Transesterification thio effects of phosphate diesters: Free energy barriers and kinetic and equilibrium isotope effects from density-functional theory

Biochemistry

Volumn 45, Issue 33, 2006, Pages 10043-10053

  Liu, Yun ^a   Gregersen, Brent A ^a   Hengge, Alvan ^b   York, Darrin M ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UTAH STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ISOTOPES; NEGATIVE IONS; PHOSPHATES; PROBABILITY DENSITY FUNCTION; SUBSTITUTION REACTIONS; SULFUR;

RATE CONTROLLING TRANSITION STATES; REVERSE REACTION MODELS; SOLVATION MODELS; TRANSESTERIFICATION;

ESTERS;

ISOTOPE; ORGANOPHOSPHATE; RIBOZYME; SOLVENT; THIOL GROUP; WATER;

ALKALINITY; AQUEOUS SOLUTION; ARTICLE; CATALYSIS; CHEMICAL BOND; CHEMICAL STRUCTURE; DENSITY FUNCTIONAL THEORY; ENERGY; KINETICS; PRIORITY JOURNAL; REACTION ANALYSIS; SOLVATION; STRUCTURE ANALYSIS; TRANSESTERIFICATION;

CATALYSIS; ELECTROSTATICS; ESTERIFICATION; KINETICS; MODELS, CHEMICAL; OXYGEN ISOTOPES; PHOSPHORIC ACID ESTERS; PHOSPHORYLATION; RNA; RNA, CATALYTIC; SOLVENTS; THERMODYNAMICS; WATER;

EID: 33747503207     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060869f     Document Type: Article

References (96)

