Taking Ockham's razor to enzyme dynamics and catalysis

Nature Chemistry

Volumn 4, Issue 3, 2012, Pages 169-176

  Glowacki, David R ^a   Harvey, Jeremy N ^a   Mulholland, Adrian J ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME;

CATALYSIS; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; KINETICS; METABOLISM; PROTEIN CONFORMATION; REVIEW;

CATALYSIS; ENZYMES; KINETICS; MODELS, CHEMICAL; MODELS, MOLECULAR; PROTEIN CONFORMATION;

EID: 84857542642     PISSN: 17554330     EISSN: 17554349     Source Type: Journal    
DOI: 10.1038/nchem.1244     Document Type: Review

References (83)

1. Nagel, Z. D. & Klinman, J. P. A 21st century revisionist's view at a turning point in enzymology. Nature Chem. Biol. 5, 543-550 (2009).
2. Kamerlin, S. C. L. & Warshel, A. At the dawn of the 21st century: Is dynamics the missing link for understanding enzyme catalysis? Proteins 78, 1339-1375 (2010).
3. Rothlisberger, D. et al. Kemp elimination catalysts by computational enzyme design. Nature 453, 190-194 (2008).
4. Siebrand, W. & Smedarchina, Z. Model for the analysis of enzymatic proton-transfer reactions with an application to soybean lipoxygenase-1 and six mutants. J. Phys. Org. Chem. 23, 620-631 (2010).
5. Johannissen, L. O., Scrutton, N. S. & Sutcliffe, M. J. How does pressure affect barrier compression and isotope effects in an enzymatic hydrogen tunneling reaction? Angew. Chem. Int. Ed. 50, 2129-2132 (2011).
6. Schwartz, S. D. & Schramm, V. L. Enzymatic transition states and dynamic motion in barrier crossing. Nature Chem. Biol. 5, 552-559 (2009).
7. Masgrau, L. et al. Atomic description of an enzyme reaction dominated by proton tunneling. Science 312, 237-241 (2006).
8. Cha, Y., Murray, C. J. & Klinman, J. P. Hydrogen tunneling in enzyme reactions. Science 243, 1325-1330 (1989). (Pubitemid 19085368)
9. Basran, J., Sutcliffe, M. J. & Scrutton, N. S. Enzymatic H-transfer requires vibration-driven extreme tunneling. Biochemistry 38, 3218-3222 (1999).
10. Glickman, M. H. & Klinman, J. P. Nature of rate-limiting steps in the soybean lipoxygenase-1 reaction. Biochemistry 34, 14077-14092 (1995).
11. Forrest, L. R. et al. Mechanism for alternating access in neurotransmitter transporters. Proc. Natl Acad. Sci. USA 105, 10338-10343 (2008).
12. Pentikainen, U., Pentikainen, O. T. & Mulholland, A. J. Cooperative symmetric to asymmetric conformational transition of the apo-form of scavenger decapping enzyme revealed by simulations. Proteins 70, 498-508 (2008).
13. Strickland, N., Mulholland, A. J. & Harvey, J. N. The Fe-CO bond energy in myoglobin: A QM/MM study of the effect of tertiary structure. Biophys. J. 90, L27-L29 (2006).
14. Koshland, D. E. Application of a theory of enzyme specificity to protein synthesis. Proc. Natl. Acad. Sci. USA 44, 98-104 (1958).
15. Ma, B. Y. & Nussinov, R. Enzyme dynamics point to stepwise conformational selection in catalysis. Curr. Opin. Chem. Biol. 14, 652-659 (2010).
16. Zhou, H. X. From induced fit to conformational selection: A continuum of binding mechanism controlled by the timescale of conformational transitions. Biophys. J. 98, L15-L17 (2010).
17. Vértessy, B. G. & Orosz, F. From "fluctuation fit" to "conformational selection": Evolution, rediscovery, and integration of a concept. BioEssays 33, 30-34 (2011).
18. Van der Kamp, M. W., Perruccio, F. & Mulholland, A. J. High-level QM/MM modelling predicts an arginine as the acid in the condensation reaction catalysed by citrate synthase. Chem. Commun. 1874-1876 (2008). (Pubitemid 351503468)
