Incorporation of hydrostatic pressure into models of hydrogen tunneling highlights a role for pressure-modulated promoting vibrations

Biochemistry

Volumn 47, Issue 37, 2008, Pages 9880-9887

  Hay, Sam ^a   Scrutton, Nigel S ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FLUID MECHANICS; HYDRAULICS; HYDRODYNAMICS; HYDROGEN; HYDROSTATIC PRESSURE; ISOTOPES; LATTICE VIBRATIONS; NONMETALS; TUNNELING (EXCAVATION); VIBRATIONS (MECHANICAL);

ATOMIC FLUCTUATIONS; CHLORANIL; COMBINED EFFECTS; CRYSTAL VIOLET; DATA SETS; FITTING FUNCTIONS; GENERALIZED EXPRESSION; HYDROGEN-TRANSFER REACTIONS; KINETIC ISOTOPE EFFECTS; MORPHINONE REDUCTASE; NUCLEAR QUANTUM MECHANICAL EFFECTS; PRESSURE DEPENDENCE; REACTION COORDINATE; SENSITIVE PROBE; TEMPERATURE-DEPENDENT; TRANSFER REACTIONS; TUNNELING DISTANCE;

EXCAVATION;

CHLORANIL; CRYSTAL VIOLET; HYDROGEN; MORPHINE; OXIDOREDUCTASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE;

ARTICLE; CHEMICAL REACTION; HYDROSTATIC PRESSURE; ISOTOPE ANALYSIS; MOLECULAR PROBE; PRIORITY JOURNAL; PROTON TRANSPORT; QUANTUM MECHANICS; REDUCTION; TEMPERATURE SENSITIVITY; VIBRATION;

BACTERIAL PROTEINS; CHLORANIL; GENTIAN VIOLET; HYDROGEN; HYDROSTATIC PRESSURE; KINETICS; NAD; OXIDOREDUCTASES; TEMPERATURE; THERMODYNAMICS; VIBRATION;

EID: 51849095467     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi8005972     Document Type: Article

References (49)

