Anomeric effect in "high energy" phosphate bonds. Selective destabilization of the scissile bond and modulation of the exothermicity of hydrolysis

Journal of the American Chemical Society

Volumn 130, Issue 11, 2008, Pages 3349-3358

  Ruben, Eliza A ^a   Plumley, Joshua A ^c   Chapman, Michael S ^b   Evanseck, Jeffrey D ^c  

^a FLORIDA STATE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c DUQUESNE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXOTHERMIC REACTIONS; FREE ENERGY; GROUND STATE; HYDROLYSIS; PHOSPHATES;

PHOSPHATE BONDS; PHOSPHOTRANSFER POTENTIAL; SCISSILE BONDS;

BOND LENGTH;

OXYGEN; PHOSPHATE;

ANALYTIC METHOD; ARTICLE; CHEMICAL BOND; CHEMICAL REACTION; CORRELATION ANALYSIS; DENSITY FUNCTIONAL THEORY; HYDROLYSIS; MOLECULAR INTERACTION; SENSITIVITY ANALYSIS; THERMODYNAMICS;

EID: 84961984918     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja073652x     Document Type: Article

References (133)

1. Allen, K. N.; Dunaway-Mariano, D. Trends. Biochem. Sci. 2004, 29 (9), 495-503.
2. Lipmann, F. Adv. Enzymol. Relat. Subj. Biochem. 1941, 1, 99-162.
3. Boyer, P. D.; Stokes, B. O.; Wolcott, R. G.; Degani, C. Fed. Proc. 1975, 34 (8), 1711-1717.
4. Knowles, J. R. Annu. Rev. Biochem. 1980, 49, 877-919.
5. Westheimer, F. H. Science 1987, 235, 1173.
6. Cleland, W.; Hengge, A. FASEB J. 1995, 9 (15), 1585-1594.
7. Diaz, N.; Field, M. J. J. Am. Chem. Soc. 2004, 126 (2), 529-542.
8. Dittrich, M.; Hayashi, S.; Schulten, K. Biophys. J. 2003, 85 (4), 2253-2266.
9. Lopez, X.; Schaefer, M.; Dejaegere, A.; Karplus, M. J. Am. Chem. Soc. 2002, 124 (18), 5010-5018.
10. Benkovic, S. J.; Schray, K. J. Chemical Basis of Biological Phosphoryl Transfer. In The Enzymes; Boyer, P. D., Ed.; Academic Press: New York, 1973; Vol. 8, pp 201-238.
11. Dzeja, P. P.; Terzic, A. J. Exp. Biol. 2003, 206 (12), 2039-2047.
12. Williams, N. H. Biochim. Biophys. Acta 2004, 1697 (1-2), 279-287.
13. Florian, J.; Warshel, A. J. Phys. Chem. B 1998, 102 (4), 719-734.
14. Florian, J.; Warshel, A. J. Am. Chem. Soc. 1997, 119 (23), 5473-5474.
15. Florian, J.; Aqvist, J.; Warshel, A. J. Am. Chem. Soc. 1998, 120 (44), 11524-11525.
16. Strajbl, M.; Shurki, A.; Warshel, A. Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (25), 14834-14839.
17. Klahn, M.; Rosta, E.; Warshel, A. J. Am. Chem. Soc. 2006, 128 (47), 15310-15323.
18. Aqvist, J.; Kolmodin, K.; Florian, J.; Warshel, A. Chem. Biol. 1999, 6 (3), R71-R80.
19. Admiraal, S. J.; Schneider, B.; Meyer, P.; Janin, J.; Veron, M.; Deville-Bonne, D.; Herschlag, D. Biochemistry 1999, 38 (15), 4701-11.
20. Admiraal, S. J.; Herschlag, D. J. Am. Chem. Soc. 2000, 122 (10), 2145-2148.
