Environmental effects on phosphoryl group bonding probed by vibrational spectroscopy: Implications for understanding phosphoryl transfer and enzymatic catalysis

Journal of the American Chemical Society

Volumn 124, Issue 38, 2002, Pages 11295-11306

  Cheng, Hu ^a,d   Nikolic Hughes, Ivana ^b   Wang, Jianghua H ^a,e   Deng, Hua ^a   O'Brien, Patrick J ^a,f   Wu, Li ^a   Zhang, Zhong Yin ^a   Herschlag, Daniel ^b,c   Callender, Robert ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b Stanford University   (United States)

^c STANFORD UNIVERSITY   (United States)

^d YALE UNIVERSITY   (United States)

^e Marubeni America Corporation   (United States)

^f HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL SUBSTRATES;

ALCOHOLS; BONDING; CATALYSIS; ELECTROSTATICS; ENZYMES; SPECTROSCOPY;

PHOSPHORUS;

PHOSPHATE; PHOSPHORUS DERIVATIVE;

ARTICLE; CATALYSIS; CHEMICAL BOND; COVALENT BOND; DRUG ISOLATION; ENZYME PHOSPHORYLATION; LINEAR SYSTEM; STRUCTURE ANALYSIS;

BINDING SITES; CATALYSIS; DIMETHYL SULFOXIDE; ENZYMES; PHOSPHORIC ACID ESTERS; SPECTROPHOTOMETRY, INFRARED; SPECTRUM ANALYSIS, RAMAN; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS; WATER;

EID: 0037174379     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja026481z     Document Type: Article

References (78)