1. Perreault, D. M., and Anslyn, E. V. (1997) Unifying the Current Data on the Mechanism of Cleavage-Transesterification of RNA, Angew. Chem., Int. Ed. 36, 432-450.
2. Zhou, D.-M., and Taira, K. (1998) The Hydrolysis of RNA: From Theoretical Calculations to the Hammerhead Ribozyme-Mediated Cleavage of RNA, Chem. Rev. 98, 991-1026.
3. Oivanen, M., Kuusela, S., and Lönnberg, H. (1998) Kinetics and Mechanisms for the Cleavage and Isomerization of the Phosphodiester Bonds of RNA by Bronsted Acids and Bases, Chem. Rev. 98, 961-990.
4. Hengge, A. C. (2002) Isotope effects in the study of phosphoryl and sulfuryl transfer reactions, Acc. Chem. Res. 35, 105-112.
5. Hengge, A. C. (2001) Isotope effects in the study of enzymatic phosphoryl transfer reactions, FEBS Lett. 501, 99-102.
6. Herschlag, D., Piccirilli, J. A., and Cech, T. R. (1991) Ribozyme-Catalyzed and Nonenzymic Reactions of Phosphate Diesters: Rate Effects upon Substitution of Sulfur for a Nonbridging Phosphoryl Oxygen Atom, Biochemistry 30, 4844-4854.
7. Scott, W. G. (1999) Biophysical and biochemical investigations of RNA catalysis in the hammerhead ribozyme, Q. Rev. Biophys. 32, 241-294.
8. Suzumura, K., Takagi, Y., Orita, M., and Taira, K. (2004) NMR-Based Reappraisal of the Coordination of a Metal Ion at the ProRp Oxygen of the A9/G10.1 Site in a Hammerhead Ribozyme, J. Am. Chem. Soc. 126 (47), 15504-15511.
9. Onyido, I., Swierczek, K., Purcell, J., and Hengge, A. C. (2005) A Concerted Mechanism for the Transfer of the Thiophosphinoyl Group from Aryl Dimethylphosphinothioate Esters to Oxyanionic Nucleophiles in Aqueous Solution, J. Am. Chem. Soc. 127, 7703-7711.
10. Åqvist, J., Kolmodin, K., Florian, J., and Warshel, A. (1999) Mechanistic alternatives in phosphate monoester hydrolysis: What conclusions can be drawn from available experimental data? Chem. Biol. 6 (3), R71-R80.
11. Karplus, M. (2000) Aspects of Protein Reaction Dynamics: Deviations from Simple Behavior, J. Phys. Chem. B 104, 11-27.
12. Friesner, R. A., and Beachy, M. D. (1998) Quantum mechanical calculations on biological systems, Curr. Opin. Struct. Biol. 8, 257-262.
13. Warshel, A. (2003) Computer simulations of enzyme catalysis: Methods, progress, and insights, Annu. Rev. Biophys. Biomol. Struct. 32, 425-443.
14. Garcia-Viloca, M., Gao, J., Karplus, M., and Truhlar, D. G. (2004) How enzymes work: Analysis by modern rate theory and computer simulations, Science 303, 186-195.
15. Lim, C., and Karplus, M. (1990) Nonexistence of dianionic pentacovalent intermediates in an ab initio study of the base-catalyzed hydrolysis of ethylene phosphate, J. Am. Chem. Soc. 112, 5872-5873.
16. Uchimaru, T., Tanabe, K., Nishikawa, S., and Taira, K. (1991) Ab Initio Studies of a Marginally Stable Intermediate in the Base-Catalyzed Methanolysis of Dimethyl Phosphate and Nonexistence of the Stereoelectronically Unfavorable Transition State, J. Am. Chem. Soc. 113, 4351-4353.
17. Lim, C., and Tole, P. (1992) Concerted Hydroxyl Ion Attack and Pseudorotation in the Base-Catalyzed Hydrolysis of Methyl Ethylene Phosphate, J. Phys. Chem. 96, 5217-5219.
18. Mercero, J. M., Barrett, P., Lam, C. W., Fowler, J. E., Ugalde, J. M., and Pedersen, L. G. (2000) Quantum Mechanical Calculations on Phosphate Hydrolysis Reactions, J. Comput. Chem. 21, 43-51.
19. Arantes, G. M., and Chaimovich, B. (2005) Thiolysis and Alcoholysis of Phosphate Tri- and Monoesters with Alkyl and Aryl Leaving Groups. An ab Initio Study in the Gas Phase, J. Phys. Chem. A 109, 5625-5635.
20. Dejaegere, A., Lim, C., and Karplus, M. (1991) Dianionic Pentacoordinate Species in the Base-Catalyzed Hydrolysis of Ethylene and Dimethyl Phosphate, J. Am. Chem. Soc. 113, 4353-4355.
21. Dejaegere, A., and Karplus, M. (1993) Hydrolysis Rate Difference between Cyclic and Acyclic Phosphate Esters: Solvation versus Strain, J. Am. Chem. Soc. 115 (12), 5316-5317.
