate reductase by tea catechins: Origin of slow-binding inhibition and pH studies

Biochemistry

Volumn 44, Issue 20, 2005, Pages 7512-7525

  Navarro Perán, Enma ^a   Cabezas Herrera, Juan ^b   Hiner, Alexander N P ^a   Sadunishvili, Tinatin ^c   García Cánovas, Francisco ^a   Rodríguez López, José Neptuno ^a  

^a UNIVERSITY OF MURCIA   (Spain)

^b HOSPITAL UNIVERSITARIO VIRGEN DE LA ARRIXACA   (Spain)

^c Durmishidze Institute of Biochemistry and Biotechnology   (Georgia)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; ENZYMES; FLUORESCENCE; IONIZATION; PH EFFECTS; PHYSIOLOGY; QUENCHING; TITRATION;

DIHYDROFOLATE REDUCTASE (DHFR); ENZYME-INHIBITOR COMPLEX; PROTONATED SPECIES;

BIOCHEMISTRY;

CATECHIN; DIHYDROFOLATE REDUCTASE; EPICATECHIN GALLATE; EPIGALLOCATECHIN GALLATE; POLYPHENOL; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG BINDING; ENZYME INHIBITION; FLUORESCENCE; FLUOROMETRY; IONIZATION; LIVER; NONHUMAN; PH; PHASE TRANSITION; PRIORITY JOURNAL; PROTON TRANSPORT; STEADY STATE; TEA; TITRIMETRY;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CAMELLIA SINENSIS; CATECHIN; CATTLE; FLAVONOIDS; FOLIC ACID ANTAGONISTS; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; LIVER; MODELS, CHEMICAL; MOLECULAR SEQUENCE DATA; PHENOLS; SPECTROMETRY, FLUORESCENCE; SPECTROPHOTOMETRY, ULTRAVIOLET; TEA; TETRAHYDROFOLATE DEHYDROGENASE;

BOVINAE;

EID: 18844383997     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050160t     Document Type: Article

References (45)

