Thymidylate synthase catalyzed H-transfers: Two chapters in one tale

Journal of the American Chemical Society

Volumn 132, Issue 28, 2010, Pages 9820-9825

  Wang, Zhen ^a   Kohen, Amnon ^a  

^a E11 SSH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BOND ACTIVATION; C-H BOND CLEAVAGE; CHEMICAL TRANSFORMATIONS; COMPLEX REACTIONS; DONOR-ACCEPTORS; ENZYMATIC REACTION; HYDRIDE TRANSFERS; INTRINSIC KINETICS; OVERALL RATE; PHYSICAL NATURE; RATE LIMITING; TEMPERATURE DEPENDENT; THYMIDYLATE SYNTHASE;

CHEMICAL BONDS; ISOTOPES;

PROTON TRANSFER;

THYMIDYLATE SYNTHASE;

ARTICLE; CATALYST; CHEMICAL REACTION; CHEMICAL STRUCTURE; ENZYME MECHANISM; GEOMETRY; HYDROGEN BOND; KINETICS; PROTON TRANSPORT; TEMPERATURE;

BIOCATALYSIS; HYDROGEN BONDING; KINETICS; THYMIDYLATE SYNTHASE;

EID: 77954637249     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/ja103010b     Document Type: Article

References (58)

1. Boehr, D. D., McElheny, D., Dyson, H. J., and Wright, P. E. Science 2006, 313, 1638-1642
2. Henzler-Wildman, K. and Kern, D. Nature 2007, 450, 964-972
3. Henzler-Wildman, K. A., Lei, M., Thai, V., Kerns, S. J., Karplus, M., and Kern, D. Nature 2007, 450, 913-916
4. Henzler-Wildman, K. A., Thai, V., Lei, M., Ott, M., Wolf-Watz, M., Fenn, T., Pozharski, E., Wilson, M. A., Petsko, G. A., Karplus, M., Hubner, C. G., and Kern, D. Nature 2007, 450, 838-844
5. Fraser, J. S., Clarkson, M. W., Degnan, S. C., Erion, R., Kern, D., and Alber, T. Nature 2009, 462, 669-673
6. Allemann, R. K., Evans, R. M., and Loveridge, E. J. Biochem. Soc. Trans. 2009, 37, 349-353
7. Benkovic, S. J. and Hammes-Schiffer, S. Science 2003, 301, 1196-1202
8. Boehr, D. D., Dyson, H. J., and Wright, P. E. Biochemistry 2008, 47, 9227-9233
9. Cui, Q. and Karplus, M. J. Phys. Chem. B 2002, 106, 7927-7947
10. Hammes-Schiffer, S. Acc. Chem. Res. 2006, 39, 93-100
11. Kohen, A. Hydrogen-Transfer Reactions; Hynes, J. T., Klinman, J. P., Limbach, H.-H., and Schowen, R. L., Eds.; Wiley VCH: Weinheim, 2007; Vol. 4, pp 1311 - 1340.
12. Nagel, Z. D. and Klinman, J. P. Nat. Chem. Biol. 2009, 5, 543-550
13. Schramm, V. L. Arch. Biochem. Biophys. 2005, 433, 13-26
14. Sutcliffe, M. J., Masgrau, L., Roujeinikova, A., Johannissen, L. O., Hothi, P., Basran, J., Ranaghan, K. E., Mulholland, A. J., Leys, D., and Scrutton, N. S. Philos. Trans. R. Soc. B, Biol. Sci. 2006, 361, 1375-1386
15. Kiefer, P. M. and Hynes, J. T. Isotope effects in chemistry and biology; Kohen, A. and Limbach, H. H., Eds.; Taylor & Francis, CRC Press: Boca Raton, FL, 2006; Vol. Ch. 21, pp 549 - 578.
16. Knapp, M. J., Meyer, M., and Klinman, J. P. Hydrogen-Transfer Reactions; Hynes, J. T., Klinman, J. P., Limbach, H.-H., and Schowen, R. L., Eds.; Wiley-VCH Verlag GmbH & Co. KGaA: New York, 2007; pp 1241 - 1284.
17. Schwartz, S. D. Isotope effects in chemistry and biology; Kohen, A. and Limbach, H. H., Eds.; Taylor & Francis, CRC Press: Boca Raton, FL, 2006; Vol. Ch. 18, pp 475 - 498.
18. Truhlar, D. G. Isotope effects in chemistry and biology; Kohen, A. and Limbach, H. H., Eds.; Taylor & Francis, CRC Press: Boca Raton, FL, 2006; Vol. Ch. 22, pp 579 - 620.
19. Warshel, A., Olsson, M. H. M., and Villá-Freixa, J. Isotope effects in chemistry and biology; Kohen, A. and Limbach, H. H., Eds.; Taylor & Francis: CRC Press: Boca Raton, FL, 2006; Vol. Ch. 23, pp 621 - 644.
20. Marcus, R. A. J. Phys. Chem. B 2007, 111, 6643-6654
21. Marcus, R. A. J. Chem. Phys. 2006, 125, 194504
22. Bell, R. P. The tunnel effect in chemistry; NY: Chapman & Hall.: London, UK and New York, 1980.
23. Pu, J., Gao, J., and Truhlar, D. G. Chem. Rev. 2006, 106, 3140-3169
24. Marcus, R. A. and Sutin, N. Biochim. Biophys. Acta 1985, 811, 265-322
25. The DHA coordinate usually includes tens of atoms, as D and A represent all atoms directly involved in the H-transfer, rather than just the donor atom and acceptor atom of hydrogen.
