The enzyme aromatic amine dehydrogenase induces a substrate conformation crucial for promoting vibration that significantly reduces the effective potential energy barrier to proton transfer

Journal of the Royal Society Interface

Volumn 5, Issue SUPPL. 3, 2008, Pages

  Johannissen, Linus O ^a   Scrutton, Nigel S ^b   Sutcliffe, Michael J ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Hydrogen tunnelling; Kinetic isotope effect; Molecular dynamics; Promoting vibrations

Indexed keywords

AROMATIC COMPOUNDS; ENERGY BARRIERS; ENZYMES; MOLECULAR PHYSICS; POTENTIAL ENERGY; PROTON TRANSFER; REACTION KINETICS; VIBRATIONS (MECHANICAL);

AMINE DEHYDROGENASE; AROMATIC AMINES; CATALYTIC EFFECTS; EFFECTIVE POTENTIALS; HYDROGEN TUNNELING; IMINOQUINONE; KINETIC ISOTOPES EFFECTS; POTENTIAL ENERGY BARRIER; PROMOTING VIBRATION; QUANTUM MECHANICAL/MOLECULAR MECHANICAL;

MOLECULAR DYNAMICS;

ARALKYLAMINE DEHYDROGENASE; HYDROGEN; IMINOQUINONE; OXIDOREDUCTASE; PROTON; QUINONE DERIVATIVE; TRYPTAMINE; TRYPTAMINE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; COMPARATIVE STUDY; ENZYME ACTIVE SITE; QUANTUM THEORY; VIBRATION;

CATALYTIC DOMAIN; HYDROGEN; MODELS, CHEMICAL; MODELS, MOLECULAR; OXIDOREDUCTASES ACTING ON CH-NH GROUP DONORS; PROTONS; QUANTUM THEORY; QUINONES; TRYPTAMINES; VIBRATION;

EID: 58749097088     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2008.0068.focus     Document Type: Article

References (40)

