Kinetic isotope effects for proton-coupled electron transfer reactions

Isotope Effects in Chemistry and Biology

Volumn , Issue , 2005, Pages 499-519

  Hammes Schiffer, Sharon ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85056381668     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1201/9781420028027     Document Type: Chapter

References (99)

1. Babcock, G. T., Barry, B. A., Debus, R. J., Hoganson, C. W., Atamian, M., McIntosh, L., Sithole, I., and Yocum, C. F., Water oxidation in photosystem 2: from radical chemistry to multielectron chemistry, Biochemistry, 28, 9557-9565, 1989.
2. Okamura, M. Y. and Feher, G., Proton-transfer in reaction centers from photosynthetic bacteria, Annu. Rev. Biochem., 61, 861-896, 1992.
3. Tommos, C., Tang, X.-S., Warncke, K., Hoganson, C. W., Styring, S., McCracken, J., Diner, B. A., and Babcock, G. T., Spin-density distribution, conformation, and hydrogen bonding of the redox-active tyrosine YZ in photosystem II from multiple electron magnetic-resonance spectroscopies: implications for photosynthetic oxygen evolution, J. Am. Chem. Soc., 117, 10325-10335, 1995.
4. Hoganson, C. W. and Babcock, G. T., A metalloradical mechanism for the generation of oxygen from water in photosynthesis, Science, 277, 1953-1956, 1997.
5. Hoganson, C. W., Lydakis-Simantiris, N., Tang, X.-S., Tommos, C., Warncke, K., Babcock, G. T., Diner, B. A., McCracken, J., and Styring, S., A hydrogen-atom abstraction model for the function of YZ in photosynthetic oxygen evolution, Photosynth. Res., 47, 177-184, 1995.
6. Blomberg, M. R. A., Siegbahn, P. E. M., Styring, S., Babcock, G. T., Akermark, B., and Korall, P., A quantum chemical study of hydrogen abstraction from manganese-coordinated water by a tyrosyl radical: a model for water oxidation in photosystem II, J. Am. Chem. Soc., 119, 8285-8292, 1997.
7. Diner, B. A. and Babcock, G. T., Structure, dynamics and energy conversion efficiency in photosystem II, In Oxygenic Photosynthesis: The Light Reactions, Ort, D. R. and Yocum, C. F., Eds., Kluwer, Dordrecht, The Netherlands, pp. 213-247, 1996.
8. Babcock, G. T. and Wikstrom, M., Oxygen activation and the conservation of energy in cell respiration, Nature, 356, 301-309, 1992.
9. Malmstrom, B. G., Vectorial chemistry in bioenergetics-cytochrome c oxidase as a redox-linked proton pump, Acc. Chem. Res., 26, 332-338, 1993.
10. Siegbahn, P. E. M., Eriksson, L., Himo, F., and Pavlov, M., Hydrogen atom transfer in ribonucleotide reductase (RNR), J. Phys. Chem. B, 102, 10622-10629, 1998.
11. Roth, J. P., Lovel, S., and Mayer, J. M., Intrinsic barriers for electron and hydrogen atom transfer reactions of biomimetic iron complexes, J. Am. Chem. Soc., 122, 5486-5498, 2000.
12. Sjodin, M., Styring, S., Akermark, B., Sun, L., and Hammarstrom, L., Proton-coupled electron transfer from tyrosine in a tyrosine-ruthenium-tris-bipyridine complex: comparison with tyrosinez oxidation in photosystem II, J. Am. Chem. Soc., 122, 3932-3936, 2000.
13. Binstead, R. A. and Meyer, T. J., H-atom transfer between metal complex ions in solution, J. Am. Chem. Soc., 109, 3287-3297, 1987.
14. Farrer, B. T. and Thorp, H. H., Driving force and isotope dependence of the kinetics of proton-coupled electron transfer in oxoruthenium (IV) polypyridyl complexes, Inorg. Chem., 38, 2497-2502, 1999.
15. Huynh, M. H. V. and Meyer, T. J., Proton-coupled electron transfer from phosphorus: a P-H/P-D kinetic isotope effect of 178, Angew. Chem. Int. Ed., 41, 1395-1398, 2002.