21. Cheng, H.; Nikolic-Hughes, I.; Wang, J. H.; Deng, H.; O'Brien, P. J.; Wu, L.; Zhang, Z.-Y.; Herschlag, D.; Callender, R. J. Am. Chem. Soc. 2002, 124 (38), 11295-11306.
22. Herschlag, D.; Jencks, W. P. J. Am. Chem. Soc. 1989, 111 (19), 7579-7586.
23. Hollfelder, F.; Herschlag, D. Biochemistry 1995, 34 (38), 12255-12264.
24. Maegley, K. A.; Admiraal, S. J.; Herschlag, D. PNAS 1996, 93 (16), 8160-8166.
25. O'Brien, P. J.; Herschlag, D. Biochemistry 2002, 41 (9), 3207-3225.
26. Jones, P. G.; Sheldrick, G. M.; Kirby, A. J.; K. W. Y. A. Acta Crystallogr., Sect. C: Cryst. Struct. Commun. 1984, 40 550-552.
27. Jones, P. G.; Sheldrick, G. M.; Kirby, A. J.; K. W. Y. A. Acta Crystallogr., Sect. C: Cryst. Struct. Commun. 1984, C40, 547-549.
28. Caughlan, C. N.; Inorg. Chem. 1967, 6, (11), 1998-2002.
29. Garbassi, F.; Giarda, L.; Fagherazzi, G. Acta Crystallogr., Sect. B: Struct. Crystallogr. Cryst. Commun. 1972, 28, 1665-1670.
30. Sorensen-Stowell, K.; Hengge, A. C. J. Org. Chem. 2005, 70 (12), 4805-4809.
31. Sorensen-Stowell, K.; Hengge, A. C. J. Org. Chem. 2005, 70 (21), 8303-8308.
32. Barth, A.; Bezlyepkina, N. J. Biol. Chem. 2004, 279 (50), 51888-51896.
33. Florian, J.; Strajbl, M.; Warshel, A. J. Am. Chem. Soc. 1998, 120 (31), 7959-7966.
34. Aqvist, J.; Kolmodin, K.; Florian, J.; Warshel, A. Chem. Biol. 1999, 6 (3), R71-R80.
35. Loncke, P. G.; Berti, P. J. J. Am. Chem. Soc. 2006, 128 (18), 6132-6140.
36. Gorenstein, D. G.; Luxon, B. A.; Findlay, J. B. J. Am. Chem. Soc. 1977, 99 (24), 8048-8049.
37. Gorenstein, D. G.; Luxon, B. A.; Findlay, J. B.; Momii, R. J. Am. Chem. Soc. 1977, 99 (12), 4170-4172.
38. Gorenstein, D. G. Chem. Rev. 1987, 87 (5), 1047-1077.
39. Taira, K.; Gorenstein, D. G. J. Am. Chem. Soc. 1984, 106 (25), 7825-7831.
40. Taira, K.; Fanni, T.; Gorenstein, D. G. J. Am. Chem. Soc. 1984, 106 (5), 1521-1523.
41. Range, K.; McGrath, M. J.; Lopez, X.; York, D. M. J. Am. Chem. Soc. 2004, 126 (6), 1654-1665.
42. Klahn, M.; Schlitter, J.; Gerwert, K. Biophys. J. 2005, 88 (6), 3829-3844.
43. Cheng, H.; Sukal, S.; Deng, H.; Leyh, T. S.; Callender, R. Biochemistry 2001, 40 (13), 4035-4043.
44. Shurki, A.; Strajbl, M.; Schutz, C. N.; Warshel, A. Methods Enzymol. 2004, 380, 52-84.
45. Voet, D.; Voet, J. G. Biochemistry; 2nd ed.; John Wiley: New York, 1995; pp 428-434.
46. Jones, P. G.; Kirby, A. J. J. Am. Chem. Soc. 1984, 106 (21), 6207-6212.
47. Allen, F. H.; Kirby, A. J. J. Am. Chem. Soc. 1984, 106 (21), 6197-6200.
48. Gautier, A. Heterocycles 2006, 67 (2), 823-837.
49. Whitehead, A.; McReynolds, M. D.; Moore, J. D.; Hanson, P. R. Org. Lett. 2005, 7 (15), 3375-3378.
50. Egli, M.; Minasov, G.; Tereshko, V.; Pallan, P. S.; Teplova, M.; Inamati, G. B.; Lesnik, E. A.; Owens, S. R.; Ross, B. S.; Prakash, T. P.; Manoharan, M. Biochemistry 2005, 44 (25), 9045-9057.