1. Agarwal, P. K., Billeter, S. R. & Hammes-Schiffer, S. 2002a Nuclear quantum effects and enzyme dynamics in dihy-drofolate reductase catalysis. J. Phys. Chem. B 106, 3283-3293. (doi:10.1021/jp020190v) (Pubitemid 35290281)
2. Agarwal, P. K., Billeter, S. R., Rajagopalan, P. T., Benkovic, S. J. & Hammes-Schiffer, S. 2002b Network of coupled promoting motions in enzyme catalysis. Proc. Natl Acad. Sci. USA 99, 2794-2799. (doi:10.1073/pnas.052005999) (Pubitemid 34240540)
3. Alhambra, C., Corchado, J., Sanchez, M.L., Garcia-Viloca, M., Gao, J. & 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, 11 326-11 340. (doi:10.1021/jp0120312) (Pubitemid 35338485)
4. Ball, P. 2004 Enzymes: by chance, or by design? Nature 431, 396-397. (doi:10.1038/431396a) (Pubitemid 39329558)
5. Benkovic, S. J. & Hammes-Schiffer, S. 2003 A perspective on enzyme catalysis. Science 301, 1196-1202. (doi:10.1126/science.1085515) (Pubitemid 37052200)
6. Billeter, S. R., Webb, S. P., Agarwal, P. K., Iordanov, T. & Hammes-Schiffer, S. 2001 Hydride transfer in liver alcohol dehydrogenase: quantum dynamics, kinetic isotope effects, and role of enzyme motion. J. Am. Chem. Soc. 123, 11 262-11 272. (doi:10.1021/ja011384b) (Pubitemid 33065363)
7. Brooks, B. R., Bruccoleri, R. E., Olafson, B. D., States, D. J., Swaminathan, S. & Karplus, M. 1983 CHARMM-a program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4, 187-217. (doi:10.1002/jcc.540040211)
8. Caratzoulas, S., Mincer, J. S. & Schwartz, S. D. 2002 Identification of a protein-promoting vibration in the reaction catalyzed by horse liver alcohol dehydrogenase. J. Am. Chem. Soc. 124, 3270-3276. (doi:10.1021/ja017146y) (Pubitemid 34270366)
9. Cui, Q. & Karplus, M. 2002 Quantum mechanics/molecular mechanics studies of triosephosphate isomerase-catalyzed reactions: effect of geometry and tunneling on proton-transfer rate constants. J. Am. Chem. Soc. 124, 3093-3124. (doi:10.1021/ja0118439) (Pubitemid 34249983)
10. Dybala-Defratyka, A., Paneth, P., Banerjee, R. & Truhlar, D. G. 2007 Coupling of hydrogenic tunneling to active-site motion in the hydrogen radical transfer catalyzed by a coenzyme B12-dependent mutase. Proc. Natl Acad. Sci. USA 104, 10 774-10 779. (doi:10.1073/pnas.0702188104) (Pubitemid 47175177)
11. Field, M. J., Bash, P. A. & Karplus, M. 1990 A combined quantum-mechanical and molecular mechanical potential for molecular-dynamics simulations. J. Comput. Chem. 11, 700-733. (doi:10.1002/jcc.540110605)
12. Gao, J. & Truhlar, D. G. 2002 Quantum mechanical methods for enzyme kinetics. Annu. Rev. Phys. Chem. 53, 467-505. (doi:10.1146/annurev.physchem.53. 091301.150114) (Pubitemid 35336261)
13. Garcia-Viloca, M., Alhambra, C., Truhlar, D. G. & Gao, J. 2001 Inclusion of quantum-mechanical vibrational energy in reactive potentials of mean force. J. Chem. Phys. 114, 9953-9958. (doi:10.1063/1.1371497) (Pubitemid 32586000)
14. Garcia-Viloca, M., Truhlar, D. G. & Gao, J. 2003 Reaction-path energetics and kinetics of the hydride transfer reaction catalyzed by dihydrofolate reductase. Biochemistry 42, 13 558-13 575. (doi:10.1021/bi034824f) (Pubitemid 37444907)
15. Hammes-Schiffer, S. 2006 Hydrogen tunneling and protein motion in enzyme reactions. Acc. Chem. Res. 39, 93-100. (doi:10.1021/ar040199a)
16. Hay, S., Sutcliffe, M. J. & Scrutton, N. S. 2007 Promoting motions in enzyme catalysis probed by pressure studies of kinetic isotope effects. Proc. Natl Acad. Sci. USA 104, 507-512. (doi:10.1073/pnas.0608408104) (Pubitemid 46123055)
17. Henzler-Wildman, K.&Kern, D.2007 Dynamic personalities of proteins. Nature 450, 964-972. (doi:10.1038/nature06522) (Pubitemid 350273626)
18. Hothi, P., Lee, M., Cullis, P.M., Leys, D.& Scrutton, N.S.2008 Catalysis by the isolated tryptophan tryptophylquinone-containing subunit of aromatic amine dehydrogenase is distinctfrom nativeenzymeandsynthetic model compounds and allows further probing of TTQ mechanism. Biochemistry 47, 183-194. (doi:10.1021/bi701690u)
19. Jezierska, A., Panek, J. J., Koll, A. & Mavri, J. 2007 Car-Parrinello simulation of an O-H stretching envelope and potential of mean force of an intramolecular hydrogen bonded system: application to a Mannich base in solid state and in vacuum. J. Chem. Phys. 126, 205 101-205 109. (doi:10.1063/1. 2736692) (Pubitemid 46872212)
20. Johannissen, L. O., Hay, S., Scrutton, N. S. & Sutcliffe, M. J. 2007 Proton tunneling in aromatic amine dehydrogenase is driven by a short-range sub-picosecond promoting vibration: consistency of simulation and theory with experiment. J. Phys. Chem. B 111, 2631-2638. (doi:10. 1021/jp066276w) (Pubitemid 46548747)