19. Henzler-Wildman, K. A. et al. Intrinsic motions along an enzymatic reaction trajectory. Nature 450, 838-813 (2007).
20. Venkitakrishnan, R. P. et al. Conformational changes in the active site loops of dihydrofolate reductase during the catalytic cycle. Biochemistry 43, 16046-16055 (2004). (Pubitemid 40041018)
21. Min, W. et al. Fluctuating enzymes: Lessons from single-molecule studies. Accounts Chem. Res. 38, 923-931 (2005).
22. Lodola, A. et al. Conformational effects in enzyme catalysis: Reaction via a high energy conformation in fatty acid amide hydrolase. Biophys. J. 92, L20-L22 (2007). (Pubitemid 46145768)
23. Chouard, T. Breaking the protein rules. Nature 471, 151-153 (2011).
24. Tokuriki, N. & Tawfik, D. S. Protein dynamism and evolvability. Science 324, 203-207 (2009).
25. Wolf-Watz, M. et al. Linkage between dynamics and catalysis in a thermophilic-mesophilic enzyme pair. Nature Struct. Mol. Biol. 11, 945-949 (2004). (Pubitemid 39315297)
26. Daggett, V. Protein folding-simulation. Chem. Rev. 106, 1898-1916 (2006). (Pubitemid 43792785)
27. Warshel, A. Bicycle-pedal model for the first step in the vision process. Nature 260, 679-683 (1976).
28. Van der Kamp, M. W., Shaw, K. E., Woods, C. J. & Mulholland, A. J. Biomolecular simulation and modelling: Status, progress and prospects. J. R. Soc. Interface 5, S173-S190 (2008).
29. Lonsdale, R., Harvey, J. N., Manby, F. R. & Mulholland, A. J. Comment on "A stationary-wave model of enzyme catalysis" by Carlo Canepa. J. Comput. Chem. 32, 368-369 (2011).
30. McGeagh, J. D., Ranaghan, K. E. & Mulholland, A. J. Protein dynamics and enzyme catalysis: Insights from simulations. Biochim. Biophys. Acta 1814, 1077-1092 (2011).
31. Hammes-Schiffer, S. & Benkovic, S. J. Relating protein motion to catalysis. Annu. Rev. Biochem. 75, 519-541 (2006). (Pubitemid 44118042)
32. Benkovic, S. J. & Hammes-Schiffer, S. A perspective on enzyme catalysis. Science 301, 1196-1202 (2003). (Pubitemid 37052200)
33. Garcia-Viloca, M., Gao, J., Karplus, M. & Truhlar, D. G. How enzymes work: Analysis by modern rate theory and computer simulations. Science 303, 186-195 (2004). (Pubitemid 38057561)
34. Pisliakov, A. V., Cao, J., Kamerlin, S. C. L. & Warshel, A. Enzyme millisecond conformational dynamics do not catalyze the chemical step. Proc. Natl Acad. Sci. USA 106, 17359-17364 (2009).
35. Pu, J. Z., Gao, J. L. & Truhlar, D. G. Multidimensional tunneling, recrossing, and the transmission coefficient for enzymatic reactions. Chem. Rev. 106, 3140-3169 (2006). (Pubitemid 44376930)
36. Gilbert, R. G. & Smith, S. C. Theory of Unimolecular and Recombination Reactions (Blackwell, 1990).
37. Bowman, G. R. & Pande, V. S. Protein folded states are kinetic hubs. Proc. Natl Acad. Sci. USA 107, 10890-10895 (2010).
38. Huang, R. et al. Direct observation of the full transition from ballistic to diffusive Brownian motion in a liquid. Nature Phys. 7, 576-580 (2011).
39. Laidler, K. J. Chemical Kinetics 3rd edn (Harper International, 1987).
40. Lourderaj, U. & Hase, W. L. Theoretical and computational studies of non-RRKM unimolecular dynamics. J. Phys. Chem. A 113, 2236-2253 (2009).
41. Heazlewood, B. R. et al. Near-threshold H/D exchange in CD3CHO photodissociation. Nature Chem. 3, 443-448 (2011).
42. Glowacki, D. R. & Pilling, M. J. Unimolecular reactions of peroxy radicals in atmospheric chemistry and combustion. ChemPhysChem 11, 3836-3843 (2010).
43. Miller, J. A. & Klippenstein, S. J. Master equation methods in gas phase chemical kinetics. J. Phys. Chem. A 110, 10528-10544 (2006). (Pubitemid 44547240)