22. Tole, P., and Lim, C. (1993) New Insights into the Base-Catalyzed Hydrolysis of Methyl Ethylene Phosphate, J. Phys. Chem. 97, 6212-6219.
23. Tole, P., and Lim, C. (1994) The Significance of Electrostatic Effects in Phospho-Ester Hydrolysis, J. Am. Chem. Soc. 116 (9), 3922-3931.
24. Chang, N., and Lim, C. (1997) An ab initio study of nucleophilic attack of trimethyl phosphate: Factors influencing site reactivity, J. Phys. Chem. A 101, 8706-8713.
25. Florián, J., and Warshel, A. (1997) A fundamental assumption about OH-attack in phosphate ester hydrolysis is not fully justified, J. Am. Chem. Soc. 119, 5473-5474.
26. Florián, J., and Warshel, A. (1998) Phosphate ester hydrolysis in aqueous solution: Associative versus dissociative mechanisms, J. Phys. Chem. B 102, 719-734.
27. Hu, C.-H., and Brinck, T. (1999) Theoretical Studies of the Hydrolysis of the Methyl Phosphate Anion, J. Phys. Chem. A 103, 5379-5386.
28. Lopez, X., Dejaegere, A., and Karplus, M. (2001) Solvent Effects on the Reaction Coordinate of the Hydrolysis of Phosphates and Sulfates: Application of Hammond and Anti-Hammond Postulates to Understand Hydrolysis in Solution, J. Am. Chem. Soc. 123, 11755-11763.
29. a in phosphoranes: Implications for phosphate ester hydrolysis, J. Am. Chem. Soc. 124 (18), 5010-5018.
30. Chen, X., and Zhan, C.-G. (2004) Theoretical determination of activation free energies for alkaline hydrolysis of cyclic and acyclic phosphodiesters in aqueous solution, J. Phys. Chem. A. 108, 6407-6413.
31. Xu, D., Guo, H., Liu, Y., and York, D. M. (2005) Theoretical Studies of Dissociative Phosphoryl Transfer in Interconversion of Phosphoenolpyruvate to Phosphonopyruvate: Solvent Effects, Thio Effects, and Implications for Enzymatic Reactions, J. Phys. Chem. B 109, 13827-13834.
32. Florián, J., Åqvist, J., and Warshel, A. (1998) On the reactivity of phosphate monoester dianions in aqueous solution: Brönsted linear free-energy relationships do not have an unique mechanistic interpretation, J. Am. Chem. Soc. 120, 11524-11525.
33. Liang, C., and Allen, L. C. (1987) Sulfur Does Not Form Double Bonds in Phosphorothioate Anions, J. Am. Chem. Soc. 109, 6449-6453.
34. Florián, J., Strajbl, M., and Warshel, A. (1998) Conformational flexibility of phosphate, phosphonate, and phosphorothioate methyl esters in aqueous solution, J. Am. Chem. Soc. 120, 7959-7966.
35. Lopez, C. S., Faza, O. N., Gregersen, B. A., Lopez, X., de Lera, A. R., and York, D. M. (2004) Pseudorotation of Natural and Chemically Modified Biological Phosphoranes: Implications for RNA Catalysis, ChemPhysChem 5, 1045-1049.
36. Liu, Y., Lopez, X., and York, D. M. (2005) Kinetic isotope effects on thio-substituted biological phosphoryl transfer reactions from density-functional theory, Chem. Commun. 31, 3909-3911.
37. Uchimaru, T., Stec, W. J., and Taira, K. (1997) Mechanism of the Chemoselective and Stereoselective Ring Opening of Oxathiaphosphoranes: An Ab Initio Study, J. Org. Chem. 62, 5793-5800.
38. Uchimaru, T., Stec, W. J., Tsuzuki, S., Hirose, T., Tanabe, K., and Taira, K. (1996) Ab initio investigation on nucleophilic ring opening of 1,3,2-oxathiaphosphorane: Nucleophilic substitution at phosphorus coupled with pseudorotation, Chem. Phys. Lett. 263, 691-696.
39. Scott, W. G., Murray, I. B., Arnold, J. R. P., Stoddard, B. L., and Klug, A. (1996) Capturing the structure of a catalytic RNA intermediate: The hammerhead ribozyme, Science 274, 2065-2069.
40. Walter, N. G., and Burke, J. M. (1998) The hairpin ribozyme: Structure, assembly and catalysis, Curr. Opin. Chem. Biol. 2, 24-30.
41. Rupert, P. B., Massey, A. P., Sigurdsson, S. T., and Ferré- D'Amaré, A. R. (2002) Transition State Stabilization by a Catalytic RNA, Science 298, 1421-1424.