1. (a) Plapp, B. V. Methods Enzymol. 1995, 249, 91.
2. (b) Gerlt, J. A. Chem. Rev. 1987, 87, 1079.
3. (a) Muller, Y. A.; Schulz, G. E. Science 1993, 259, 965.
4. (b) Anderson, A. C.; Perry, K. M.; Freymann, D. M.; Stroud, R. M. J. Mol. Biol. 2000, 297, 645.
5. (c) Zechel, D. L.; Withers, S. G. Acc. Chem. Res. 2000, 33, 11.
6. (d) Schlichting, I.; Berendzen, J.; Chu, K.; Stock, A. M.; Maves, S. A.; Benson, D. E.; Sweet, B. M.; Ringe, D.; Petsko, G. A.; Sligar, S. G. Science 2000, 287, 1615.
7. (a) Pauling, L. Chem. Eng. News 1946, 24, 1375.
8. (b) Warshel, A. J. Biol. Chem. 1998, 273, 27035.
9. (c) Jencks, W. P. Catalysis in Chemistry and Enzymology; McGraw-Hill: New York, 1969.
10. Fersht, A. Enzyme structure and mechanism; W. H. Freeman & Co.; New York, 1977.
11. (e) Bruice, T. C.; Benkovic, S. J. Biochemistry 2000, 39, 6267.
12. (f) Polanyi, M. Z. Elektrochem. 1921, 27, 142.
13. (a) Rees, D. C. J. Mol. Biol. 1980, 141, 323.
14. (b) Li, Y. K.; Kuliopulos, A.; Mildvan, A. S.; Talalay, P. Biochemistry 1993, 32, 1816.
15. (c) Sternberg, M. J. E.; Hayes, F. R. F.; Russell, A. J.; Thomas, P. G.; Fersht, A. R. Nature 1987, 330, 86.
16. (a) Gilson, M. K.; Honig, B. H. Nature 1987, 330, 84.
17. (b) Warshel, A.; Russell, S. T. Q. Rev. Biophys. 1984, 17, 283.
18. (c) Lee, L. P.; Tidor, B. Nat. Struct. Biol. 2001, 8, 73.
19. (d) Schaefer, M.; Karplus, M. J. Phys. Chem. 1996, 100, 1578.
20. (a) Thornburg, L. D.; Henot, F.; Bash, D. P.; Hawkinson, D. C.; Bartel, S. D.; Pollack, R. M. Biochemistry 1998, 37, 10499.
21. (b) Czerwinski, R. M.; Harris, T. K.; Massiah, M. A.; Mildvan, A. S.; Whitman, C. P. Biochemistry 2001, 40, 1984.
22. s, symmetric stretch frequency.
23. Kirby, A. J. Chem. Ind. 1963, 1877.
24. (a) Hall, A. D.; Williams, A. Biochemistry 1986, 25, 4784.
25. (b) Zhang, Z.-Y.; Etten, R. L. V. J. Biol. Chem. 1991, 266, 1516.
26. Callender, R.; Deng, H. Annu. Rev. Biophys. Biomol. Struct. 1994, 23, 215.
27. Cheng, H.; Sukal, S.; Deng, H.; Leyh, T. S.; Callender, R. Biochemistry 2001, 40, 4035.
28. Taussky, H. H.; Shorr, E.; Kurzmann, G. J. Biol. Chem. 1953, 202, 675.
29. Gordy, W. J. Chem. Phys. 1946, 14, 305.
30. Badger, R. M.; Bauer, S. H. J. Chem. Phys. 1937, 5, 839.
31. Deng, H.; Wang, J.; Callender, R.; Ray, W. J. J. Phys. Chem. B 1998, 102, 3617.
32. Wang, J.; Xiao, D.; Deng, H.; Webb, M. R.; Callender, R. Biochemistry 1998, 37, 11106.
33. (a) Brown, I. D.; Shannon, R. D. Acta Crystallogr. 1973, A29, 3617.
34. (b) Brown, I. D.; Wu, K. K. Acta Crystallogr. 1976, B32, 1957.
35. (c) Brown, I. D. Acta Crystallogr. 1992, B48, 553.
36. (d) Calleri, M.; Speakman. J. C. Acta Crystallogr. 1964, 17, 1097.
37. 15
38. (a) Abell, K. W. Y.; Kirby, A. J. Tetrahedron Lett. 1986, 27, 1085.
39. (b) Grzyska, P. K.; Czyryca, P. G.; Golightly, J.; Small, K.; Larsen, P.; Hoff, R. H.; Hengge, A. C. J. Org. Chem. 2002, 67, 1214.
40. (a) Cleland, W. W.; Hengge, A. C. FASEB J. 1995, 9, 1585.
41. (b) Benkovic, S. J.; Schray, K. J. In Transition States of Biochemical Processes; Gandour, R. D., Schowen, R. L., Eds.; Plenum: New York, 1978; p 493.
42. (c) Williams, A. J. Am. Chem. Soc. 1985, 107, 6335.
43. (d) Thatcher, G. R. J.; Kluger, R. Adv. Phys. Org. Chem. 1989, 25, 99.
44. Hengge, A. C. In Comprehensive Biological Catalysis; Sinnott, M. L., Ed.; Academic Press: London, 1998; p 517.
45. (a) Allen, F. H.; Kirby, A. J. J. Am. Chem. Soc. 1984, 106, 6197.
46. (b) Briggs, A. J.; Glenn, R.; Jones, P. G.; Kirby, A. J.; Ramaswamy, P. J. Am. Chem. Soc. 1984, 106, 6200.
47. Jones, P. G.; Kirby, A. J. J. Am. Chem. Soc. 1984, 106, 6207.