51. Matsukawa, S.; Yamamoto, Y.; Akiba, K.-y. Heterocycles 2003, 59 (2), 707-719.
52. Zhang, X.; Harrison, D. H. T.; Cui, Q. J. Am. Chem. Soc. 2002, 124 (50), 14871-14878.
53. Labande, A.; Ruiz, J.; Astruc, D. J. Am. Chem. Soc. 2002, 124 (8), 1782-1789.
54. Toney, M. D. Biochemistry 2001, 40 (5), 1378-1384.
55. Velikian, I.; Acharya, P.; Trifonova, A.; Foldesi, A.; Chattopadhyaya, J. J. Phys. Org. Chem. 2000, 13 (5), 300-305.
56. Alber, F.; Folkers, G.; Carloni, P. J. Phys. Chem. B 1999, 103 (29), 6121-6126.
57. Acharya, P.; Kawrot, B.; Sprinzl, M.; Thibaudeau, C.; Chattopadhyaya, J. J. Chem. Soc., Perkin Trans. 1999, 2 (7), 1531-1536.
58. Parker, E. J.; Coggins, J. R.; Abell, C. J. Org. Chem. 1997, 62 (24), 8582-8585.
59. Tole, P.; Lim, C. Do stereoelectronic effects control the structure and reactivity of trigonal-bipyramidal phosphoesters? ACS Symp. Ser. 1993, 539 (Anomeric Effect and Associated Stereoelectronic Effects), 240-55.
60. Johnson, L. N.; Hu, S. H.; Barford, D. Faraday Discuss. 1992, 93 (Structure and Activity of Enzymes), 131-42.
61. Uchimaru, T.; Tanabe, K.; Nishikawa, S.; Taira, K. J. Am. Chem. Soc. 1991, 113 (11), 4351-3.
62. Boger, D. L.; Munk, S. A.; Zarrinmayeh, H. J. Am. Chem. Soc. 1991, 113 (10), 3980-3.
63. Voityuk, A. A. Izv. Akad. Nauk SSSR, Ser. Khim. 1990, 11, 2528-32.
64. Kluger, R.; Taylor, S. D. J. Am. Chem. Soc. 1990, 112 (18), 6669-71.
65. Van Genderen, M. H. P.; Kook, L. H.; Buck, H. M. Recl. Trav. Chim. Pays-Bas 1989, 108 (1), 28-35.
66. Gorenstein, D. G.; Chang, A.; Yang, J. C. Tetrahedron 1987, 43, (3), 469-78.
67. Gorenstein, D. G.; Schroeder, S. A.; Miyasaki, M.; Fu, J. M.; Roongta, V.; Abuaf, P.; Chang, A.; Yang, J. C. Bioact. Mol. 1987, 3 (Biophosphates Their Analogues), 487-502.
68. Fanni, T. A. Stereoelectronic effects in phosphates, phosphorothionates, and phosphoranes; 1985.
69. Kluger, R.; Thatcher, G. R. J. J. Am. Chem. Soc 1985, 107 (21), 6006-11.
70. Yakovlev, G. I.; Bocharov, A. L.; Moiseev, G. P.; Mikhailov, S. N. Bioorg. Khim. 1985, 11 (2), 205-10.
71. Yakovlev, G. I.; Bocharov, A. L.; Moiseev, G. P.; Mikhailov, S. N. FEBS Lett. 1985, 179 (2), 217-20.
72. Taira, K.; Gorenstein, D. G. J. Am. Chem. Soc. 1984, 106 (25), 7825-31.
73. Taira, K.; Fanni, T.; Gorenstein, D. G. J. Org. Chem. 1984, 49 (23), 4531-6.
74. Taira, K.; Fanni, T.; Gorenstein, D. G. J. Am. Chem. Soc. 1984, 106 (5), 1521-3.
75. Gorenstein, D. G.; Rowell, R.; Taira, K. ACS Symp. Ser. 1981, 171 (Phosphorus Chem.), 69-75.
76. Gorenstein, D. G.; Luxon, B. A.; Goldfield, E. M. J. Am. Chem. Soc. 1980, 102 (5), 1757-9.
77. Gorenstein, D. G.; Luxon, B. A.; Findlay, J. B. 2. J. Am. Chem. Soc. 1979, 101 (20), 5869-75.
