Role of Y94 in proton and hydride transfers catalyzed by thymidylate synthase

Biochemistry

Volumn 46, Issue 49, 2007, Pages 14188-14197

  Hong, Baoyu ^a,c   Maley, Frank ^b   Kohen, Amnon ^a  

^a E11 SSH   (United States)

^b WADSWORTH CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; CARBON; CATALYST ACTIVITY; DNA; ESCHERICHIA COLI; HYDRIDES; PROTONS;

CARBON-BOUND PROTON; HYDRIDE TRANSFERS; THYMIDYLATE SYNTHASE; URACIL BASE;

ENZYMES;

ISOTOPE; PROTON; THYMIDYLATE SYNTHASE; TYROSINE;

ARTICLE; CATALYSIS; CHEMICAL STRUCTURE; ENZYME MECHANISM; HYDROGEN BOND; KINETICS; NONHUMAN; PRIORITY JOURNAL; SYNTHESIS; TEMPERATURE;

AMINO ACID SEQUENCE; HYDROGEN; KINETICS; PROTONS; TETRAHYDROFOLATES; THYMIDYLATE SYNTHASE; TYROSINE;

ESCHERICHIA COLI; LACTOBACILLUS CASEI;

EID: 37149004947     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701363s     Document Type: Article

References (53)