16. Huynh, M.H. and Meyer, T.J., personal communication, 2003.
17. Bahnson, B. J., Park, D. H., Kim, K., Plapp, B. V., and Klinman, J. P., Unmasking of hydrogen tunneling in the horse liver alcohol dehydrogenase reaction by site-directed mutagenesis, Biochemistry, 32, 5503-5507, 1993.
18. Bahnson, B. J. and Klinman, J. P., Hydrogen tunneling in enzyme catalysis, Methods Enzymol., 249, 373-397, 1995.
19. Fierke, C. A., Johnson, K. A., and Benkovic, S. J., Construction and evaluation of the kinetic scheme associated with dihydrofolate reductase from Escherichia coli, Biochemistry, 26, 4085-4092, 1987.
20. Rickert, K. W. and Klinman, J. P., Nature of hydrogen transfer in soybean lipoxygenase 1: separation of primary and secondary isotope effects, Biochemistry, 38, 12218-12228, 1999.
21. Jonsson, T., Glickman, M. H., Sun, S., and Klinman, J. P., Experimental evidence for extensive tunneling of hydrogen in the lipoxygenase reaction: implications for enzyme catalysis, J. Am. Chem. Soc., 118, 10319-10320, 1996.
22. Glickman, M. H., Wiseman, J. S., and Klinman, J. P., Extremely large isotope effects in the soybean lipoxygenase-linoleic acid reaction, J. Am. Chem. Soc., 116, 793-794, 1994.
23. Hwang, C.-C. and Grissom, C. B., Unusually large deuterium isotope effect in soybean lipoxygenase is not caused by a magnetic isotope effect, J. Am. Chem. Soc., 116, 795-796, 1994.
24. Knapp, M. J., Rickert, K. W., and Klinman, J. P., Temperature dependent isotope effects in soybean lipoxygenase-1: correlating hydrogen tunneling with protein dynamics, J. Am. Chem. Soc., 124, 3865-3874, 2002.
25. Soudackov, A. and Hammes-Schiffer, S., Multistate continuum theory for multiple charge transfer reactions in solution, J. Chem. Phys., 111, 4672-4687, 1999.
26. Soudackov, A. and Hammes-Schiffer, S., Derivation of rate expressions for nonadiabatic protoncoupled electron transfer reactions in solution, J. Chem. Phys., 113, 2385-2396, 2000.
27. Hammes-Schiffer, S., Theoretical perspectives on proton-coupled electron transfer reactions, Acc. Chem. Res., 34, 273-281, 2001.
28. Iordanova, N., Decornez, H., and Hammes-Schiffer, S., Theoretical study of electron, proton, and proton-coupled electron transfer reactions in iron bi-imidazoline complexes, J. Am. Chem. Soc., 123, 3723-3733, 2001.
29. Carra, C., Iordanova, N., and Hammes-Schiffer, S., Proton-coupled electron transfer in a model for tyrosine oxidation in photosystem II, J. Am. Chem. Soc., 125, 10429-10436, 2003.
30. Iordanova, N. and Hammes-Schiffer, S., Theoretical investigation of large kinetic isotope effects for proton-coupled electron transfer in ruthenium polypyridyl complexes, J. Am. Chem. Soc., 124, 4848-4856, 2002.
31. Iordanova, N., Theoretical Investigations of Proton-Coupled Electron Transfer Reactions in Condensed Phases, Chemistry Department, Pennsylvania State University, University Park, 2003.
32. Hatcher, E., Soudackov, A. V., and Hammes-Schiffer, S., Proton-coupled electron transfer in soybean lipoxygenase, J. Am. Chem. Soc., 126, 5763-5775, 2004.
33. Billeter, S. R., Webb, S. P., Iordanov, T., Agarwal, P. K., and Hammes-Schiffer, S., Hybrid approach for including electronic and nuclear quantum effects in molecular dynamics simulations of hydrogen transfer reactions in enzymes, J. Chem. Phys., 114, 6925-6936, 2001.
34. Billeter, S. R., Webb, S. P., Agarwal, P. K., Iordanov, T., and Hammes-Schiffer, S., Hydride transfer in liver alcohol dehydrogenase: quantum dynamics, kinetic isotope effects, and the role of enzyme motion, J. Am. Chem. Soc., 123, 11262-11272, 2001.