78. Luxon, B. A. Stereoelectronic effects in phosphate esters; 1977.
79. Gorenstein, D. G.; Luxon, B. A.; Findlay, J. B. J. Am. Chem. Soc. 1977, 99 (24), 8048-9.
80. Kar, D. Part I. Stereoelectronic effects in phosphate esters. Part II. Proton nuclear magnetic resonance study on the binding of trans-cinnamaldehyde to a-chymotrypsin; 1977.
81. Gorenstein, D. G.; Luxon, B. A.; Findlay, J. B.; Momii, R. J. Am. Chem. Soc. 1977, 99 (12), 4170-2.
82. Lehn, J. M.; Wipff, G. J. Chem. Soc., Chem. Commun. 1975, 19, 800-2.
83. Whitehead, A.; McReynolds Matthew, D.; Moore Joel, D.; Hanson Paul, R. Org. Lett. 2005, 7 (15), 3375-8.
84. Zhang, X.; Harrison David, H. T.; Cui, Q. J. Am. Chem. Soc. 2002, 124 (50), 14871-8.
85. Yakovlev, G. I.; Bocharov, A. L.; Moiseyev, G. P.; Mikhaylov, S. N. FEBS Lett. 1985, 179 (2), 217-20.
86. Tsai, M. D.; Weintraub, H. J.; Byrn, S. R.; Chang, C.; Floss, H. G. Biochemistry 1978, 17 (16), 3183-8.
87. Cramer, C. J.; Gustafson, S. M. J. Am. Chem. Soc. 1994, 116 (2), 723-734.
88. Cramer, C. J.; Gustafson, S. M. J. Am. Chem. Soc. 1993, 115 (20), 9315-9316.
89. Gauss, J.; Cramer, C. Chem. Phys. Lett. 1988, 150, 280.
90. Storer, J. W.; Uchimaru, T.; Tanabe, K.; Uebayasi, M.; Nishikawa, S.; Taira, K. J. Am. Chem. Soc. 1991, 113 (14), 5216-5219.
91. Zhou, D.-M.; Taira, K. Chem. Rev. 1998, 98 (3), 991-1026.
92. Banavali, N. K.; MacKerell, A. D. J. Am. Chem. Soc. 2001, 123 (28), 6747-6755.
93. Hernandez, J.; Ramos, R.; Sastre, N.; Meza, R.; Hommer, H.; Salas, M.; Gordillo, B. Tetrahedron 2004, 60 (48), 10927-10941.
94. Cramer, C. J.; Denmark, S. E.; Miller, P. C.; Dorow, R. L.; Swiss, K. A.; Wilson, S. R. J. Am. Chem. Soc. 1994, 116 (6), 2437-2447.
95. Kirby, A. J. Adv. Phys. Org. Chem. 1994, 29, 87-184.
96. Denehy, E.; White, J. M.; Williams, S. J. Chem. Commun. 2006, 3, 314-316.
97. Frisch, M. J.; et al. Gaussian 03, revision D.01; Gaussian, Inc.: Pittsburgh, PA, 2003.
98. Hwang, M.-J.; Chu, P.-Y.; Chen, J.-C.; Chao, I. J. Comput. Chem. 1999, 20 (16), 1702-1715.
99. Meagher, K. L.; Redman, L. T.; Carlson, H. A. J. Comput. Chem. 2003, 24 (9), 1016-1025.
100. Crowhurst, G. S.; Dalby, A. R.; Isupov, M. N.; Campbell, J. W.; Littlechild, J. A. Acta Crystallogr., Sect. D: Biol. Crystallogr. 1999, 55 (11), 1822-1826.
101. Flachner, B.; Kovari, Z.; Varga, A.; Gugolya, Z.; Vonderviszt, F.; NaraySzabo, G.; Vas, M. Biochemistry 2004, 43 (12), 3436-3449.
102. Stewart, J. J. P. J. Comput. Chem. 1989, 10 (2), 221-264.
103. Becke, A. D. Phys. Rev. A 1988, 38, 3098-3100.
104. Lee, C.; Yang, W.; Parr, R. G. Phys. Rev. B 1988, 37 (2), 785-789.
105. Francl, M. M.; Pietro, W. J.; Hehre, W. J.; Binkley, J. S.; Gordon, M. S.; Defrees, D. J.; Pople, J. A. J. Chem. Phys. 1982, 77, 3654-3665.