1. Carreras, C. W., and Santi, D. V. (1995) The catalytic mechanism and structure of thymidylate synthase, Annu. Rev. Biochem. 64, 721-762.
2. Phan, J., Steadman, D. J., Koli, S., Ding, W. C., Minor, W., Dunlap, R. B., Berger, S. H., and Lebioda, L. (2001) Structure of human thymidylate synthase suggests advantages of chemotherapy with noncompetitive inhibitors, J. Biol. Chem. 276, 14170-14177.
3. Sergeeva, O. A., Khambatta, H. G., Cathers, B. E., and Sergeeva, M. V. (2003) Kinetic properties of human thymidylate synthase, an anticancer drug target, Biochem. Biophys. Res. Commun. 307, 297-300.
4. Finer-Moore, J. S., Santi, D. V., and Stroud, R. M. (2003) Lessons and conclusions from dissecting the mechanism of a bisubstrate enzyme: Thymidylate synthase mutagenesis, function, and structure, Biochemistry 42, 248-256.
5. Stroud, R. M., and Finer-Moore, J. S. (2003) Conformational dynamics along an enzymatic reaction pathway: Thymidyate synthase, "the movie", Biochemistry 42, 239-247.
6. Saxl, R. L., Reston, J., Nie, Z., Kaiman, T. I., and Maley, F. (2003) Modification of Escherichia coli thymidylate synthase at tyrosine-94 by 5-imidazolylpropynyl-2′-deoxyuridine 5′-monophosphate, Biochemistry 42, 4544-4551.
7. Maley, F., Pedersen-Lane, J., and Changchien, L. (1995) Complete restoration of activity to inactive mutants of Escherichia coli thymidylate synthase: Evidence that E. coli thymidylate synthase is a half-the-sites activity enzyme, Biochemistry 34, 1469-1474.
8. Saxl, R. L., Changchien, L.-M., Hardy, L. W., and Maley, F. (2001) Parameters affecting the restoration of activity to inactive mutants of thymidylate synthase via subunit exchange: Further evidence that thymidylate synthase is a half-of-the-sites activity enzyme, Biochemistry 40, 5275-5282.
9. Lorenson, M. Y., Maley, G. F., and Maley, F. (1967) The purification and properties of thymidylate synthetase from chick embryo extracts, J. Biol. Chem. 242, 3332-3344.
10. Agrawal. N., Hong, B., Mihai, C., and Kohen, A. (2004) Vibrationally enhanced hydrogen tunneling in the E. coli thymidylate synthase catalyzed reaction, Biochemistry 43, 1998-2006.
11. Newby, Z., Lee, T. T., Morse, R. J., Liu, Y., Liu, L., Venkatraman, P., Santi, D. V., Finer-Moore, J. S., and Stroud, R. M. (2006) The role of protein dynamics in thymidylate synthase catalysis: Variants of conserved 2′-deoxyuridine 5′-monophosphate (dUMP)-binding Tyr-261, Biochemistry 45, 7415-7428.
12. Phan, J., Mahdavian, E., Nivens, M. C., Minor, W., Berger, S., Spencer, H. T., Dunlap, R. B., and Lebioda, L. (2000) Catalytic cysteine of thymidylate synthase is activated upon substrate binding, Biochemistry 39, 6969-6978.
13. Hyatt, D. C., Maley, F., and Monfort, W. R. (1997) Use of strain in a stereospecific catalytic mechanism: Crystal structures of Escherichia coli thymidylate synthase bound to FdUMP and methylenetetrahydrofolate, Biochemistry 36, 4585-4594.
14. Spencer, H. T., Villafranca, J. E., and Appleman, J. R. (1997) Kinetic scheme for thymidylate synthase from Escherichia coli: Determination from measurements of ligand binding, primary and secondary isotope effects and pre-steady-state catalysis, Biochemistry 36, 4212-4222.
15. Hong, B., Haddad, M., Maley, F., Jensen, J. H., and Kohen, A. (2006) Hydride transfer versus hydrogen radical transfer in thymidylate synthase, J. Am. Chem. Soc. 128, 5636-5637.
16. Kanaan, N., Marti, S., Moliner, V., and Kohen, A. (2007) A quantum mechanics/molecular mechanics study of the catalytic mechanism of the thymidylate synthase, Biochemistry 46, 3704-3713.
17. Matthews, D. A., Villafranca, J. E., Janson, C. A., Smith, W. W., Welsh, K., and Freer, S. (1990) Stereochemical mechanism of action for thymidylate synthase based on the X-ray structure of the covalent inhibitory ternary complex with 5-fluoro-2′-deoxyuridylate and 5,10-methylenetetrahydrofolate, J. Mol. Biol. 214, 937-948.
18. Fauman, E. B., Rutenber, E. E., Maley, G. F., Maley, F., and Stroud, R. M. (1994) Water-mediated substrate/product discrimination: The product complex of thymidylate synthase at 1.83 Å, Biochemistry 33, 1502-1511.
19. Liu, Y., Barrett, J. E., Schultz, P. G., and Santi, D. V. (1999) Tyrosine 146 of thymidylate synthase assists proton abstraction from the 5-position of 2′-deoxyuridine 5′-monophosphate, Biochemistry 38, 848-852.
20. Hardy, L. W., Graves, K. L., and Nalivaika, E. (1995) Electrostatic guidance of catalysis by a conserved glutamic acid in Escherichia coli dTMP synthase and bacteriophage T4 dCMP hydroxymethylase, Biochemistry 34, 8422-8432.
21. Cook, P. F. (1991) in Enzyme mechanism from isotope effects (Cook, P. F., Ed.) pp 203-230, CRC Press, Boca Raton, FL.
22. 3H]-2′- deoxyuridylate for protons of water, Biochemistry 18, 2794-2798.
23. Carreras, C. W., Climie, S. C., and Santi, D. V. (1992) Thymidylate synthase with a C-terminal deletion catalyzes partial reactions but is unable to catalyze thymidylate formation, Biochemistry 31, 6038-6044.