1. Yon, J. M., Perahia, D., and Ghelis, C. (1998) Conformational dynamics and enzyme activity. Biochimie 80, 33-42.
2. Henzler-Wildman, K., and Kern, D. (2007) Dynamic personalities of proteins. Nature 450, 964-972.
3. Antoniou, D., and Schwartz, S. D. (1997) Large kinetic isotope effects in enzymatic proton transfer and the role of substrate oscillations. Proc. Natl. Acad. Sci. U.S.A. 94, 12360-12365.
4. Masgrau, L., Roujeinikova, A., Johannissen, L. O., Hothi, P., Basran, J., Ranaghan, K. E., Mulholland, A. J., Sutcliffe, M. J., Scrutton, N. S., and Leys, D. (2006) Atomic description of an enzyme reaction dominated by proton tunneling. Science 312, 237-241.
5. Caratzoulas, S., Mincer, J. S., and 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.
6. Hay, S., Sutcliffe, M. J., and Scrutton, N. S. (2007) Promoting motions in enzyme catalysis probed by pressure studies of kinetic isotope effects. Proc. Natl. Acad. Sci. U.S.A. 104, 507-512.
7. Johannissen, L. O., Hay, S., Scrutton, N. S., and 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.
8. Knapp, M. J., Rickert, K., and 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.
9. Antoniou, D., and Schwartz, S. D. (2001) Internal enzyme motions as a source of catalytic activity: Rate-promoting vibrations and hydrogen tunneling. J. Phys. Chem. B 105, 5553-5558.
10. Bruno, W. J., and Bialek, W. (1992) Vibrationally Enhanced Tunneling as a Mechanism for Enzymatic Hydrogen Transfer. Biophys. J. 63, 689-699.
11. Kuznetsov, A. M., and Ulstrup, J. (1999) Proton and hydrogen atom tunnelling in hydrolytic and redox enzyme catalysis. Can. J. Chem. 77, 1085-1096.
12. Borgis, D., and Hynes, J. T. (1996) Curve crossing formulation for proton transfer reactions in solution. J. Phys. Chem. 100, 1118-1128.
13. Mincer, J. S., and Schwartz, S. D. (2004) Rate-promoting vibrations and coupled hydrogen-electron transfer reactions in the condensed phase: A model for enzymatic catalysis. J. Chem. Phys. 120, 7755-7760.
14. Basran, J., Sutcliffe, M. J., and Scrutton, N. S. (1999) Enzymatic H-transfer requires vibration-driven extreme tunneling. Biochemistry 38, 3218-3222.
15. Kohen, A., Cannio, R., Bartolucci, S., and Klinman, J. P. (1999) Enzyme dynamics and hydrogen tunnelling in a thermophilic alcohol dehydrogenase. Nature 399, 496-499.
16. Maglia, G., and Allemann, R. K. (2003) Evidence for environmentally coupled hydrogen tunneling during dihydrofolate reductase catalysis. J. Am. Chem. Soc. 125, 13372-13373.
17. Knapp, M. J., and Klinman, J. P. (2002) Environmentally coupled hydrogen tunneling: Linking catalysis to dynamics. Eur. J. Biochem. 269, 3113-3121.
18. Isaacs, N. S., Javaid, K., and Rannala, E. (1978) Reactions at High-Pressure. 5. Effect of Pressure on Some Primary Kinetic Isotope Effects. J. Chem. Soc., Perkin Trans. 2, 709-711.
19. Isaacs, N. S. (1984) in Isotope Effects in Organic Chemistry (Buncel, E., and Lee, C. C. Eds.) pp 67-105, Elsevier, London.
20. Isaacs, N. S., Javaid, K., and Rannala, E. (1977) Pressure Effects on Proton Tunnelling. Nature 268, 372-372.
21. Northrop, D. B. (2006) Unusual origins of isotope effects in enzyme-catalysed reactions. Philos. Trans. R. Soc. London, Ser. B 361, 1341-1349.
22. Northrop, D. B. (2002) Effects of high pressure on enzymatic activity. Biochim. Biophys. Acta 1595, 71-79.
23. Gladstone, S., Laidler, K. J., and Eyring, H. (1941) The theory of rate processes, McGraw-Hill, New York.
24. Northrop, D. B. (1999) Effects of high pressure on isotope effects and hydrogen tunneling. J. Am. Chem. Soc. 121, 3521-3524.
25. Masson, P., and Balny, C. (2005) Linear and non-linear pressure dependence of enzyme catalytic parameters. Biochim. Biophys. Acta 1724, 440-450.
26. Bell, R. (1980) The Tunnel Effect in Chemistry, Chapman % Hall, London.
27. Masgrau, L., Basran, J., Hothi, P., Sutcliffe, M. J., and Scrutton, N. S. (2004) Hydrogen tunneling in quinoproteins. Arch. Biochem. Biophys. 428, 41-51.