48. We use a simplified model to understand stabilization of the leaving group alkoxide ion substituent. Several studies have suggested that substituents in nonconjugated systems exert their effects predominantly through space rather than through the bonded chain (see, for example, ref 25 and references therein), so that consideration of substituents as attached dipoles, as in Scheme 1, may provide a reasonable representation. This approximation is useful conceptually for the treatment presented in the text. but it is not required for the conclusions that are drawn. For instance, for conjugated systems, resonance effects are likely important.
49. (a) Cole, T. W.; Mayers, C. J.; Stock, L. M. J. Am. Chem. Soc. 1974, 96, 4555.
50. (b) Petti, M. A.; Shepodd, T. J.; Barrans, R. E.; Dougherty, D. A. J. Am. Chem. Soc. 1988, 110, 6825.
51. (c) Cozzi, F.; Cinquini, M.; Annunziata, R.; Siegel, J. S. J. Am. Chem. Soc. 1993, 115, 5330.
52. 2) = 16.8 kcal/mol (at 298 K).
53. (a) Kolthoff, I. M.; Chantooni, M. K., Jr.; Bhowmik, S. J. Am. Chem. Soc. 1967, 90, 23.
54. (b) Matthews, W. S.; Bares, J. E.; Bartmess, J. E.; Bordwell, F. G.; Cornforth, F. J.; Drucker, G. E.; Margolin, Z.; McCallum, R. J.; McCollum, G. J.; Vanier, N. R. J. Am. Chem. Soc. 1975, 97, 7006.
55. (c) Bordwell, F. G. Acc. Chem. Res. 1988, 21, 456.
56. The free-energy reaction profile is grossly simplified, with only one coordinate depicting the reaction progress.
57. The attached alkyl group of the phosphate ester is ignored in this treatment. This is because the phosphate ester can vary in differential solubility in water versus DMSO depending on the alkyl group used, but this alkyl chain is, to a reasonable approximation, unchanged in going from the ground state to the transition state. As we are focused on reactivity, we do not consider this portion of the phosphate ester.
58. (a) Herschlag, D.; Jencks, W. P. J. Am. Chem. Soc. 1989, 111, 7579.
59. (b) Westheimer, F. H. Chem. Rev. 1981, 81, 313.
60. 2) = 20.6 kcal/mol (at 298 K).
61. (b) Kirby, A. J.; Varvoglis, A. G. J. Am. Chem. Soc. 1967, 89, 415.
62. Herschlag, D.; Jencks, W. P. J. Am. Chem. Soc. 1989, 111, 7587.
63. (a) Carey, P. R. J. Raman Spectrosc. 1998, 29, 7.
64. (b) Callender, R.; Deng, H. Annu. Rev. Biophys. Biomol. Struct. 1994, 23, 215.
65. (a) Jencks, W. P. In Advances in Enzymology and Related Areas of Molecular Biology; Meister, A., Ed.; John Wiley & Sons: New York. 1975; p 219.
66. (b) Narlikar, G. J.; Gopalakrishnan, V.; McConnell, T. S.; Usman, N.; Herschlag, D. Proc. Natl. Acad. Sci. U.S.A. 1995. 92, 3668.
67. (c) Burke, J. R.; Frey, P. A. Biochemistry 1993, 32, 13220.
68. Palcic, M. M.; Floss, H. G. In Vitamin B6 Pyridoxal Phosphate; Dolphin, D., Poulson, R., Avramovic, O., Eds.; John Wiley & Sons: New York, 1986; p 25.
69. Lumry, R. Adv. Chem. Phys. 1971, 21, 567.
70. Jencks, W. P.; Regenstein, J. Ionization Constants of Acids and Bases; CRC: Cleveland, OH, 1976; p J187.
71. Bourne, N.; Williams, A. J. Org. Chem. 1984, 49, 1200.
72. Zhao, Y.; Zhang, Z.-Y. Biochemistry 1996, 35, 11797-11804.
73. Murto, J. Acta Chem. Scand. 1964, 18, 1043-1053.
74. Solomons, T. W. G. In Organic Chemistry: John Wiley & Sons: New York, 1988; p 655.
75. Guthrie, J. P.; Cullimore, P. A. Can. J. Chem. 1979, 57, 797.
76. Sauers, C. K.; Jencks, W. P.; Broths, S. J. J. Am. Chem. Soc. 1975, 97, 5564.
77. (a) Trifluoroethyl phosphate was also an outlier in a previous linear freeenergy relationship of a series of alkyl phosphates (see ref 44b and references therein).
78. (b) O'Brien, P. J.; Herschlag, D. Biochemistry 2002, 41, 3207.