42. Ke, A., Zhou, K., Ding, F., Cate, J. H. D., and Doudna, J. A. (2004) A Conformational switch controls hepatitis delta virus ribozyme catalysis, Nature 429, 201-205.
43. Das, S., and Piccirilli, J. (2005) General acid catalysis by the hepatitis delta virus ribozyme, Nat. Chem. Biol. 1 (1), 45-52.
44. Truhlar, D. G., Gao, J., Garcia-Viloca, M., Alhambra, C., Corchado, J., Sanchez, M. L., and Poulsen, T. D. (2004) Ensemble-averaged variational transition state theory with optimized multidimensional tunneling for enzyme kinetics and other condensed-phase reactions, Int. J. Quantum Chem. 100, 1136-1152.
45. Saunder, M., Laidig, K. E., and Wolfsberg, M. (1989) Theoretical Calculation of Equilibrium Isotope Effects Using ab Initio Force Constants: Application to NMR Isotopic Perturbation Studies, J. Am. Chem. Soc. 111, 8989-8994.
46. Barnes, J. A., and Williams, I. H. (1996) Theoretical modelling of kinetic isotope effects for glycoside hydrolysis in aqueous solution by a hybrid quantum-mechanical/molecular-mechanical method, Chem. Commun., 193-194.
47. Rodriquez, C. F., and Williams, I. H. (1997) Ab initio theoretical investigation of the mechanism for α-lactone formation from α-halocarboxylates: Leaving group, substituent, solvent and isotope effects, J. Chem. Soc. Perkin Trans. 2, 959-965.
48. Alhambra, C., Carochado, J., Sánchez, M. L., Garcia-Viloca, M., Gao, J., and Truhlar, D. G. (2001) Canonical variational theory for enzyme kinetics with the protein mean force and multidimensional quantum mechanical tunneling dynamics. Theory and application to liver alcohol dehydrogenase, J. Phys. Chem. B 105, 11326-11340.
49. Gao, J., and Truhlar, D. G. (2002) Quantum Mechanical Methods for Enzyme Kinetics, Annu. Rev. Phys. Chem. 53, 467-505.
50. Houk, K. N., Gustafson, S. M., and Black, K. A. (1992) Theoretical secondary kinetic isotope effects and the interpretation of transition state geometries. 1. The Cope rearrangement, J. Am. Chem. Soc. 114, 8565-8572.
51. Wiest, O., Houk, K. N., Black, K. A., and Thomas, B., IV (1995) Secondary Kinetic Isotope Effects of Diastereotopic Protons in Pericyclic Reactions: A New Mechanistic Probe, J. Am. Chem. Soc. 117, 8594-8599.
52. Gregersen, B. A., Lopez, X., and York, D. M. (2004) Hybrid QM/MM Study of Thio Effects in Transphosphorylation Reactions: The Role of Solvation, J. Am. Chem. Soc. 126, 7504-7513.
53. Becke, A. D. (1993) Density-functional thermochemistry. III. The role of exact exchange, J. Chem. Phys. 98 (7), 5548-5652.
54. Lee, C., Yang, W., and Parr, R. G. (1998) Development of the Colle-Savetti correlation energy formula into a functional of the electron density, Phys. Rev. B 37, 785-789.
55. Reed, A. E., Weinstock, R. B., and Weinhold, F. (1985) Natural population analysis, J. Chem. Phys. 83, 735-746.
56. Range, K., McGrath, M. J., Lopez, X., and York, D. M. (2004) The Structure and Stability of Biological Metaphosphate, Phosphate, and Phosphorane Compounds in the Gas Phase and in Solution, J. Am. Chem. Soc. 126, 1654-1665.
57. Mayaan, E., Range, K., and York, D. M. (2004) Structure and binding of Mg(II) ions and di-metal bridge complexes with biological phosphates and phosphoranes, J. Biol. Inorg. Chem. 9 (7), 807-817.
58. López, C. S., Faza, O. N., de Lera, A. R., and York, D. M. (2005) Pseudorotation Barriers of Biological Oxyphosphoranes: A Challenge for Simulations of Ribozyme Catalysis, Chem.-Eur. J. 11, 2081-2093.
59. Tomasi, J., and Persico, M. (1994) Molecular interaction in solution: An overview of methods based on continuous distributions of the solvent, Chem. Rev. 94, 2027-2094.
60. Cossi, M., Scalmani, G., Rega, N., and Barone, V. (2002) New developments in the polarizable continuum model for quantum mechanical and classical calculations on molecules in solution, J. Chem. Phys. 117, 43-54.