44. Glowacki, D. R., Liang, C. H., Marsden, S. P., Harvey, J. N. & Pilling, M. J. Alkene hydroboration: Hot intermediates that react while they are cooling. J. Am. Chem. Soc. 132, 13621-13623 (2010).
45. Greaves, S. J. et al. Vibrationally quantum-state-specific reaction dynamics of H atom abstraction by CN radical in solution. Science 331, 1423-1426 (2011).
46. Glowacki, D. R., Marsden, S. P. & Pilling, M. J. Significance of nonstatistical dynamics in organic reaction mechanisms: Time-dependent stereoselectivity in cyclopentyne-alkene cycloadditions. J. Am. Chem. Soc. 131, 13896-13897 (2009).
47. 2 kinetics at high pressures. Phys. Chem. Chem. Phys. 11, 963-974 (2009).
48. Harvey, J. N. Ab initio transition state theory for polar reactions in solution. Faraday Discuss. 145, 487-505 (2010).
49. Cooper, A. Protein heat capacity: An anomaly that maybe never was. J. Phys. Chem. Lett. 1, 3298-3304 (2010).
50. Knapp, M. J., Rickert, K. & 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). (Pubitemid 34310901)
51. Loveridge, E. J., Tey, L. H. & Allemann, R. K. Solvent effects on catalysis by Escherichia coli dihydrofolate reductase. J. Am. Chem. Soc. 132, 1137-1143 (2010).
52. Sikorski, R. S. et al. Tunneling and coupled motion in the Escherichia coli dihydrofolate reductase catalysis. J. Am. Chem. Soc. 126, 4778-4779 (2004). (Pubitemid 38490135)
53. 2. Science 331, 448-450 (2011).
54. 3 reaction. Science 306, 2227-2229 (2004). (Pubitemid 40024453)
55. Claeyssens, F. et al. High-accuracy computation of reaction barriers in enzymes. Angew. Chem. Int. Ed. 45, 6856-6859 (2006). (Pubitemid 44654476)
56. Kanaan, N., Roca, M., Tunon, I., Marti, S. & Moliner, V. Application of Grote-Hynes theory to the reaction catalyzed by thymidylate synthase. J. Phys. Chem. B 114, 13593-13600 (2010).
57. Alhambra, C., Sanchez, M. L., Corchado, J. C., Gao, J. & Truhlar, D. G. Quantum mechanical tunneling in methylamine dehydrogenase. Chem. Phys. Lett. 347, 512-518 (2001); (Pubitemid 33628552)
58. Erratum ibid. 355, 388-394 (2002).
59. Lonsdale, R., Harvey, J. N. & Mulholland, A. J. Compound I reactivity defines alkene oxidation selectivity in cytochrome P450cam. J. Phys. Chem. B 114, 1156-1162 (2010).
60. Truhlar, D. G. Tunneling in enzymatic and nonenzymatic hydrogen transfer reactions. J. Phys. Org. Chem. 23, 660-676 (2010).
61. Lodola, A. et al. Structural fluctuations in enzyme-catalyzed reactions: Determinants of reactivity in fatty acid amide hydrolase from multivariate statistical analysis of quantum mechanics/molecular mechanics paths. J. Chem. Theory Comput. 6, 2948-2960 (2010).
62. Warshel, A. & Weiss, R. M. An empirical valence bond approach for comparing reactions in solutions and in enzymes. J. Am. Chem. Soc. 102, 6218-6226 (1980).
63. Glowacki, D. R., Paci, E. & Shalashilin, D. V. Boxed molecular dynamics: A simple and general technique for accelerating rare event kinetics and mapping free energy in large molecular systems. J. Phys. Chem. B 113, 16603-16611 (2009).
64. Greaves, S. J. et al. Vibrational excitation through tug-of-war inelastic collisions. Nature 454, 88-91 (2008). (Pubitemid 351931981)
65. Glowacki, D. R., Rose, R. A., Greaves, S. J., Orr-Ewing, A. J. & Harvey, J. N. Ultrafast energy flow in the wake of solution-phase bimolecular reactions. Nature Chem. 3, 850-855 (2011).
66. Glowacki, D. R., Orr-Ewing, A. J. & Harvey, J. N. Product energy deposition of CN + alkane H abstraction reactions in gas and solution phases. J. Chem. Phys. 134, 214508 (2011).