24. Huang, W., and Santi, D. V. (1994) Isolation of a covalent steady-state intermediate in glutamate 60 mutants of thymidylate synthase, J. Biol. Chem. 269, 31327-31329.
25. Northrop, D. B. (1975) Steady-state analysis of kinetic isotope effects in enzymatic reactions, Biochemistry 14, 2644-2651.
26. Northrop, D. B. (1977) in Isotope effects on enzyme-catalyzed reactions (Cleland, W. W., O'Leary, M. H., and Northrop, D. B., Eds.) pp 122-152, University Park Press, Baltimore.
27. Northrop, D. B. (1991) Intrinsic isotope effects in enzyme catalyzed reactions, in Enzyme mechanism from isotope effects (Cook, P. F., Ed.) pp 181-202, CRC Press, Boca Raton, FL.
28. Cleland, W. W. (2006) Enzyme mechanisms from isotope effects, in Isotope effects in chemistry and biology (Kohen, A., and Limbach, H. H., Eds.) pp 915-930, Taylor & Francis, CRC Press, Boca Raton, FL.
29. Blakley, R. L. (1960) Crystalline dihydropteroylglutamic acid, Nature 188, 231-232.
30. xH]-N5,N10-methylene 5,6,7,8-tetrahydrofolate as a substrate for thymidylate synthase, Anal. Biochem. 328, 44-50.
31. Hayatsu, H., Wataya, Y., Kai, K., and Iida, S. (1970) Reaction of sodium bisulfite with uracil, cytosine, and their derivatives, Biochemistry 9, 2858-2865.
32. Wataya, Y., and Hayatsu, H. (1972) Cysteine-catalyzed hydrogen isotope exchange at the 5 position of uridylic acid, J. Am. Chem. Soc. 94, 8927-8928.
33. Wataya, Y., and Hayatsu, H. (1972) Effects of amine on the bisulfite-catalyzed hydrogen isotope exchange at the 5 position of uridine, Biochemistry 11, 3583-3588.
34. Changchien, L.-M., Garibian, A., Frasca, V., Lobo, A., Maley, G. F., and Maley, F. (2000) High-level expression of Escherichia coli and Bacillus subtilis thymidylate synthase, Protein Expression Purif. 19, 265-270.
35. Melander, L., and Saunders, W. H. (1987) Reaction rates of isotopic molecules, 4th ed., Krieger, R. E., Malabar, FL.
36. Wang, L., Tharp, S., Selzer, T., Benkovic, S. J., and Kohen, A. (2006) Effects of a distal mutation on active site chemistry, Biochemistry 45, 1383-1392.
37. Cleland, W. W. (1980) Measurement of isotope effects by the equilibrium perturbation technique, Methods Enzymol. 64, 104-125.
38. Roberts, S. A., Hyatt, D. C., Honts, J. E., Changchien, L., Maley, G. F., Maley, F., and Montfort, W. R. (2006) Structure of the Y94F mutant of Escherichia coli thymidylate synthase, Acta Crystallogr. F62, 840-843.
39. Klinman, J. P., Humphriesg, H., and Voe, J. G. (1980) Deduction cf kinetic mechanism in multisubstrate enzyme reactions from tritium isotope effects, J. Biol. Chem. 255, 11648-11651.
40. Cook, P. F., and Cleland, W. W. (1981) Mechanistic deductions from isotope effects in multireactant enzyme mechanisms, Biochemistry 20, 1790-1796.
41. Cleland, W. W. (1987) Secondary isotope effectson enzymatic reactions, in Isotopes in organic chemistry (Buncel, E., and Lee, C. C., Eds.) pp 61-113, Elsevier, Amsterdam.
42. Kohen, A., Cannio, R., Bartolucci, S., and Klinman, J. P. (1999) Enzyme dynamics and hydrogen tunneling in a thermophilic alcohol dehydrogenase, Nature 399, 496-499.
43. Maglia, G., and Allemann, R. K. (2003) Evidence for environmentally coupled hydrogen tunneling during dihydrofolate reductase catalysis, J. Am. Chem. Soc. 125, 13372-13373.
44. Stern, M. J., and Weston, R. E. J. (1974) Phenomenological manifestations of quantum-mechanical tunneling. II. Effect on Arrhenius pre-exponential factors for primary hydrogen kinetic isotope effects, J. Chem. Phys. 60, 2808-2814.
45. Bell, R. P. (1980) The tunnel effect in chemistry, Chapman & Hall, New York,.
46. Kohen, A. (2006) Kinetic isotope effects as probes for hydrogen tunneling in enzyme catalysis, in Isotope Effects in Chemistry and Biology (Kohen, A., and Limbach, H. H., Eds.) pp 743-764, Taylor & Francis, CRC Press, Boca Raton, FL.
47. Francisco, W. A., Knapp, M. J., Blackburn, N. J., and Klinman, J. P. (2002) Hydrogen tunneling in peptidylglycine α-hydroxylation monooxygenase, J. Am. Chem. Soc. 124, 8194-8195.
48. Miller, S. M., and Klinman, J. P. (1985) Secondary isotope effects and structure-reactivity correlations in the dopamine β-monooxygenase reaction: Evidence for a chemical mechanism, Biochemistry 24, 2114-2127.
49. Knapp, M. J., and Klinman, J. P. (2002) Environmentally coupled hydrogen tunneling linking catalysis to dynamics, Eur. J. Biochem. 269, 3113-3121.
50. Nagel, Z. D., and Klinman, J. P. (2006) Tunneling and dynamics in enzymatic hydride transfer, Chem. Rev. 106, 3095-3118.
51. Wang, L., Goodey, N. M., Benkovic, S. J., and Kohen, A. (2006) Coordinated Effects of Distal Mutations on Environmentally Coupled Tunneling in Dihydrofolate Reductase, Proc. Natl. Acad. Sci. U.S.A. 103, 15753-15758.
52. Marcus, R. A. (2007) H and other transfers in enzymes and in solution: Theory and computations, a unified view. 2. Applications to experiment and computations, J. Phys. Chem. B 111, 6643-6654.
53. Kohen, A. (2003) Kinetic isotope effects as probes for hydrogen tunneling, coupled motion and dynamics contributions to enzyme catalysis, Prog. React. Kinet. Mech. 28, 119-156.