21. Knapp, M. J., Rickert, K. & Klinman, J. P. 2002 Temperature-dependent isotope effects in soybean lipoxygenase-1: correlating hydrogen tunneling with protein dynamics. J. Am. Chem. Soc. 124, 3865-3874. (doi:10.1021/ja012205t) (Pubitemid 34310901)
22. Kohen, A. 2006 Current issues in enzymatic hydrogen transfer from carbon: tunneling and coupled motion from kinetic isotope effect studies. In Hydrogen transfer reactions, vol. 4 (eds J. T. Hynes, J. P. Klinman, H. H. Limbach & R. L. Schowen), pp. 1311-1340. Weinheim, Germany: Wiley.
23. Liu, H. & Warshel, A. 2007a The catalytic effect of dihydrofolate reductase and its mutants is determined by reorganization energies. Biochemistry 46, 6011-6025. (doi:10.1021/bi700201w) (Pubitemid 46799163)
24. Liu, H. & Warshel, A. 2007b Origin of the temperature dependence of isotope effects in enzymatic reactions: the case of dihydrofolate reductase. J. Phys. Chem. B 111, 7852-7861. (doi:10.1021/jp070938f) (Pubitemid 47169697)
25. Masgrau, L. et al. 2006 Atomic description of an enzyme reaction dominated by proton tunneling. Science 312, 237-241. (doi:10.1126/science. 1126002)
26. Masgrau, L., Ranaghan, K. E., Scrutton, N. S., Mulholland, A. J. & Sutcliffe, M. J. 2007 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. (doi:10. 1021/jp067898k) (Pubitemid 46543293)
27. Nunez, S., Tresadern, G., Hillier, I. H. & Burton, N. A. 2006 An analysis of reaction pathways for proton tunnelling in methylamine dehydrogenase. Phil. Trans. R. Soc. B 361, 1387. (doi:10.1098/rstb.2006.1867) (Pubitemid 44338499)
28. Olsson, M. H., Mavri, J. & Warshel, A. 2006a Transition state theory can be used in studies of enzyme catalysis: lessons from simulations of tunnelling and dynamical effects in lipoxygenase and other systems. Phil. Trans. R. Soc. B 361, 1417-1432. (doi:10.1098/rstb.2006.1880) (Pubitemid 44338501)
29. Olsson, M. H., Parson, W. W. & Warshel, A. 2006b Dynamical contributions to enzyme catalysis: critical tests of a popular hypothesis. Chem. Rev. 106, 1737-1756. (doi:10.1021/cr040427e) (Pubitemid 43792778)
30. Pang, J., Pu, J., Gao, J., Truhlar, D. G. & Allemann, R. K. 2006 Hydride transfer reaction catalyzed by hyperthermo-philic 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. (doi:10.1021/ja061585l) (Pubitemid 43945743)
31. Pang, J., Hay, S., Scrutton, N. S. & Sutcliffe, M. J. 2008 Deep tunneling dominates the biologically important hydride transfer reaction from NADH to FMN in morphinone reductase. J. Am. Chem. Soc. 130, 7092-7097. (doi:10. 1021/ja800471f) (Pubitemid 351770152)
32. Pu, J., Gao, J. & Truhlar, D. G. 2006 Multidimensional tunneling, recrossing, and the transmission coefficient for enzymatic reactions. Chem. Rev. 106, 3140-3169. (doi:10. 1021/cr050308e) (Pubitemid 44376930)
33. Sutcliffe, M. J. & Scrutton, N. S. 2006 Computational studies of enzyme mechanism: linking theory with experiment in the analysis of enzymic H-tunnelling. Phys. Chem. Chem. Phys. 8, 4510-4516. (doi:10.1039/b609622k)
34. Tejero, I., Garcia-Viloca, M., Gonzalez-Lafont, A., Lluch, J. M. & York, D. M. 2006 Enzyme dynamics and tunneling enhanced by compression in the hydrogen abstraction catalyzed by soybean lipoxygenase-1. J. Phys. Chem. B 110, 24 708-24 719. (doi:10.1021/jp066263i) (Pubitemid 46065776)
35. Truhlar, D. G., Isaacson, A. D. & Garret, B. C. 1985 Generalized transition state theory. In Theory of chemical reaction dynamics, vol. IV (ed. M. Baer), pp. 65-136. Boca Raton, FL: CRC Press.
36. Truhlar, D. G., Gao, J. L., Garcia-Viloca, M., Alhambra, C., Corchado, J., Sanchez, M. L. & Poulsen, T. D. 2004 Ensemble-averaged variational transition state theory with optimized multidimensional tunneling for enzyme kinetics and other condensed-phase reactions. Int. J. Quant. Chem. 100, 1136-1152. (doi:10.1002/qua.20205) (Pubitemid 40748707)
37. Wand, A. J. 2001 Dynamic activation of protein function: a view emerging from NMR spectroscopy. Nat. Struct. Biol. 8, 926-931. (doi:10.1038/nsb1101-926) (Pubitemid 33032359)
38. Warshel, A. 1998 Electrostatic origin of the catalytic power of enzymes and the role of preorganized active sites. J. Biol. Chem. 273, 27 035-27 038. (doi:10.1074/jbc.273.42.27035) (Pubitemid 28500403)
39. Wong, K. F., Watney, J. B. & Hammes-Schiffer, S. 2004 Analysis of electrostatics and correlated motions for hydride transfer in dihydrofolate reductase. J. Phys. Chem. B 108, 12 231-12 241. (doi:10.1021/jp048565v)
40. Yon, J. M., Perahia, D. & Ghelis, C. 1998 Conformational dynamics and enzyme activity. Biochimie 80, 33-42. (doi:10.1016/S0300-9084(98)80054-0) (Pubitemid 28211651)