61. Barone, V., Cossi, M., and Tomasi, J. (1997) A new definition of cavities for the computation of solvation free energies by the polarizable contiuum model, J. Chem. Phys. 107 (8), 3210-3221.
62. Peng, C., Ayala, P. Y., Schlegel, H. B., and Frisch, M. J. (1996) Using redundant internal coordinates to optimize equilibrium geometries and transition states, J. Comput. Chem. 17, 49-56.
63. Bauernschmitt, R., and Ahlrichs, R. (1996) Stability analysis for solutions of the closed shell Kohn Sham equation, J. Chem. Phys. 104, 9047-9052.
64. Seeger, R., and Pople, J. A. (1977) Self-consistent molecular orbital methods. XVIII. Constraints and stability in Hartree-Fock theory, J. Chem. Phys. 66 (7), 3045-3050.
65. Cramer, C. J. (2002) Essentials of Computational Chemistry: Theories and Models, 2nd ed., John Wiley & Sons, Chichester, England.
66. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Montgomery, J. A., Jr., Vreven, T., Kudin, K. N., Burant, J. C., Millam, J. M., Iyengar, S. S., Tomasi, J., Barone, V., Mennucci, B., Cossi, M., Scalmani, G., Rega, N., Petersson, G. A., Nakatsuji, H., Hada, M., Ehara, M., Toyota, K., Fukuda, R., Hasegawa, J., Ishida, M., Nakajima, T., Honda, Y., Kitao, O., Nakai, H., Klene, M., Li, X., Knox, J. E., Hratchian, H. P., Cross, J. B., Bakken, V., Adamo, C., Jaramillo, J., Gomperts, R., Stratmann, R. E., Yazyev, O., Austin, A. J., Cammi, R., Pomelli, C., Ochterski, J. W., Ayala, P. Y., Morokuma, K., Voth, G. A., Salvador, P., Dannenberg, J. J., Zakrzewski, V. G., Dapprich, S., Daniels, A. D., Strain, M. C., Farkas, O., Malick, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Ortiz, J. V., Cui, Q., Baboul, A. G., Clifford, S., Cioslowski, J., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Martin, R. L., Fox, D. J., Keith, T., Al-Laham, M. A., Peng, C. Y., Nanayakkara, A., Challacombe, M., Gill, P. M. W., Johnson, B., Chen, W., Wong, M. W., Gonzalez, C., and Pople, J. A. (2004) Gaussian 03, revision C.02, Gaussian, Inc., Wallingford, CT.
67. Weston, R. E., Jr., and Schwarz, H. A. (1972) Chemical Kinetics, Prentice-Hall, Englewood Cliffs, NJ.
68. Corchado, J. C., Chuang, Y.-Y., Fast, P. L., Hu, W.-P., Liu, Y.-P., Lynch, G. C., Nguyen, K. A., Jackels, C. F., Ramos, A. F., Ellingson, B. A., Lynch, B. J., Melissas, V. S., Villa, J., Rossi, I., Coitino, E. L., Pu, J., Albu, T. V., Steckler, R., Garrett, B. C., Isaacson, A. D., and Truhlar, D. G. (2005) POLYRATE, version 9.3.1, University of Minnesota, Minneapolis, MN.
69. Saunders, W. H., Jr. (1980) Investigations of Rates and Mechanisms of Reactions, Vol. 6, pp 565-611, Wiley-Interscience, New York.
70. Bigeleisen, J., and Mayer, M. G. (1947) Calculation of Equilibrium Constants for Isotopic Exchange Reactions, J. Chem. Phys. 15 (5), 261-267.
71. Warshel, A., and Levitt, M. (1976) Theoretical studies of enzymatic reactions: Dielectric electrostatic and steric stabilization in the reaction of lysozyme, J. Mol. Biol. 103, 227-249.
72. Gao, J. (2003) Catalysis by enzyme conformational change as illustrated by orotidine 5′-monophosphate decarboxylase, Curr. Opin. Struct. Biol. 13, 184-192.
73. Nam, K., Gao, J., and York, D. M. (2005) An Efficient Linear-Scaling Ewald Method for Long-Range Electrostatic Interactions in Combined QM/MM Calculations, J. Chem. Theory Comput. 1 (1), 2-13.
74. Truhlar, D. G., and Garrett, B. C. (1984) Variational transition state theory, Annu. Rev. Phys. Chem. 35, 159-189.
75. Lide, D. R., Ed. (2003) CRC Handbook of Chemistry and Physics, 83rd ed., CRC Press, Boca Raton, FL.
76. Liu, X., and Reese, C. B. (1995) Uridylyl-(3′→5′)- (5′-thiouridine). An exceptionally base-labile di-ribonucleoside phosphate analogue, Tetrahedron Lett. 36 (19), 3413-3416.
77. Thomson, J. B., Patel, B. K., Jiménez, V., Eckart, K., and Eckstein, F. (1996) Synthesis and properties of diuridine phosphate analogues containing thio and amino modifications, J. Org. Chem. 61, 6273-6281.