35. Warshel, A., Computer Modeling of Chemical Reactions in Enzymes and Solutions, Wiley, New York, 1991.
36. Webb, S. P. and Hammes-Schiffer, S., Fourier grid Hamiltonian multiconfigurational self consistent field: a method to calculate multidimensional hydrogen vibrational wavefunctions, J. Chem. Phys., 113, 5214-5227, 2000.
37. Agarwal, P. K., Billeter, S. R., and Hammes-Schiffer, S., Nuclear quantum effects and enzyme dynamics in dihydrofolate reductase catalysis, J. Phys. Chem. B, 106, 3283-3293, 2002.
38. Agarwal, P. K., Billeter, S. R., Rajagopalan, P. T. R., Benkovic, S. J., and Hammes-Schiffer, S., Network of coupled promoting motions in enzyme catalysis, Proc. Natl Acad. Sci., 99, 2794-2799, 2002.
39. Watney, J. B., Agarwal, P. K., and Hammes-Schiffer, S., Effect of mutation on enzyme motion in dihydrofolate reductase, J. Am. Chem. Soc., 125, 3745-3750, 2003.
40. Marcus, R. A., Chemical and electrochemical electron-transfer theory, Annu. Rev. Phys. Chem., 15, 155-196, 1964.
41. Marcus, R. A. and Sutin, N., Electron transfers in chemistry and biology, Biochim. Biophys. Acta, 811, 265-322, 1985.
42. Zusman, L. D., Outer-sphere electron transfer in polar solvents, Chem. Phys., 49, 295-304, 1980.
43. Warshel, A., Dynamics of reactions in polar solvents: semiclassical trajectory studies of electrontransfer and proton-transfer reactions, J. Phys. Chem., 86, 2218, 1982.
44. King, G. and Warshel, A., Investigation of the free energy functions for electron transfer reactions, J. Chem. Phys., 93, 8682-8692, 1990.
45. Calef, D. F. and Wolynes, P. G., Classical solvent dynamics and electron transfer: 1. Continuum theory, J. Phys. Chem., 87, 3387-3400, 1983.
46. Newton, M. D. and Sutin, N., Electron transfer reactions in condensed phases, Annu. Rev. Phys. Chem., 35, 437-480, 1984.
47. Bixon, M. and Jortner, J., Electron transfer from isolated molecules to biomolecules, Adv. Chem. Phys., 106, 35-202, 1999.
48. Barbara, P. F., Meyer, T. J., and Ratner, M. A., Contemporary issues in electron transfer research, J. Phys. Chem., 100, 13148-13168, 1996.
49. Levich, V. G., Classical solvent dynamics and electron transfer: 1. Continuum theory, J. Phys. Chem., 87, 3387-3400, 1983.
50. Kestner, N. R., Logan, J., and Jortner, J., J. Phys. Chem., 78, 2148, 1974.
51. Ulstrup, J. and Jortner, J., J. Chem. Phys., 63, 4358, 1975.
52. Borgis, D. and Hynes, J. T., Dynamical theory of proton tunneling transfer rates in solution: general formulation, Chem. Phys., 170, 315-346, 1993.
53. Basilevsky, M. V. and Vener, M. V., Collective medium coordinates and their application in the theory of chemical reactions, J. Mol. Struct.: THEOCHEM, 398, 81, 1997.
54. Hammes-Schiffer, S., Proton-coupled electron transfer, In Electron Transfer in Chemistry, Principles, Theories, Methods, and Techniques, Vol. I, Balzani, V., Ed., Wiley-VCH, Weinheim, pp. 189-214, 2001.
55. Kim, S.-Y. and Hammes-Schiffer, S., Molecular dynamics with quantum transitions for proton transfer:quantum treatment of hydrogen and donor-acceptor motions, J. Chem. Phys., 119, 4389-4398, 2003.
56. Borgis, D. and Hynes, J. T., Curve crossing formulation for proton transfer reactions in solution, J. Phys. Chem., 100, 1118-1128, 1996.
57. Kuznetsov, A. M. and Ulstrup, J., Can. J. Chem., 77, 1085-1096, 1999.
58. Kiefer, P. M. and Hynes, J. T., J. Phys. Chem. A, 106, 1834, 2002.
59. Kiefer, P. M. and Hynes, J. T., J. Phys. Chem. A, 106, 1850, 2002.
60. Staib, A., Borgis, D., and Hynes, J. T., Proton transfer in hydrogen bonded acid-base complexes in polar solvents, J. Chem. Phys., 102, 2487-2505, 1995.