1. Lockshin, A., Moran, R. G., and Danenberg, P. V. (1979) Thymidylate synthetase purified to homogeneity from human leukemic cells, Proc. Natl. Acad. Sci. U.S.A. 76, 750-754.
2. Blakley, R. L. (1969) The Biochemistry of Folic Acid and Related Pteridines, Elsevier, New York.
3. Davies, J. F., II, Delcamp, T. J., Prendergast, N. J., Ashford, V. A., Freisheim, J. H., and Kraut, J. (1990) Crystal structures of recombinant human dihydrofolate reductase complexed with folate and 5-deazafolate, Biochemistry 29, 9467-9479.
4. Appleman, J. R., Beard, W. A., Delcamp, T. J., Prendergast, N. J., Freisheim, J. H., and Blakley, R. L. (1989) Atypical transient state kinetics of recombinant human dihydrofolate reductase produced by hysteretic behavior. Comparison with dihydrofolate reductases from other sources, J. Biol. Chem. 264, 2625-2633.
5. Lewis, W. S., Cody, V., Galitsky, N., Luft, J. R., Pangborn, W., Chunduru, S. K., Spencer, H. T., Appleman, J. R., and Blakley, R. L. (1995) Methotrexate-resistant variants of human dihydrofolate reductase with substitutions of leucine 22. Kinetics, crystallography, and potential as selectable markers, J. Biol Chem. 270, 5057-5064.
6. Schnell, J. R., Dyson, H. J., and Wright, P. E. (2004) Structure, dynamics, and catalytic function of dihydrofolate reductase, Annu. Rev. Biophys. Biomol. Struct. 33, 119-140.
7. Mukhtar, H., and Ahmad, N. (2000) Tea polyphenols: Prevention of cancer and optimizing health, Am. J. Clin. Nutr. 71, 1698S-1702S.
8. Fujiki, H., Sugunuma, M., Imai, K., and Nakachi, K. (2002) Green tea: Cancer preventive beverage and/or drug, Cancer Lett. 188, 9-13.
9. Mabe, K., Yamada, M., Oguni, I., and Takahashi, T. (1999) In vitro and in vivo activities of tea catechins against Helicobacter pylori, Antimicrob. Agents Chemother. 43, 1788-1791.
10. Hamilton-Miller, J. M. T. (2001) Anti-cariogenic properties of tea (Camellia sinensis), J. Med. Microbiol. 50, 299-302.
11. Yam, T. S., Hamilton-Miller, J. M. T., and Shah, S. (1998) The effect of a component of tea (Camellia sinensis) on methicillin resistance, PBP2′ synthesis, and β-lactamase production in Staphylococcus aureus, J. Antimicrob. Chemother. 42, 211-216.
12. Jung, Y. D., and Ellis, L. M. (2001) Inhibition of tumour invasion and angiogenesis by epigallocatechin gallate (EGCG), a major component of green tea, Int. J. Exp. Pathol. 82, 309-316.
13. Gupta, S., Hussain, T., and Makhtar, H. (2003) Molecular pathway for (-)-epigallocatechin-3-gallate-induced cell arrest and apoptosis of human prostate carcinoma cells, Arch. Biochem. Biophys. 410, 177-185.
14. Yang, G. Y., Liao, J., Kim, K., Yurkow, E. J., and Yang, C. S. (1998) Inhibition of growth and induction of apoptosis in human cancer cell lines by tea polyphenols, Carcinogenesis 19, 611-616.
15. Navarro-Perán, E., Cabezas-Herrera, J., García- Cánovas, F., Durrant, M. C., Thorneley, R. N. F., and Rodríguez-López, J. N. (2005) The antifolate activity of tea catechins, Cancer Res. 65, 2059-2064.
16. Navarro-Perán, E., Cabezas-Herrera, J., and Rodríguez- López, J. N. (2004) GB Patent 0419181.3.
17. Williams, J. W., Morrison, J. F., and Duggleby, R. G. (1979) Methotrexate, a high-affinity pseudosubstrate of dihydrofolate reductase, Biochemistry 18, 2567-2573.
18. Stone, S. R., and Morrison, J. F. (1982) Kinetic mechanism of the reaction catalyzed by dihydrofolate reductase from Escherichia coli, Biochemistry 21, 3757-3765.
19. Cornish-Bowden, A. (1979) in Fundamentals of Enzyme Kinetics, pp 34-37, Butterworth and Co., London.
20. Marquardt, D. W. (1963) An algorithm for least-squares estimation of nonlinear parameters, J. Soc. Ind. Appl. Math. 11, 431-441.
21. Jandel Scientific (1994) Sigma Plot 2.01 for Windows, Jandel Scientific, Corte Madera, CA.
22. García-Sevilla, F., Garrido del Solo, C., Duggleby, R. G., García-Cánovas, F., Peyro-García, R., and Varón, R. (2000) Use of a windows program for simulation of the progress curves of reactants and intermediates involved in enzyme-catalyzed reactions, BioSystems 54, 151-164.
23. Stone, S. R., and Morrison, J. F. (1986) Mechanism of inhibition of dihydrofolate reductases from bacterial and vertebrate sources by various classes of folate analogues, Biochim. Biophys. Acta 869, 275-285.