78. Dantzman, C. L., and Kiessling, L. L. (1996) Reactivity of a 20-thio nucleotide analog, J. Am. Chem. Soc. 118, 11715-11719.
79. Liu, X., and Reese, C. B. (1996) 3′-Thiouridylyl- (3′→5′)-uridine, Tetrahedron Lett. 37 (6), 925-928.
80. Weinstein, L. B., Earnshaw, D. J., Cosstick, R., and Cech, T. R. (1996) Synthesis and characterization of an RNA dinucleotide containing a 30-S-phosphorothiolate linkage, J. Am. Chem. Soc. 118 (43), 10341-10350.
81. Burgers, P. M. J., and Eckstein, F. (1979) Diastereomers of 5′-O-Adenosyl 3′-O-Uridyl Phosphorothioate: Chemical Synthesis and Enzymatic Properties, Biochemistry 18, 592-596.
82. Almer, H., and Strömberg, R. (1991) Intramolecular transesterification in thiophosphate-analogues of an RNA-dimer, Tetrahedron Lett. 32 (30), 3723-3726.
83. Almer, H., and Strömberg, R. (1996) Base catalysis and leaving group dependence in intramolecular alcoholysis of uridine 30-(aryl phosphorothioate)s, J. Am. Chem. Soc. 118, 7921-7928.
84. Ora, M., Oivanen, M., and Lönnberg, H. (1996) Hydrolysis and Desulfurization of the Diastereomeric Phosphoromonothioate Analogs of Uridine 20,30-Cyclic Monophosphate, J. Org. Chem. 61, 3951-3955.
85. Ora, M., Oivanen, M., and Lönnberg, H. (1997) Phosphoester Hydrolysis and Intramolecular Transesterification of Ribonucleoside 20- and 30-Phosphoromonothioate Triestes: Kinetics and Mechanisms for the Reactions of 50-O-Methyluridine 20- and 30-Dimethylphosphoromonothioates, J. Org. Chem. 62, 3246-3253.
86. Ora, M., Järvi, J., Oivanen, M., and Lönnberg, H. (2000) Hydrolytic Reactions of the Phosphorodithioate Analogue of Uridylyl(30,50) uridine: Kinetics and Mechanisms for the Cleavage, Desulfurization, and Isomerization of the Internucleosidic Linkage, J. Org. Chem. 65, 2651-2657.
87. Oivanen, M., Ora, M., Almer, H., Strömberg, R., and Lönnberg, H. (1995) Hydrolytic reactions of the diastereomeric phosphoromonothioate analogs of uridylyl(3′,5′)uridine: Kinetics and mechanisms for desulfurization, phosphoester hydrolysis, and transesterification to the 2′,5′-isomers, J. Org. Chem. 60, 5620-5627.
88. Nielsen, J., Brill, W. K.-D., and Caruthers, M. H. (1988) Synthesis and characterization of dinucleoside phosphorodithioates, Tetrahedron Lett. 29 (24), 2911-2914.
89. Petersen, K. H., and Nielsen, J. (1990) Chemical synthesis of dimer ribonucleotides containing internucleotidic phosphorodithioate linkages, Tetrahedron Lett. 31 (6), 911-914.
90. Gerratana, B., Sowa, G. A., and Cleland, W. W. (2000) Characterization of the transition-state structures and mechanisms for the isomerization and cleavage reactions of uridine 30-m-nitrobenzyl phosphate, J. Am. Chem. Soc. 122 (51), 12615-12621.
91. Cassano, A. G., Anderson, V. E., and Harris, M. E. (2002) Evidence for Direct Attack by Hydroxide in Phosphodiester Hydrolysis, J. Am. Chem. Soc. 124, 10964-10965.
92. Hogg, J. L., Rodgers, J., Kovach, I. M., and Schowen, R. L. (1980) Kinetic Isotope-Effect Probes of Transition-State Structure. Vibrational Analysis of Model Transition States for Carbonyl Addition, J. Am. Chem. Soc. 102, 79-85.
93. Paneth, P., and O'Leary, M. H. (1991) Nitrogen and Deuterium Isotope Effects on Quaternization of N,N-Dimethyl-p-toluidine, J. Am. Chem. Soc. 113, 1691-1693.
94. Catrina, I. E., and Hengge, A. C. (2003) Comparisons of Phosphorothioate with Phosphate Transfer Reactions for a Monoester, Diester, and Triester: Isotope Effect Studies, J. Am. Chem. Soc. 125, 7546-7552.
95. Catrina, I. E., and Hengge, A. C. (1999) Comparisons of phosphorothioate and phosphate monoester transfer reactions: Activation parameters, solvent effects, and the effect of metal ions, J. Am. Chem. Soc. 121, 2156-2163.
96. Purcell, J., and Hengge, A. C. (2005) The Thermodynamics of Phosphate versus Phosphorothioate Ester Hydrolysis, J. Org. Chem. 70, 8437-8442.