61. Cukier, R. I., Proton-coupled electron transfer reactions: evaluation of rate constants, J. Phys. Chem., 100, 15428-15443, 1996.
62. Cukier, R. I. and Nocera, D. G., Proton-coupled electron transfer, Annu. Rev. Phys. Chem., 49, 337-369, 1998.
63. Mayer, J. M., Hrovat, D. A., Thomas, J. L., and Borden, W. T., Proton-coupled electron transfer versus hydrogen atom transfer in benzyl/toluene, methoxyl/methanol, and phenoxyl/phenol self-exchange reactions, J. Am. Chem. Soc., 124, 11142-11147, 2002.
64. Soudackov, A.V., Hatcher, E., and Hammes-Schiffer, S., J. Chem. Phys., 122, 014505, 2005.
65. Zhou, Z. and Khan, S. U. M., Inner-sphere reorganization energy of ions in solution: a molecular orbital calculation, J. Phys. Chem., 93, 5292-5295, 1989.
66. Basilevsky, M. V., Rostov, I. V., and Newton, M. D., A frequency-resolved cavity model (FRCM) for treating equilibrium and non-equilibrium solvation energies, Chem. Phys., 232, 189-199, 1998.
67. Newton, M. D., Basilevsky, M. V., and Rostov, I. V., A frequency-resolved cavity model (FRCM) for treating equilibrium and non-equilibrium solvation energies 2: evaluation of solvent reorganization energies, Chem. Phys., 232, 201-210, 1998.
68. Neria, E. and Karplus, M., A position dependent friction model for solution reactions in the high friction regime: proton transfer in triosephosphate isomerase (TIM), J. Chem. Phys., 105, 10812-10818, 1996.
69. Bennett, C. H., Algorithms for Chemical Computation, Christofferson, R. E., Ed., American Chemical Society, Washington, DC, 1997.
70. Keck, J. C., Variational theory of chemical reaction rates applied to three-body recombinations, J. Chem. Phys., 32, 1035-1050, 1960.
71. Anderson, J. B., Statistical theories of chemical reactions. Distributions in the transition region, J. Chem. Phys., 58, 4684-4692, 1973.
72. Chandler, D., A story of rare events: from barriers, to electrons, to unknown pathways, In Classical and Quantum Dynamics in Condensed Phase Simulations, Berne, B. J., Ciccotti, G., and Coker, D. F., Eds., World Scientific, Singapore, pp. 3-23, 1998.
73. Tully, J. C., Molecular dynamics with electronic transitions, J. Chem. Phys., 93, 1061-1071, 1990.
74. Hammes-Schiffer, S., Mixed quantum/classical dynamics of hydrogen transfer reactions, J. Phys. Chem. A, 102, 10443-10454, 1998.
75. Rajagopalan, P. T. R., Lutz, S., and Benkovic, S. J., Coupling interactions of distal residues enhance dihydrofolate reductase catalysis: mutational effects on hydride transfer rates, Biochemistry, 41, 12618-12628, 2002.
76. Cameron, C. E. and Benkovic, S. J., Evidence for a functional role of the dynamics of glycine-121 of Escherichia coli dihydrofolate reductase obtained from kinetic analysis of a site-directed mutant, Biochemistry, 36, 15792-15800, 1997.
77. Samuelsson, B., Dahlen, S.-E., Lindgren, J., Rouzer, C. A., and Serhan, C. N., Leukotrienes and lipoxins: structures, biosynthesis, and biological effects, Science, 237, 1171-1176, 1987.
78. Holman, T. R., Zhou, J., and Solomon, E. L., Spectroscopic and functional characterization of a ligand coordination mutant of soybean lipoxygenase-1: first coordination sphere analogue of human 15- lipoxygenase, J. Am. Chem. Soc., 120, 12564-12572, 1998.
79. Glickman, M. H. and Klinman, J. P., Nature of rate-limiting steps in the soybean lipoxygenase-1 reaction, Biochemistry, 34, 14077-14092, 1995.