67. Ruggiero, G. D., Williams, I. H., Roca, M., Moliner, V. & Tunon, I. QM/MM determination of kinetic isotope effects for COMT-catalyzed methyl transfer does not support compression hypothesis. J. Am. Chem. Soc. 126, 8634-8635 (2004). (Pubitemid 38955711)
68. Strajbl, M., Shurki, A., Kato, M. & Warshel, A. Apparent NAC effect in chorismate mutase reflects electrostatic transition state stabilization. J. Am. Chem. Soc. 125, 10228-10237 (2003). (Pubitemid 37022233)
69. Liu, H. B. & Warshel, A. The catalytic effect of dihydrofolate reductase and its mutants is determined by reorganization energies. Biochemistry 46, 6011-6025 (2007). (Pubitemid 46799163)
70. Dybala-Defratyka, A., Paneth, P., Banerjee, R. & Truhlar, D. G. Coupling of hydrogenic tunneling to active-site motion in the hydrogen radical transfer catalyzed by a coenzyme B-12-dependent mutase. Proc. Natl Acad. Sci. USA 104, 10774-10779 (2007). (Pubitemid 47175177)
71. Zuev, P. S. et al. Carbon tunneling from a single quantum state. Science 299, 867-870 (2003). (Pubitemid 36182440)
72. Schreiner, P. R. et al. Capture of hydroxymethylene and its fast disappearance through tunnelling. Nature 453, 906-942 (2008).
73. Brunton, G., Griller, D., Barclay, L. R. C. & Ingold, K. U. Kinetic applications of electron paramagnetic resonance spectroscopy. 26. Quantum-mechanical tunneling in the isomerization of sterically hindered aryl radicals. J. Am. Chem. Soc. 98, 6803-6811 (1976).
74. Olsson, M. H. M., Siegbahn, P. E. M. & Warshel, A. Simulations of the large kinetic isotope effect and the temperature dependence of the hydrogen atom transfer in lipoxygenase. J. Am. Chem. Soc. 126, 2820-2828 (2004). (Pubitemid 38314288)
75. Liu, H. B. & Warshel, A. Origin of the temperature dependence of isotope effects in enzymatic reactions: The case of dihydrofolate reductase. J. Phys. Chem. B 111, 7852-7861 (2007). (Pubitemid 47169697)
76. Williams, I. H. Quantum catalysis? A comment on tunnelling contributions for catalysed and uncatalysed reactions. J. Phys. Org. Chem. 23, 685-689 (2010).
77. Masgrau, L., Ranaghan, K. E., Scrutton, N. S., Mulholland, A. J. & Sutcliffe, M. J. Tunneling and classical paths for proton transfer in an enzyme reaction dominated by tunneling: Oxidation of tryptamine by aromatic amine dehydrogenase. J. Phys. Chem. B 111, 3032-3047 (2007). (Pubitemid 46543293)
78. Ranaghan, K. E., Masgrau, L., Scrutton, N. S., Sutcliffe, M. J. & Mulholland, A. J. Analysis of classical and quantum paths for deprotonation of methylamine by methylamine dehydrogenase. ChemPhysChem 8, 1816-1835 (2007).
79. Hay, S., Sutcliffe, M. J. & Scrutton, N. S. Promoting motions in enzyme catalysis probed by pressure studies of kinetic isotope effects. Proc. Natl Acad. Sci. USA 104, 507-512 (2007). (Pubitemid 46123055)
80. Pang, J. Y., Pu, J. Z., Gao, J. L., Truhlar, D. G. & Allemann, R. K. Hydride transfer reaction catalyzed by hyperthermophilic dihydrofolate reductase is dominated by quantum mechanical tunneling and is promoted by both inter-and intramonomeric correlated motions. J. Am. Chem. Soc. 128, 8015-8023 (2006). (Pubitemid 43945743)
81. Agmon, N. & Hopfield, J. J. CO binding to heme proteins: A model for barrier height distributions and slow conformational changes. J. Chem. Phys. 79, 2042-2053 (1983).
82. Knowles, J. R. Enzyme catalysis: Not different, just better. Nature 350, 121-124 (1991). (Pubitemid 21912173)
83. Skodje, R. T. & Truhlar, D. G. Parabolic tunneling calculations. J. Phys. Chem. 85, 624-628 (1981).