24. Williams, E. A., and Morrison, J. F. (1992) Human dihydrofolate reductase: Reduction of alternative substrates, pH effects, and inhibition by deazafolates, Biochemistry 31, 6801-6811.
25. Dunn, S. M. J., and King, R. W. (1980) Kinetics of ternary complex formation between dihydrofolate reductase, coenzyme, and inhibitors, Biochemistry 19, 766-773.
26. Andrews, J., Fierke, C. A., Birdsall, B., Ostler, G., Feeney, J., Roberts, G. C. K., and Benkovic, S. J. (1989) A kinetic study of wild-type and mutant dihydrofolate reductases from Lactobacillus casei, Biochemistry 28, 5743-5750.
27. Navarro-Martínez, M. D., Navarro-Perán, E., Cabezas-Herrera, J., Ruiz-Gómez, J., García-Cánovas, F., and Rodríguez-López, J. N. (2005) Antifolate activity of epigallocatechin gallate against Stenotrophomonas maltophilia. Antimicrob. Agents Chemother. (in press).
28. Birdsall, B., Burgen, A. S. V., and Roberts, G. C. K. (1980) Binding of coenzyme analogues to Lactobacillus casei dihydrofolate reductase: Binary and ternary complexes, Biochemistry 19, 3723-3731.
29. Cayley, P. J., Dunn, S. M. J., and King, R. W. (1981) Kinetics of substrate, coenzyme, and inhibitor binding to Escherichia coli dihydrofolate reductase, Biochemistry 20, 874-879.
30. Rajagopalan, P. T. R., Zhang, Z., McCourt, L., Dwyer, M., Benkovic, S. J., and Hammes, G. G. (2002) Interaction of dihydrofolate reductase with methotrexate: Ensemble and single-molecule kinetics, Proc. Natl. Acad. Sci. U.S.A. 99, 13481-13486.
31. Golicnik, M., and Stojan, J. (2004) Slow-binding inhibition: A theoretical and practical course for students, Biochem. Mol. Biol. Educ. 32, 228-235.
32. Hirasawa, M., and Takada, K. (2004) Multiple effects of green tea catechin on the antifungal activity of antimycotics against Candida albicans, J. Antimicrob. Chemother. 53, 225-229.
33. Cocco, L., Roth, B., Temple, C., Montgomery, J. A., London, R. E., and Blakley, R. L. (1983) Protonated state of methotrexate, trimethoprim, and pyrimethamine bound to dihydrofolate reductase, Arch. Biochem. Biophys. 226, 567-577.
34. Nam, S., Smith, D. M., and Dou, Q. P. (2001) Ester bond-containing tea polyphenols potently inhibit proteasome activity in vitro and in vivo, J. Biol. Chem. 276, 13322-13330.
35. Fang, M. Z., Wang, Y., Ai, N., Hou, Z., Sun, Y., Lu, H., Welsh, W., and Yang C. S. (2003) Tea polyphenol (-)-epigallocatechin-3-gallate inhibits DNA methyltransferase and reactivates methylation-silenced genes in cancer cell lines, Cancer Res. 63, 7563-7570.
36. Stone, S. R., and Morrison, J. F. (1983) The pH dependence of the binding of dihydrofolate and substrate analogues to dihydrofolate reductase from Escherichia coli, Biochim. Biophys. Acta 745, 247-258.
37. Kobayashi, K., Terada, C., and Tsukamoto, I. (2002) Methotrexate-induced apoptosis in hepatocytes after partial hepatectomy, Eur. J. Pharmacol. 438, 19-24.
38. Yang, C. S. (1997) Inhibition of carcinogenesis by tea, Nature 389, 134-135.
39. + and biopterin, Biochemistry 31, 7264-7273.
40. Schweitzer, B. J., Srimatkandada, S., Gritsman, H., Sheridan, R., Venkataraghavan, R., and Bertino, J. R. (1989) Probing the role of two hydrophobic active site residues in the human dihydrofolate reductase by site-directed mutagenesis, J. Biol. Chem. 264, 20786-20795.
41. Rowe, P. B., and Russel, P. J. (1973) Dihydrofolate reductase. Studies on the activation of the bovine liver enzyme, J. Biol. Chem. 248, 984-991.
42. Thompson, P. D., and Freisheim, J. H. (1991) Conversion of arginine to lysine at position 70 of human dihydrofolate reductase: Generation of a methotrexate-insensitive mutant enzyme, Biochemistry 30, 8124-8130.
43. Webb, S. D., Sherratt, J. A., and Fish, R. G. (1999) Mathematical modelling of tumour acidity: Regulation of intracellular pH, J. Theor. Biol. 196, 237-250.
44. Heydendael, V. M. R., Spuls, P. I., Opmeer, B. C., de Borgie, C. A., Reitsma, J. B., Goldschmidt, W. F., Bossuyt, P. M., Bos, J. D., and de Rie, M. A. (2003) Methotrexate versus cyclosporine in moderate-to-severe chronic plaque psoriasis, N. Engl. J. Med. 349, 658-665.
45. Correa, A., Stolley, A., and Liu, Y. (2000) Prenatal tea consumption and risk of anencephaly and spina bifida, Ann. Epidemiol. 10, 476-477.