26. 1 in Figure 1). This has been discussed in more detail in ref 12.
27. Roston, D. and Kohen, A. Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 9572-9577
28. Bandaria, J. N., Cheatum, C. M., and Kohen, A. J. Am. Chem. Soc. 2009, 131, 10151-10155
29. Bandaria, J. N., Dutta, S., Hill, S. E., Kohen, A., and Cheatum, C. M. J. Am. Chem. Soc. 2008, 130, 22-23
30. Carreras, C. W. and Santi, D. V. Annu. Rev. Biochem. 1995, 64, 721-762
31. Stroud, R. M. and Finer-Moore, J. S. Biochemistry 2003, 42, 239-247
32. Agrawal, N., Hong, B., Mihai, C., and Kohen, A. Biochemistry 2004, 43, 1998-2006
33. Hong, B., Haddad, M., Maley, F., Jensen, J. H., and Kohen, A. J. Am. Chem. Soc. 2006, 128, 5636-5637
34. Hong, B., Maley, F., and Kohen, A. Biochemistry 2007, 46, 14188-14197
35. Kanaan, N., Martí, S., Moliner, V., and Kohen, A. Biochemistry 2007, 46, 3704-3713
36. Kanaan, N., Marti, S., Moliner, V., and Kohen, A. J. Phys. Chem. A 2009, 113, 2176-2181
37. 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. Biochemistry 2006, 45, 7415-7428
38. Spencer, H. T., Villafranca, J. E., and Appleman, J. R. Biochemistry 1997, 36, 4212-4222
39. Basran, J., Harris, R. J., Sutcliffe, M. J., and Scrutton, N. S. J. Biol. Chem. 2003, 278, 43973-43982
40. Heyes, D. J., Sakuma, M., de Visser, S. P., and Scrutton, N. S. J. Biol. Chem. 2009, 284, 3762-3767
41. Finer-Moore, J. S., Santi, D. V., and Stroud, R. M. Biochemistry 2003, 42, 248-256
42. Cook, P. F. and Cleland, W. W. Enzyme Kinetics and Mechanism; Garland Science: London; New York, 2007; pp 253 - 324.
43. Northrop, D. B. Enzyme mechanism from isotope effects; Cook, P. F., Ed.; CRC Press: Boca Raton, FL, 1991; pp 181 - 202.
44. +).
45. Melander, L. and Saunders, W. H. Reaction rates of isotopic molecules, 4th ed.; Krieger, R. E: Malabar, FL, 1987.
46. Edwards, S. J., Soudackov, A. V., and Hammes-Schiffer, S. J. Phys. Chem. A 2009, 113, 2117-2126
47. Liu, H. and Warshel, A. J. Phys. Chem. B 2007, 111, 7852-7861
48. Meyer, M. P. and Klinman, J. P. Chem. Phys. 2005, 319, 283-296
49. Pu, J., Ma, S., Gao, J., and Truhlar, D. G. J. Phys. Chem. B 2005, 109, 8551-8556
50. Truhlar, D. G. J. Phys. Org. Chem. 2010, in press (available as Early View online).
51. Kohen, A., Cannio, R., Bartolucci, S., and Klinman, J. P. Nature 1999, 399, 496-499
52. Sikorski, R. S., Wang, L., Markham, K. A., Rajagopalan, P. T., Benkovic, S. J., and Kohen, A. J. Am. Chem. Soc. 2004, 126, 4778-4779
53. Wang, L., Goodey, N. M., Benkovic, S. J., and Kohen, A. Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 15753-15758
54. As a disclaimer to the proposed theme, we wish to point out that the generality of this phenomenon is not yet clear, as only a limited number of enzymes have been studied at this level. Some recent studies have reported temperature-dependent KIEs for the presumed natural substrate under hypothesized physiological conditions [refs 39 and 40 ] and temperature-independent KIEs with one substrate compared with temperature-dependent KIEs with a 15× faster substrate [Pudney et al. J. Am. Chem. Soc. 2009, 131, 17072-17073]. Furthermore, it is not always easy to ensure that the natrual substrates and physiological conditions in vivo are used for the experiments and that the intrinsic KIEs have been fully extracted. Finally, one has to bear in mind that enzymes may not evolve to make the chemical reaction as fast as possible, but to best fit the metabolic needs of the organism.
55. Changchien, L.-M., Garibian, A., Frasca, V., Lobo, A., Maley, G. F., and Maley, F. Protein Express. Purif. 2000, 19, 265-270
56. Hayatsu, H., Wataya, Y., Kai, K., and Iida, S. Biochemistry 1970, 9, 2858-2865
57. Wataya, Y., Hayatsu, H., and Kawazoe, Y. J. Am. Chem. Soc. 1972, 94, 8927-8928
58. Wataya, Y. and Hayatsu, H. Biochemistry 1972, 11, 3583-3588