28. Dutton, P. L., Munro, A. W., Scrutton, N. S., and Sutcliffe, M. J. (2006) Introduction. Quantum catalysis in enzymes: Beyond the transition state theory paradigm. Philos. Trans. R. Soc. London, Ser. B 361, 1293-1294.
29. Marcus, R. A. (1956) Theory of Oxidation-Reduction Reactions Involving Electron Transfer. J. Chem. Phys. 24, 966-978.
30. Marcus, R. A., and Sutin, N. (1985) Electron Transfers in Chemistry and Biology. Biochim. Biophys. Acta 811, 265-322.
31. Tejero, I., Garcia-Viloca, M., Gonzalez-Lafont, A., Lluch, J. M., and 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, 24708-24719.
32. Pang, J., Hay, S., Scrutton, N. S., and 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.
33. Miyashita, O., and Go, N. (1999) Pressure dependence of protein electron transfer reactions: Theory and simulation. J. Phys. Chem. B 103, 562-571.
34. Moser, C. C., Keske, J. M., Warncke, K., Farid, R. S., and Dutton, P. L. (1992) Nature of Biological Electron Transfer. Nature 355, 796-802.
35. Kundrot, C. E., and Richards, F. M. (1987) Crystal Structure of Hen Egg-White Lysozyme at a Hydrostatic Pressure of 1000 atm. J. Mol. Biol. 193, 157-170.
36. Hermes, J. D., Morrical, S. W., Oleary, M. H., and Cleland, W. W. (1984) Variation of Transition-State Structure as a Function of the Nucleotide in Reactions Catalyzed by Dehydrogenases. 2. Formate Dehydrogenase. Biochemistry 23, 5479-5488.
37. Scharschmidt, M., Fisher, M. A., and Cleland, W. W. (1984) Variation of Transition-State Structure as a Function of the Nucleotide in Reactions Catalyzed by Dehydrogenases. 1. Liver Alcohol Dehydrogenase with Benzyl Alcohol and Yeast Aldehyde Dehydrogenase with Benzaldehyde. Biochemistry 23, 5471-5478.
38. Marcus, R. A. (2006) Summarizing lecture: Factors influencing enzymatic H-transfers, analysis of nuclear tunnelling isotope effects and thermodynamic versus specific effects. Philos. Trans. R. Soc. London, Ser. B 361, 1445-1455.
39. Park, H., Girdaukas, G. G., and Northrop, D. B. (2006) Effect of pressure on a heavy-atom isotope effect of yeast alcohol dehydrogenase. J. Am. Chem. Soc. 128, 1868-1872.
40. Meyer, M. P., and Klinman, J. P. (2005) Modeling temperature dependent kinetic isotope effects for hydrogen transfer in a series of soybean lipoxygenase mutants: The effect of anharmonicity upon transfer distance. Chem. Phys. 319, 283-296.
41. Ulstrup, J., and Jortner, J. (1975) Effect of Intramolecular Quantum Modes on Free-Energy Relationships for Electron-Transfer Reactions. J. Chem. Phys. 63, 4358-4368.
42. Meyer, M. P., Tomchick, D. R., and Klinman, J. P. (2008) Enzyme structure and dynamics affect hydrogen tunneling: The impact of a remote side chain (1553) in soybean lipoxygenase-1. Proc. Natl. Acad. Sci. U.S.A. 105, 1146-1151.
43. Hatcher, E., Soudackov, A. V., and Hammes-Schiffer, S. (2007) Proton-coupled electron transfer in soybean lipoxygenase: Dynamical behavior and temperature dependence of kinetic isotope effects. J. Am. Chem. Soc. 129, 187-196.
44. Hatcher, E., Soudackov, A., and Hammes-Schiffer, S. (2005) Nonadiabatic proton-coupled electron transfer reactions: Impact of donor-acceptor vibrations, reorganization energies, and couplings on dynamics and rates. J. Phys. Chem. B 109, 18565-18574.
45. Lucazeau, G. (2003) Effect of pressure and temperature on Raman spectra of solids: anharmonicity. J. Raman Spectrosc. 34, 478-496.
46. Benson, A. M., and Drickamer, H. G. (1957) Stretching Vibrations in Condensed Systems:Especially Bonds Containing Hydrogen. J. Chem. Phys. 27, 1164-1174.
47. Yenice, K. M., and Lee, S. A. (1992) Raman pectroscopy of Potassium Selenate at High ressure. J. Raman Spectrosc. 23, 299-302.
48. Gekko, K. (2002) Compressibility gives new insight into protein dynamics and enzyme function. Biochim. Biophys. Acta 1595, 382-386.
49. Cooper, A. (1976) Thermodynamic Fluctuations in Protein Molecules. Proc. Natl. Acad. Sci. U.S.A. 73, 2740-2741.