106. Clark, T.; Chandrasekhar, J.; Spitznagel, G. W.; Schleyer, P. v. R. J. Comput. Chem. 1983, 4, 294.
107. Miertus, S.; Scrocco, E.; Tomasi, J. J. Chem. Phys. 1981, 55, 117.
108. Besler, B. H.; Merz, K. M.; Kollman, P. A. J. Comput. Chem. 1990, 11, (4), 431-439.
109. Ruben, E. A.; Chapman, M. S.; Evanseck, J. D. J. Am. Chem. Soc. 2005, 127 (50), 17789-17798.
110. Glendening, E. D.; Badenhoop, J. K.; Reed, A. E.; Carpenter, J. E. Weinhold, F. NBO 3.1, 1996.
111. Alabugin, I. V.; Zeidan, T. A. J. Am. Chem. Soc. 2002, 124 (12), 3175-3185.
112. Alabugin, I. V.; Mariappan, M.; Zeidan, T. A. J. Am. Chem. Soc. 2003, 125 (46), 14014-14031.
113. Cramer, C. J.; Kelterer, A. M.; French, A. D. J. Comput. Chem. 2001, 22 (11), 1194-1204.
114. Kitaura, K.; Morokuma, K. Int. J. Quant. Chem. 1976, 10 (2), 325-340.
115. Mo, Y.; Peyerimhoff, S. D. J. Chem. Phys. 1998, 109 (5), 1687-1697.
116. Mo, Y.; Gao, J. Acc. Chem. Res. 2007, 40 (2), 113-119.
117. Garrett, R. H.; Grisham, C. M. Biochemistry, 2nd ed.; Saunders: Fort Worth, 1999; pp 56-80.
118. Berg, J.; Tymoczko, J. L.; Stryer, L. Biochemistry, 5th ed.; W. H. Freeman & Co.: New York, 2002; pp 374-383.
119. Pauling, L. The Nature of the Chemical Bond; Cornell University Press: Ithaca, NY, 1939.
120. Grzyska, P. K.; Czyryca, P. G.; Golightly, J.; Small, K.; Larsen, P.; Hoff, R. H.; Hengge, A. C. J. Org. Chem. 2002, 67 (4), 1214-1220.
121. Miertus, S.; Tomasi, J. J. Chem. Phys. 1982, 65, 239.
122. Stryer, L.; Berg, J. M.; Tmoczko, J. L. Biochemistry, 5th ed.; Freeman: New York, 2001.
123. Jencks, W. P.; Regenstein, J. Handbook of Biochemistry and Molecular Biology; Cleveland, 1976; pp 305-351.
124. Popov, K. I.; Sultanova, N. M.; Ronkkomaki, H. Russian J. Phys. Chem. 2006, 80 (10), 1680-1682.
125. Briggs, A. J.; Glenn, R.; Jones, P. G.; Kirby, A. J.; Ramaswamy, P. J. Am. Chem. Soc 1984, 106 (21), 6200-6206.
126. Kirby, A. J. The Anomeric Effect and Related Stereoelectronic Effects at Oxygen; Springer-Verlag: Berlin, 1983.
127. Dejaegere, A.; Lim, C.; Karplus, M. J. Am. Chem. Soc. 1991, 113 (11), 4353-4355.
128. Umeyama, H.; Morokuma, K. J. Am. Chem. Soc. 1977, 99 (5), 1316-1332.
129. Reed, A. E.; Curtiss, L. A.; Weinhold, F. Chem. Rev. 1988, 88 (6), 899-926.
130. Glendening, E. D.; Streitwieser, A. J. Chem. Phys. 1994, 100 (4), 2900-2909.
131. Allin, C.; Gerwert, K. Biochemistry 2001, 40 (10), 3037-3046.
132. Grigorenko, B. L.; Nemukhin, A. V.; Shadrina, M. S.; Topol, I. A.; Burt, S. K. Proteins: Struct., Funct., Bioinf. 2007, 66 (2), 456-466.
133. Topol, I. A.; Cachau, R. E.; Nemukhin, A. V.; Grigorenko, B. L.; Burt, S. K. Biochim. Biophys. Acta 2004, 1700 (1), 125-136.