80. Lewis, E. R., Johansen, E., and Holman, T. R., Large competitive kinetic isotope effects in human 5- lipoxygenase catalysis measured by a novel HPLC method, J. Am. Chem. Soc., 121, 1395-1396, 1999.
81. Lehnert, N. and Solomon, E. L., Density-functional investigation on the mechanism of H-atom abstraction by lipoxygenase, J. Biol. Inorg. Chem., 8, 294-305, 2003.
82. Bahnson, B. J., Colby, T. D., Chin, J. K., Goldstein, B. M., and Klinman, J. P., A link between protein structure and enzyme catalyzed hydrogen tunneling, Proc. Natl Acad. Sci. USA, 94, 12797-12802, 1997.
83. Rucker, J. and Klinman, J. P., Computational study of tunneling and coupled motion in alcohol dehydrogenase-catalyzed reactions: implication for measured hydrogen and carbon isotope effects, J. Am. Chem. Soc., 121, 1997-2006, 1999.
84. Alhambra, C., Corchado, J. C., Sanchez, M. L., Gao, J. L., and Truhlar, D. G., Quantum dynamics of hydride transfer in enzyme catalysis, J. Am. Chem. Soc., 122, 8197-8203, 2000.
85. Webb, S. P., Agarwal, P. K., and Hammes-Schiffer, S., Combining electronic structure methods with the calculation of hydrogen vibrational wavefunctions: application to hydride transfer in liver alcohol dehydrogenase, J. Phys. Chem. B, 104, 8884-8894, 2000.
86. 2O-, and HLADH-NADH-PhCHO, J. Am. Chem. Soc., 123, 11952-11959, 2001.
87. Villa, J. and Warshel, A., Energetics and dynamics of enzymatic reactions, J. Phys. Chem. B, 105, 7887-7907, 2001.
88. Caratzoulas, S., Mincer, J. S., and Schwartz, S. D., Identification of a protein-promoting vibration in the reaction catalyzed by horse liver alcohol dehydrogenase, J. Am. Chem. Soc., 124, 3270-3276, 2002.
89. Miller, G. P. and Benkovic, S. J., Stretching exercises-flexibility in dihydrofolate reductase catalysis, Chem. Biol., 5, R105-R113, 1998.
90. Sawaya, M. R. and Kraut, J., Loop and subdomain movements in the mechanism of Escherichia coli dihydrofolate reductase: crystallographic evidence, Biochemistry, 36, 586-603, 1997.
91. Falzone, C. J., Wright, P. E., and Benkovic, S. J., Dynamics of a flexible loop in dihydrofolate reductase from Escherichia coli and its implication for catalysis, Biochemistry, 33, 439-442, 1994.
92. Osborne, M. J., Schnell, J., Benkovic, S. J., Dyson, H. J., and Wright, P. E., Backbone dynamics in dihydrofolate reductase complexes: role of loop flexibility in the catalytic mechanism, Biochemistry, 40, 9846-9859, 2001.
93. Radkiewicz, J. L. and Brooks, C. L., Protein dynamics in enzymatic catalysis: exploration of dihydrofolate reductase, J. Am. Chem. Soc., 122, 225-231, 2000.
94. Rod, T. H., Radkiewicz, J. L., and Brooks, C. L. III, Correlated motion and the effect of distal mutations in dihydrofolate reductase, Proc. Natl Acad. USA, 100, 6980-6985, 2003.
95. Garcia-Viloca, M., Truhlar, D. G., and Gao, J., Reaction-path energetics and kinetics of the hydride transfer reaction catalyzed by dihydrofolate reductase, Biochemistry, 42, 13558-13575, 2003.
96. Hammes-Schiffer, S., Impact of enzyme motion on activity, Biochemistry, 41, 13335-13343, 2002.
97. Bruno, W. J. and Bialek, W., Vibrationally enhanced tunneling as a mechanism for enzymatic hydrogen transfer, Biophys. J., 63, 689-699, 1992.
98. Antoniou, D., Caratzoulas, S., Kalyanaraman, C., Mincer, J. S., and Schwartz, S. D., Barrier passage and protein dynamics in enzymatically catalyzed reactions, Eur. J. Biochem., 269, 3103-3112, 2002.
99. Benkovic, S. J. and Hammes-Schiffer, S., A perspective on enzyme catalysis, Science, 301, 1196, 2003.